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    The hierarchy of root branching order determines bacterial composition, microbial carrying capacity and microbial filtering

    1.Vandenkoornhuyse, P., Quaiser, A., Duhamel, M., Le Van, A. & Dufresne, A. The importance of the microbiome of the plant holobiont. N. Phytol. 206, 1196–1206 (2015).Article 

    Google Scholar 
    2.Feng, H. et al. Identification of chemotaxis compounds in root exudates and their sensing chemoreceptors in plant-growth-promoting Rhizobacteria Bacillus amyloliquefaciens SQR9. Mol. Plant Microbe Interact. 31, 995–1005 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Dennis, P. G., Miller, A. J. & Hirsch, P. R. Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol. Ecol. 72, 313–327 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    4.Walker, T. S., Bais, H. P., Grotewold, E. & Vivanco, J. M. Root exudation and rhizosphere biology. Plant Physiol. 132, 44 (2003).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Zhalnina, K. et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat. Microbiol. 3, 470–480 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Schreiter, S. et al. Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front. Microbiol. 5, 144 (2014).8.Zhang, N. et al. Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374, 689–700 (2014).CAS 
    Article 

    Google Scholar 
    9.Yang, C.-H. & Crowley, D. E. Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl. Environ. Microbiol. 66, 345 (2000).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.DeAngelis, K. M. et al. Selective progressive response of soil microbial community to wild oat roots. ISME J. 3, 168–178 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    11.Peiffer, J. A. et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl Acad. Sci. USA 110, 6548 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    12.Shi, S. et al. Successional trajectories of rhizosphere bacterial communities over consecutive seasons. mBio 6, e00746–00715 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    13.Lu, T. et al. Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome 6, 231 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Mei, C. & Flinn, B. S. The use of beneficial microbial endophytes for plant biomass and stress tolerance improvement. Recent Pat. Biotechnol. 4, 81–95 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    15.Hijri, M. Analysis of a large dataset of mycorrhiza inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26, 209–214 (2016).PubMed 
    Article 

    Google Scholar 
    16.Waschkies, C., Schropp, A. & Marschner, H. Relations between grapevine replant disease and root colonization of grapevine (Vitis sp.) by fluorescent pseudomonads and endomycorrhizal fungi. Plant Soil 162, 219–227 (1994).Article 

    Google Scholar 
    17.Benizri, E. et al. Replant diseases: bacterial community structure and diversity in peach rhizosphere as determined by metabolic and genetic fingerprinting. Soil Biol. Biochem. 37, 1738–1746 (2005).CAS 
    Article 

    Google Scholar 
    18.Pankhurst, C. E. et al. Management practices to improve soil health and reduce the effects of detrimental soil biota associated with yield decline of sugarcane in Queensland, Australia. Soil Tillage Res. 72, 125–137 (2003).Article 

    Google Scholar 
    19.Fitzpatrick, C. R. et al. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc. Natl Acad. Sci. USA 115, E1157 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    20.Zhang, Y. et al. Huanglongbing impairs the rhizosphere-to-rhizoplane enrichment process of the citrus root-associated microbiome. Microbiome 5, 97 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Edwards, J. et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl Acad. Sci. USA 112, E911 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    22.Hu, L. et al. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 2738 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    23.Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.McCormack, M. L. et al. Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. N. Phytol. 207, 505–518 (2015).Article 

    Google Scholar 
    25.Pregitzer, K. S. et al. Fine root architecture of nine North American trees. Ecol. Monogr. 72, 293–309 (2002).Article 

    Google Scholar 
    26.Holdaway, R. J., Richardson, S. J., Dickie, I. A., Peltzer, D. A. & Coomes, D. A. Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. J. Ecol. 99, 954–963 (2011).Article 

    Google Scholar 
    27.Fitter, A. H. Morphometric analysis of root systems: application of the technique and influence of soil fertility on root system development in two herbaceous species. Plant Cell Environ. 5, 313–322 (1982).
    Google Scholar 
    28.Valenzuela-Estrada, L. R., Vera-Caraballo, V., Ruth, L. E. & Eissenstat, D. M. Root anatomy, morphology, and longevity among root orders in Vaccinium corymbosum (Ericaceae). Am. J. Bot. 95, 1506–1514 (2008).PubMed 
    Article 

    Google Scholar 
    29.Hishi, T. Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions. J. For. Res. 12, 126–133 (2007).Article 

    Google Scholar 
    30.Guo, D. et al. Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. N. Phytol. 180, 673–683 (2008).Article 

    Google Scholar 
    31.Makita, N. et al. Fine root morphological traits determine variation in root respiration of Quercus serrata. Tree Physiol. 29, 579–585 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Guo, D., Mitchell, R. J., Withington, J. M., Fan, P.-P. & Hendricks, J. J. Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. J. Ecol. 96, 737–745 (2008).CAS 
    Article 

    Google Scholar 
    33.Gu, J., Yu, S., Sun, Y., Wang, Z. & Guo, D. Influence of root structure on root survivorship: an analysis of 18 tree species using a minirhizotron method. Ecol. Res. 26, 755–762 (2011).Article 

    Google Scholar 
    34.Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Tibbett, M. & Sanders, F. E. Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality. Ann. Bot. 89, 783–789 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Sanders, F. E. & Tinker, P. B. Phosphate flow into mycorrhizal roots. Pestic. Sci. 4, 385–395 (1973).CAS 
    Article 

    Google Scholar 
    37.Hodge, A. & Storer, K. Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386, 1–19 (2015).CAS 
    Article 

    Google Scholar 
    38.Bending, G. D. & Read, D. J. The structure and function of the vegetative mycelium of ectomycorrhizal plants. N. Phytol. 130, 401–409 (1995).CAS 
    Article 

    Google Scholar 
    39.Chen, W. et al. Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. Proc. Natl Acad. Sci. USA 113, 8741 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    40.Gui, H., Hyde, K., Xu, J. & Mortimer, P. Arbuscular mycorrhiza enhance the rate of litter decomposition while inhibiting soil microbial community development. Sci. Rep. 7, 42184–42184 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Svenningsen, N. B. et al. Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J. 12, 1296–1307 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Olsson, P. A. & Wallander, H. Interactions between ectomycorrhizal fungi and the bacterial community in soils amended with various primary minerals. FEMS Microbiol. Ecol. 27, 195–205 (1998).CAS 
    Article 

    Google Scholar 
    43.Hestrin, R., Hammer, E. C., Mueller, C. W. & Lehmann, J. Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun. Biol. 2, 233 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    44.Garbaye, J. Helper bacteria: a new dimension to the mycorrhizal symbiosis. N. Phytol. 128, 197–210 (1994).Article 

    Google Scholar 
    45.Phillips, R. P., Brzostek, E. & Midgley, M. G. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. N. Phytol. 199, 41–51 (2013).CAS 
    Article 

    Google Scholar 
    46.Cornelissen, J., Aerts, R., Cerabolini, B., Werger, M. & van der Heijden, M. Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129, 611–619 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Reich, P. B. et al. Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol. Lett. 8, 811–818 (2005).Article 

    Google Scholar 
    48.Minerovic, A. J., Valverde-Barrantes, O. J. & Blackwood, C. B. Physical and microbial mechanisms of decomposition vary in importance among root orders and tree species with differing chemical and morphological traits. Soil Biol. Biochem. 124, 142–149 (2018).CAS 
    Article 

    Google Scholar 
    49.Fan, P. & Guo, D. Slow decomposition of lower order roots: a key mechanism of root carbon and nutrient retention in the soil. Oecologia 163, 509–515 (2010).PubMed 
    Article 

    Google Scholar 
    50.Segal, E., Kushnir, T., Mualem, Y. & Shani, U. Water uptake and hydraulics of the root hair rhizosphere. Vadose Zone J. 7, 1027–1034 (2008).Article 

    Google Scholar 
    51.Gordon, W. S. & Jackson, R. B. Nutrient concentrations in fine roots. Ecology 81, 275–280 (2000).Article 

    Google Scholar 
    52.Ma, Z. et al. Evolutionary history resolves global organization of root functional traits. Nature 555, 94–97 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Yates, C. F. et al. Tree‐induced alterations to soil properties and rhizoplane‐associated bacteria following 23 years in a common garden. Plant Soil, https://doi.org/10.1007/s11104-021-04846-8 (2021).54.Fierer, N., Bradford, M. A. & Jackson, R. B. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364 (2007).Article 
    PubMed 

    Google Scholar 
    55.Wang, N., Wang, C. & Quan, X. Variations in fine root dynamics and turnover rates in five forest types in northeastern China. J. Forestry Res. 31, 871–884 (2020).CAS 
    Article 

    Google Scholar 
    56.Kong, D. et al. Nonlinearity of root trait relationships and the root economics spectrum. Nat. Commun. 10, 2203 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    57.Jia, S., Wang, Z., Li, X., Zhang, X. & McLaughlin, N. B. Effect of nitrogen fertilizer, root branch order and temperature on respiration and tissue N concentration of fine roots in Larix gmelinii and Fraxinus mandshurica. Tree Physiol. 31, 718–726 (2011).PubMed 
    Article 

    Google Scholar 
    58.Lavely, E. K. et al. On characterizing root function in perennial horticultural crops. Am. J. Botany, https://doi.org/10.1002/ajb2.1530 (2020).59.Iffis, B., St-Arnaud, M. & Hijri, M. Bacteria associated with arbuscular mycorrhizal fungi within roots of plants growing in a soil highly contaminated with aliphatic and aromatic petroleum hydrocarbons. FEMS Microbiol. Lett. 358, 44–54 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    60.Toljander, J. F., Lindahl, B. D., Paul, L. R., Elfstrand, M. & Finlay, R. D. Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol. Ecol. 61, 295–304 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    61.McCormack, M., Adams, T. S., Smithwick, E. A. H. & Eissenstat, D. M. Predicting fine root lifespan from plant functional traits in temperate trees. N. Phytol. 195, 823–831 (2012).Article 

    Google Scholar 
    62.Freschet, G. T. et al. Climate, soil and plant functional types as drivers of global fine-root trait variation. J. Ecol. 105, 1182–1196 (2017).Article 

    Google Scholar 
    63.Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    64.Apprill, A., McNally, S., Parsons, R. J. & Weber, L. K. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75, 129–137 (2015).Article 

    Google Scholar 
    65.Trexler, R. V. & Bell, T. H. Testing sustained soil-to-soil contact as an approach for limiting the abiotic influence of source soils during experimental microbiome transfer. FEMS Microbiol. Lett. 366, https://doi.org/10.1093/femsle/fnz228 (2019).66.Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    67.Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).CAS 
    Article 

    Google Scholar 
    69.DeSantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    70.McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLOS ONE 8, e61217 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Bressan, M. et al. A rapid flow cytometry method to assess bacterial abundance in agricultural soil. Appl. Soil Ecol. 88, 60–68 (2015).Article 

    Google Scholar 
    72.Oksanen, J. et al. Vegan: community ecology package. R. Package Version 2. 2-1 2, 1–2 (2015).
    Google Scholar 
    73.Bisanz, J. E. MicrobeR: Handy functions for microbiome analysis in R. (2019).74.R Foundation for Statistical Computing. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012). More

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    Microbial evolution and transitions along the parasite–mutualist continuum

    1.Garcia, J. R. & Gerardo, N. M. The symbiont side of symbiosis: do microbes really benefit? Front. Microbiol. 5, 510 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Law, R. & Dieckmann, U. Symbiosis through exploitation and the merger of lineages in evolution. Proc. Biol. Sci. 265, 1245–1253 (1998).PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    3.Keeling, P. J. & McCutcheon, J. P. Endosymbiosis: the feeling is not mutual. J. Theor. Biol. 434, 75–79 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Wooldridge, S. A. Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? BioEssays 32, 615–625 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Mushegian, A. A. & Ebert, D. Rethinking ‘mutualism’ in diverse host-symbiont communities. BioEssays 38, 100–108 (2016).PubMed 
    Article 

    Google Scholar 
    6.Mathis, K. A. & Bronstein, J. L. Our current understanding of commensalism. Ann. Rev. Ecol. Evol. Syst. 51, 167–189 (2020).Article 

    Google Scholar 
    7.Ewald, P. W. Transmission modes and evolution of the parasitism-mutualism continuum. Ann. N. Y. Acad. Sci. 503, 295–306 (1987).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Bronstein, J. L. Conditional outcomes in mutualistic interactions. Trends Ecol. Evol. 9, 214–217 (1994).CAS 
    PubMed 
    Article 

    Google Scholar 
    9.Schu, M. G. & Schrallhammer, M. Cultivation conditions can cause a shift from mutualistic to parasitic behavior in the symbiosis between Paramecium and its bacterial symbiont Caedibacter taeniospiralis. Curr. Microbiol. 75, 1099–1102 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Osman, E. O. et al. Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities. Microbiome 8, 8 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Kümmerli, R., Jiricny, N., Clarke, L. S., West, S. A. & Griffin, A. S. Phenotypic plasticity of a cooperative behaviour in bacteria. J. Evol. Biol. 22, 589–598 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Kumamoto, C. A. Niche-specific gene expression during C. albicans infection. Curr. Opin. Microbiol. 11, 325–330 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    13.Thrall, P. H., Hochberg, M. E., Burdon, J. J. & Bever, J. D. Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol. Evol. 22, 120–126 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Chamberlain, S. A., Bronstein, J. L. & Rudgers, J. A. How context dependent are species interactions? Ecol. Lett. 17, 881–890 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Sachs, J. L., Skophammer, R. G. & Regus, J. U. Evolutionary transitions in bacterial symbiosis. Proc. Natl Acad. Sci. USA 108 (Suppl. 2), 10800–10807 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Hosokawa, T. et al. Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations. Nat. Microbiol. 1, 1–7 (2016).Article 
    CAS 

    Google Scholar 
    17.Gupta, A. & Nair, S. Dynamics of insect–microbiome interaction influence host and microbial symbiont. Front. Microbiol. 11, 1357 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Lutzoni, F. & Pagel, M. Accelerated evolution as a consequence of transitions to mutualism. Proc. Natl Acad. Sci. USA 94, 11422–11427 (1997).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Kaltenpoth, M. et al. Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis. Proc. Natl Acad. Sci. USA 111, 6359–6364 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Manzano-Marı́n, A. et al. Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems. ISME J. 14, 259–273 (2020).Article 
    CAS 

    Google Scholar 
    21.Miyauchi, S. et al. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nat. Commun. 11, 5125 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.McFall-Ngai, M. J. The importance of microbes in animal development: lessons from the squid-Vibrio symbiosis. Annu. Rev. Microbiol. 68, 177–194 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Brown, S. P., Cornforth, D. M. & Mideo, N. Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol. 20, 336–342 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Fisher, R. M., Henry, L. M., Cornwallis, C. K., Kiers, E. T. & West, S. A. The evolution of host-symbiont dependence. Nat. Commun. 8, 15973 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.McDowell, J. M. Genomes of obligate plant pathogens reveal adaptations for obligate parasitism. Proc. Natl Acad. Sci. USA 108, 8921–8922 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Wilson, B. A. & Salyers, A. A. Is the evolution of bacterial pathogens an out-of-body experience? Trends Microbiol. 11, 347–350 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. The evolution of cooperation. Q. Rev. Biol. 79, 135–160 (2004).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Bull, J. J. & Rice, W. R. Distinguishing mechanisms for the evolution of co-operation. J. Theor. Biol. 149, 63–74 (1991).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Sachs, J. L., Skophammer, R. G., Bansal, N. & Stajich, J. E. Evolutionary origins and diversification of proteobacterial mutualists. Proc. Biol. Sci. 281, 20132146 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    30.Duron, O. et al. The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii. PLoS Pathog. 11, e1004892 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    31.Clayton, A. L. et al. A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insect–bacterial symbioses. PLoS Genet. 8, e1002990 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.West, S. A., Kiers, E. T., Simms, E. L. & Denison, R. F. Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc. Biol. Sci. 269, 685–694 (2002).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Sørensen, M. E. S. et al. The role of exploitation in the establishment of mutualistic microbial symbioses. FEMS Microbiol. Lett. 366, fnz148 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971).Article 

    Google Scholar 
    35.Frederickson, M. E. Mutualisms are not on the verge of breakdown. Trends Ecol. Evol. 32, 727–734 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Mueller, U. G., Ishak, H., Lee, J. C., Sen, R. & Gutell, R. R. Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): a test of two symbiont-association models. Antonie Van Leeuwenhoek 98, 195–212 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Dietel, A.-K., Kaltenpoth, M. & Kost, C. Convergent evolution in intracellular elements: plasmids as model endosymbionts. Trends Microbiol. 26, 755–768 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Hurst, G. D. D. Extended genomes: symbiosis and evolution. Interface Focus. 7, 20170001 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Melnyk, R. A., Hossain, S. S. & Haney, C. H. Convergent gain and loss of genomic islands drive lifestyle changes in plant-associated Pseudomonas. ISME J. 13, 1575–1588 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.King, K. C. et al. Rapid evolution of microbe-mediated protection against pathogens in a worm host. ISME J. 10, 1915–1924 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Shapiro, J. W. & Turner, P. E. Evolution of mutualism from parasitism in experimental virus populations. Evolution 72, 707–712 (2018).PubMed 
    Article 

    Google Scholar 
    42.Zhang, H. et al. A 2-kb mycovirus converts a pathogenic fungus into a beneficial endophyte for brassica protection and yield enhancement. Mol. Plant. 13, 1420–1433 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    43.Tso, G. H. W. et al. Experimental evolution of a fungal pathogen into a gut symbiont. Science 362, 589–595 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Harrison, E., Guymer, D., Spiers, A. J., Paterson, S. & Brockhurst, M. A. Parallel compensatory evolution stabilizes plasmids across the parasitism-mutualism continuum. Curr. Biol. 25, 2034–2039 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Porter, S. S., Faber-Hammond, J., Montoya, A. P., Friesen, M. L. & Sackos, C. Dynamic genomic architecture of mutualistic cooperation in a wild population of Mesorhizobium. ISME J. 13, 301–315 (2019).PubMed 
    Article 

    Google Scholar 
    46.Herrera, P. et al. Molecular causes of an evolutionary shift along the parasitism–mutualism continuum in a bacterial symbiont. Proc. Natl Acad. Sci. USA 117, 21658–21666 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Li, E. et al. Rapid evolution of bacterial mutualism in the plant rhizosphere. Preprint at bioRxiv https://doi.org/10.1101/2020.12.07.414607 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    48.Pankey, M. S. et al. Host-selected mutations converging on a global regulator drive an adaptive leap towards symbiosis in bacteria. eLife 6, e24414 (2017).Article 

    Google Scholar 
    49.Jansen, G. et al. Evolutionary transition from pathogenicity to commensalism: global regulator mutations mediate fitness gains through virulence attenuation. Mol. Biol. Evol. 32, 2883–2896 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Chain, P. S. G. et al. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl Acad. Sci. USA 101, 13826–13831 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    51.Hendry, T. A. et al. Ongoing transposon-mediated genome reduction in the luminous bacterial symbionts of deep-sea ceratioid anglerfishes. mBio 9, e01033-18 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Nygaard, S. et al. Reciprocal genomic evolution in the ant–fungus agricultural symbiosis. Nat. Commun. 7, 12233 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Bennett, G. M. & Moran, N. A. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc. Natl Acad. Sci. USA 112, 10169–10176 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    54.Gluck-Thaler, E. et al. Repeated gain and loss of a single gene modulates the evolution of vascular pathogen lifestyles. bioRxiv https://doi.org/10.1101/2020.04.24.058529 (2020).Article 

    Google Scholar 
    55.Arredondo-Alonso, S. et al. Plasmids shaped the recent emergence of the major nosocomial pathogen Enterococcus faecium. mBio 11, e03284-19 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Driscoll, T. P. et al. Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas. Preprint at bioRxiv https://doi.org/10.1101/2020.06.01.128066 (2020).Article 

    Google Scholar 
    57.Frantzeskakis, L. et al. Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen. BMC Genomics 19, 381 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    58.Savory, E. A. et al. Evolutionary transitions between beneficial and phytopathogenic Rhodococcus challenge disease management. eLife 6, e30925 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Barreto, H. C., Sousa, A. & Gordo, I. The landscape of adaptive evolution of a gut commensal bacteria in aging mice. Curr. Biol. 30, 1102–1109.e5 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    60.Parkhill, J. et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523–527 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    61.Deng, W. et al. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184, 4601–4611 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Achtman, M. et al. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl Acad. Sci. USA 96, 14043–14048 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Rasmussen, S. et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 163, 571–582 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Hinnebusch, B. J. et al. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296, 733–735 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    65.Lindler, L. E., Plano, G. V., Burland, V., Mayhew, G. F. & Blattner, F. R. Complete DNA sequence and detailed analysis of the Yersinia pestis KIM5 plasmid encoding murine toxin and capsular antigen. Infect. Immun. 66, 5731–5742 (1998).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Du, Y., Rosqvist, R. & Forsberg, Å. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70, 1453–1460 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    67.Sun, Y.-C., Jarrett, C. O., Bosio, C. F. & Hinnebusch, B. J. Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis. Cell Host Microbe 15, 578–586 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Ohnishi, M., Kurokawa, K. & Hayashi, T. Diversification of Escherichia coli genomes: are bacteriophages the major contributors? Trends Microbiol. 9, 481–485 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Franzin, F. M. & Sircili, M. P. Locus of enterocyte effacement: a pathogenicity island involved in the virulence of enteropathogenic and enterohemorragic Escherichia coli subjected to a complex network of gene regulation. Biomed. Res. Int. 2015, 534738 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    70.Brito, I. L. et al. Mobile genes in the human microbiome are structured from global to individual scales. Nature 535, 435–439 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Broaders, E., O’Brien, C., Gahan, C. G. M. & Marchesi, J. R. Evidence for plasmid-mediated salt tolerance in the human gut microbiome and potential mechanisms. FEMS Microbiol. Ecol. 92, fiw019 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    72.McCarthy, A. J. et al. Extensive horizontal gene transfer during Staphylococcus aureus co-colonization in vivo. Genome Biol. Evol. 6, 2697–2708 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Frazão, N., Sousa, A., Lässig, M. & Gordo, I. Horizontal gene transfer overrides mutation in Escherichia coli colonizing the mammalian gut. Proc. Natl Acad. Sci. USA 116, 17906–17915 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    74.Niehus, R., Mitri, S., Fletcher, A. G. & Foster, K. R. Migration and horizontal gene transfer divide microbial genomes into multiple niches. Nat. Commun. 6, 8924 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    75.Koonin, E. V. Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Res https://doi.org/10.12688/f1000research.8737.1 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    76.Nowack, E. C. M. et al. Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora. Proc. Natl Acad. Sci. USA 113, 12214–12219 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    77.Bordenstein, S. R. & Bordenstein, S. R. Eukaryotic association module in phage WO genomes from Wolbachia. Nat. Commun. 7, 13155 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Waterworth, S. C. et al. Horizontal gene transfer to a defensive symbiont with a reduced genome in a multipartite beetle microbiome. mBio 11, e02430-19 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    79.Ma, W., Dong, F. F. T., Stavrinides, J. & Guttman, D. S. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genet. 2, e209 (2006).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    80.Nikoh, N. et al. Evolutionary origin of insect–Wolbachia nutritional mutualism. Proc. Natl Acad. Sci. USA 111, 10257–10262 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    81.Sheppard, S. K., Guttman, D. S. & Fitzgerald, J. R. Population genomics of bacterial host adaptation. Nat. Rev. Genet. 19, 549–565 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    82.Day, T., Gandon, S., Lion, S. & Otto, S. P. On the evolutionary epidemiology of SARS-CoV-2. Curr. Biol. 30, R849–R857 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    83.Tardy, L., Giraudeau, M., Hill, G. E., McGraw, K. J. & Bonneaud, C. Contrasting evolution of virulence and replication rate in an emerging bacterial pathogen. Proc. Natl Acad. Sci. USA 116, 16927–16932 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    84.Alves, J. M. et al. Parallel adaptation of rabbit populations to myxoma virus. Science 363, 1319–1326 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    85.Kerr, P. J. Myxomatosis in Australia and Europe: a model for emerging infectious diseases. Antivir. Res. 93, 387–415 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    86.Longdon, B. et al. The causes and consequences of changes in virulence following pathogen host shifts. PLoS Pathog. 11, e1004728 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    87.van Boven, M. et al. Detecting emerging transmissibility of avian influenza virus in human households. PLoS Comput. Biol. 3, e145 (2007).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    88.Moses, A. S., Millar, J. A., Bonazzi, M., Beare, P. A. & Raghavan, R. Horizontally acquired biosynthesis genes boost Coxiella burnetii’s physiology. Front. Cell Infect. Microbiol. 7, 174 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    89.Flórez, L. V. et al. Antibiotic-producing symbionts dynamically transition between plant pathogenicity and insect-defensive mutualism. Nat. Commun. 8, 1–9 (2017).Article 

    Google Scholar 
    90.Anderson, R. M. & May, R. M. Coevolution of hosts and parasites. Parasitology 85, 411–426 (1982).PubMed 
    Article 

    Google Scholar 
    91.Ewald, P. W. Host-parasite relations, vectors, and the evolution of disease severity. Annu. Rev. Ecol. Syst. 14, 465–485 (1983).Article 

    Google Scholar 
    92.Bull, J. J. Perspective: Virulence. Evolution 48, 1423–1437 (1994).CAS 
    PubMed 

    Google Scholar 
    93.Rafaluk, C., Jansen, G., Schulenburg, H. & Joop, G. When experimental selection for virulence leads to loss of virulence. Trends Parasitol. 31, 426–434 (2015).PubMed 
    Article 

    Google Scholar 
    94.Alizon, S. & Van Baalen, M. Transmission-virulence trade-offs in vector-borne diseases. Theor. Popul. Biol. 74, 6–15 (2008).PubMed 
    Article 

    Google Scholar 
    95.Cressler, C. E., McLeod, D. V., Rozins, C., Hoogen, J. V. D. & Day, T. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology 143, 915–930 (2016).PubMed 
    Article 

    Google Scholar 
    96.Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).CAS 
    PubMed 
    Article 

    Google Scholar 
    97.Yamamura, N. Vertical transmission and evolution of mutualism from parasitism. Theor. Popul. Biol. 44, 95–109 (1993).Article 

    Google Scholar 
    98.Hall, J. P. J., Brockhurst, M. A., Dytham, C. & Harrison, E. The evolution of plasmid stability: are infectious transmission and compensatory evolution competing evolutionary trajectories? Plasmid 91, 90–95 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    99.Kiers, E. T. & Denison, R. F. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu. Rev. Ecol. Evol. Syst. 39, 215–236 (2008).Article 

    Google Scholar 
    100.Werner, G. D. A. et al. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. Proc. Natl Acad. Sci. USA 115, 5229–5234 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    101.Herre, E. A. et al. The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol. Evol. 14, 49–53 (1999).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    102.Nussbaumer, A. D., Fisher, C. R. & Bright, M. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441, 345–348 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    103.Dusi, E., Krenek, S., Petzoldt, T., Kaltz, O. & Berendonk, T. U. When enemies do not become friends: experimental evolution of heat-stress adaptation in a vertically transmitted parasite. Preprint at bioRxiv https://doi.org/10.1101/2020.01.23.917773 (2020).Article 

    Google Scholar 
    104.Engelstädter, J. & Hurst, G. D. D. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 40, 127–149 (2009).Article 

    Google Scholar 
    105.Fenton, A., Johnson, K. N., Brownlie, J. C. & Hurst, G. D. D. Solving the Wolbachia paradox: modeling the tripartite interaction between host, Wolbachia, and a natural enemy. Am. Nat. 178, 333–342 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    106.Zug, R. & Hammerstein, P. Evolution of reproductive parasites with direct fitness benefits. Heredity 120, 266–281 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    107.Drew, G. C., Frost, C. L. & Hurst, G. D. Reproductive parasitism and positive fitness effects of heritable microbes. in eLS https://onlinelibrary.wiley.com/doi/abs/10.1002/9780470015902.a0028327 (2019).108.Parratt, S. R. et al. Superparasitism drives heritable symbiont epidemiology and host sex ratio in a wasp. PLoS Pathog. 12, e1005629 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    109.Sachs, J. L. & Wilcox, T. P. A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc. Biol. Sci. 273, 425–429 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    110.Le Clec’h, W., Dittmer, J., Raimond, M., Bouchon, D. & Sicard, M. Phenotypic shift in Wolbachia virulence towards its native host across serial horizontal passages. Proc. Biol. Sci. 284, 20171076 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    111.Stewart, A. D., Logsdon, J. M. & Kelley, S. E. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59, 730–739 (2005).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    112.Rigaud, T., Souty-Grosset, C., Raimond, R., Mocquard, J.-P. & Juchault, P. Feminizing endocytobiosis in the terrestrial crustacean Armadilidium vulgare Latr. (isopoda) – recent acquisitions. Cell Res. 15, 259–273 (1991).
    Google Scholar 
    113.King, K. C. Defensive symbionts. Curr. Biol. 29, R78–R80 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    114.Flórez, L. V., Biedermann, P. H. W., Engl, T. & Kaltenpoth, M. Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat. Prod. Rep. 32, 904–936 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    115.Couret, J., Huynh-Griffin, L., Antolic-Soban, I., Acevedo-Gonzalez, T. S. & Gerardo, N. M. Even obligate symbioses show signs of ecological contingency: impacts of symbiosis for an invasive stinkbug are mediated by host plant context. Ecol. Evol. 9, 9087–9099 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    116.Ashby, B. & King, K. Friendly foes: the evolution of host protection by a parasite. Evol. Lett. 1, 211–221 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    117.Duron, O. Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. FEMS Microbiol. Ecol. 90, 184–194 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    118.Ferrari, J., Darby, A. C., Daniell, T. J., Godfray, H. C. J. & Douglas, A. E. Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol. Entomol. 29, 60–65 (2004).Article 

    Google Scholar 
    119.Oliver, K. M., Russell, J. A., Moran, N. A. & Hunter, M. S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA 100, 1803–1807 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    120.Polin, S., Simon, J.-C. & Outreman, Y. An ecological cost associated with protective symbionts of aphids. Ecol. Evol. 4, 826–830 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    121.Degnan, P. H., Yu, Y., Sisneros, N., Wing, R. A. & Moran, N. A. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc. Natl Acad. Sci. USA 106, 9063–9068 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    122.Weldon, S. R., Strand, M. R. & Oliver, K. M. Phage loss and the breakdown of a defensive symbiosis in aphids. Proc. Biol. Sci. 280, 20122103 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    123.Weeks, A. R., Turelli, M., Harcombe, W. R., Reynolds, K. T. & Hoffmann, A. A. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5, e114 (2007).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    124.Kwong, W. K., del Campo, J., Mathur, V., Vermeij, M. J. A. & Keeling, P. J. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature 568, 103–107 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    125.Tuovinen, V. et al. Two basidiomycete fungi in the cortex of wolf lichens. Curr. Biol. 29, 476–483.e5 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    126.Spribille, T. et al. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353, 488–492 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    127.Coyte, K. Z. & Rakoff-Nahoum, S. Understanding competition and cooperation within the mammalian gut microbiome. Curr. Biol. 29, R538–R544 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    128.Lopez-Medina, E. et al. Candida albicans inhibits Pseudomonas aeruginosa virulence through suppression of pyochelin and pyoverdine biosynthesis. PLoS Pathog. 11, e1005129 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    129.Harriott, M. M. & Noverr, M. C. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob. Agents Chemother. 53, 3914–3922 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    130.Diebel, L. N., Liberati, D. M., Diglio, C. A., Dulchavsky, S. A. & Brown, W. J. Synergistic effects of Candida and Escherichia coli on gut barrier function. J. Trauma. Acute Care Surg. 47, 1045 (1999).CAS 
    Article 

    Google Scholar 
    131.Barroso-Batista, J. et al. Specific eco-evolutionary contexts in the mouse gut reveal Escherichia coli metabolic versatility. Curr. Biol. 30, 1049–1062.e7 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    132.King, K. C., Stevens, E. & Drew, G. C. Microbiome: evolution in a world of interaction. Curr. Biol. 30, R265–R267 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    133.Zilber-Rosenberg, I. & Rosenberg, E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723–735 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    134.Douglas, A. E. & Werren, J. H. Holes in the hologenome: why host-microbe symbioses are not holobionts. mBio 7, e02099 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    135.Bakken, J. S. et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin. Gastroenterol. Hepatol. 9, 1044–1049 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    136.Bourtzis, K. et al. Harnessing mosquito–Wolbachia symbiosis for vector and disease control. Acta Tropica 132, S150–S163 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    137.O’Neill, S. L. in Dengue and Zika: Control and Antiviral Treatment Strategies (eds Hilgenfeld, R. & Vasudevan, S. G.) 355–360 (Springer, 2018).138.Nelson, P. G. & May, G. Coevolution between mutualists and parasites in symbiotic communities may lead to the evolution of lower virulence. Am. Nat. 190, 803–817 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    139.Nelson, P. & May, G. Defensive symbiosis and the evolution of virulence. Am. Nat. 196, 333–343 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    140.Ford, S. A. & King, K. C. Harnessing the power of defensive microbes: evolutionary implications in nature and disease control. PLoS Pathog. 12, e1005465 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    141.Nowak, M. A. & May, R. M. Superinfection and the evolution of parasite virulence. Proc. Biol. Sci. 255, 81–89 (1994).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    142.Alizon, S., de Roode, J. C. & Michalakis, Y. Multiple infections and the evolution of virulence. Ecol. Lett. 16, 556–567 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    143.Frank, S. A. Host–symbiont conflict over the mixing of symbiotic lineages. Proc. Biol. Sci. 263, 339–344 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    144.Ford, S. A., Kao, D., Williams, D. & King, K. C. Microbe-mediated host defence drives the evolution of reduced pathogen virulence. Nat. Commun. 7, 1–9 (2016).Article 
    CAS 

    Google Scholar 
    145.Engl, T. et al. Evolutionary stability of antibiotic protection in a defensive symbiosis. Proc. Natl Acad. Sci. USA 115, E2020–E2029 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    146.Foster, K. R., Schluter, J., Coyte, K. Z. & Rakoff-Nahoum, S. The evolution of the host microbiome as an ecosystem on a leash. Nature 548, 43–51 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    147.Schneider, D. S. & Ayres, J. S. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat. Rev. Immunol. 8, 889–895 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    148.Voges, M. J. E. E. E., Bai, Y., Schulze-Lefert, P. & Sattely, E. S. Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome. Proc. Natl Acad. Sci. USA 116, 12558–12565 (2019).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    149.Gandon, S. & Michalakis, Y. Evolution of parasite virulence against qualitative or quantitative host resistance. Proc. Biol. Sci. 267, 985–990 (2000).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    150.Best, A., White, A. & Boots, M. The coevolutionary implications of host tolerance. Evolution 68, 1426–1435 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    151.Bor, B. et al. Rapid evolution of decreased host susceptibility drives a stable relationship between ultrasmall parasite TM7x and its bacterial host. Proc. Natl Acad. Sci. USA 115, 12277–12282 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    152.Schulte, R. D., Makus, C., Hasert, B., Michiels, N. K. & Schulenburg, H. Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc. Natl Acad. Sci. USA 107, 7359–7364 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    153.Kerr, P. J. et al. Next step in the ongoing arms race between myxoma virus and wild rabbits in Australia is a novel disease phenotype. Proc. Natl Acad. Sci. USA 114, 9397–9402 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    154.Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. Host sanctions and the legume–rhizobium mutualism. Nature 425, 78–81 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    155.Frederickson, M. E. Rethinking mutualism stability: cheaters and the evolution of sanctions. Q. Rev. Biol. 88, 269–295 (2013).PubMed 
    Article 

    Google Scholar 
    156.Kiers, E. T. et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    157.Fitt, W. K. & Trench, R. K. The relation of diel patterns of cell division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. N. Phytol. 94, 421–432 (1983).Article 

    Google Scholar 
    158.Wilkerson, F. P., Kobayashi, D. & Muscatine, L. Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7, 29–36 (1988).Article 

    Google Scholar 
    159.Lowe, C. D., Minter, E. J., Cameron, D. D. & Brockhurst, M. A. Shining a light on exploitative host control in a photosynthetic endosymbiosis. Curr. Biol. 26, 207–211 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    160.Kodama, Y. & Fujishima, M. Symbiotic Chlorella variabilis incubated under constant dark conditions for 24 hours loses the ability to avoid digestion by host lysosomal enzymes in digestive vacuoles of host ciliate Paramecium bursaria. FEMS Microbiol. Ecol. 90, 946–955 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    161.Iwai, S., Fujita, K., Takanishi, Y. & Fukushi, K. Photosynthetic endosymbionts benefit from host’s phagotrophy, including predation on potential competitors. Curr. Biol. 29, 3114–3119.e3 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    162.Reisser, W. et al. Viruses distinguish symbiotic Chlorella spp. of Paramecium bursaria. Endocytobiosis Cell Res. 7, 245–251 (1991).
    Google Scholar 
    163.Ahmadjian, V. The lichen symbiosis. Ann. Botany 75, 101–102 (1993).
    Google Scholar 
    164.Wilson, C. G. & Sherman, P. W. Anciently asexual bdelloid rotifers escape lethal fungal parasites by drying up and blowing away. Science 327, 574–576 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    165.Matsuura, Y. et al. Recurrent symbiont recruitment from fungal parasites in cicadas. Proc. Natl Acad. Sci. USA 115, E5970–E5979 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    166.Bergstrom, C. T. & Lachmann, M. The Red King effect: when the slowest runner wins the coevolutionary race. Proc. Natl Acad. Sci. USA 100, 593–598 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    167.Veller, C., Hayward, L. K., Hilbe, C. & Nowak, M. A. The Red Queen and King in finite populations. Proc. Natl Acad. Sci. USA 114, E5396–E5405 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    168.Vigneron, A. et al. Insects recycle endosymbionts when the benefit is over. Curr. Biol. 24, 2267–2273 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    169.Baker, D. M., Freeman, C. J., Wong, J. C. Y., Fogel, M. L. & Knowlton, N. Climate change promotes parasitism in a coral symbiosis. ISME J. 12, 921–930 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    170.Hom, E. F. Y. & Murray, A. W. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345, 94–98 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    171.Hall, J. P. J. et al. Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects. Env. Microbiol. 17, 5008–5022 (2015).CAS 
    Article 

    Google Scholar 
    172.Banaszak, A. T., García Ramos, M. & Goulet, T. L. The symbiosis between the gastropod Strombus gigas and the dinoflagellate Symbiodinium: an ontogenic journey from mutualism to parasitism. J. Exp. Mar. Biol. Ecol. 449, 358–365 (2013).Article 

    Google Scholar 
    173.Nakazawa, T. & Katayama, N. Stage-specific parasitism by a mutualistic partner can increase the host abundance. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2020.602675 (2020).Article 

    Google Scholar 
    174.Wintermute, E. H. & Silver, P. A. Emergent cooperation in microbial metabolism. Mol. Syst. Biol. 6, 407 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    175.Yurtsev, E. A., Conwill, A. & Gore, J. Oscillatory dynamics in a bacterial cross-protection mutualism. Proc. Natl Acad. Sci. USA 113, 6236–6241 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    176.Hoek, T. A. et al. Resource availability modulates the cooperative and competitive nature of a microbial cross-feeding mutualism. PLoS Biol. 14, e1002540 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    177.Hillesland, K. L. & Stahl, D. A. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc. Natl Acad. Sci. USA 107, 2124–2129 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    178.Regus, J. U., Gano, K. A., Hollowell, A. C., Sofish, V. & Sachs, J. L. Lotus hosts delimit the mutualism–parasitism continuum of Bradyrhizobium. J. Evol. Biol. 28, 447–456 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    179.Hay, M. E. et al. Mutualisms and aquatic community structure: the enemy of my enemy is my friend. Annu. Rev. Ecol. Evol. Syst. 35, 175–197 (2004).Article 

    Google Scholar 
    180.Pike, V. L., Lythgoe, K. A. & King, K. C. On the diverse and opposing effects of nutrition on pathogen virulence. Proc. Biol. Sci. 286, 20191220 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    181.Corbin, C., Heyworth, E. R., Ferrari, J. & Hurst, G. D. D. Heritable symbionts in a world of varying temperature. Heredity 118, 10–20 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    182.Thomas, M. B. & Blanford, S. Thermal biology in insect-parasite interactions. Trends Ecol. Evol. 18, 344–350 (2003).Article 

    Google Scholar 
    183.Delor, I. & Cornelis, G. R. Role of Yersinia enterocolitica Yst toxin in experimental infection of young rabbits. Infect. Immun. 60, 4269–4277 (1992).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    184.Kouse, A. B., Righetti, F., Kortmann, J., Narberhaus, F. & Murphy, E. R. RNA-mediated thermoregulation of iron-acquisition genes in Shigella dysenteriae and pathogenic Escherichia coli. PLoS ONE 8, e63781 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    185.Kishimoto, M., Baird, A. H., Maruyama, S., Minagawa, J. & Takahashi, S. Loss of symbiont infectivity following thermal stress can be a factor limiting recovery from bleaching in cnidarians. ISME J. 14, 3149–3152 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    186.Zhang, B., Leonard, S. P., Li, Y. & Moran, N. A. Obligate bacterial endosymbionts limit thermal tolerance of insect host species. Proc. Natl Acad. Sci. USA 116, 24712–24718 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    187.Guay, J.-F., Boudreault, S., Michaud, D. & Cloutier, C. Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. J. Insect Physiol. 55, 919–926 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    188.Bensadia, F., Boudreault, S., Guay, J.-F., Michaud, D. & Cloutier, C. Aphid clonal resistance to a parasitoid fails under heat stress. J. Insect Physiol. 52, 146–157 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    189.Vorburger, C. & Gouskov, A. Only helpful when required: a longevity cost of harbouring defensive symbionts. J. Evol. Biol. 24, 1611–1617 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    190.Parratt, S. R. & Laine, A.-L. The role of hyperparasitism in microbial pathogen ecology and evolution. ISME J. 10, 1815–1822 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    191.Kamada, N., Chen, G. Y., Inohara, N. & Núñez, G. Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14, 685–690 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    192.Hajishengallis, G. & Lamont, R. J. Dancing with the stars: how choreographed bacterial interactions dictate nososymbiocity and give rise to keystone pathogens, accessory pathogens, and pathobionts. Trends Microbiol. 24, 477–489 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    193.Neville, B. A., d’Enfert, C. & Bougnoux, M.-E. Candida albicans commensalism in the gastrointestinal tract. FEMS Yeast Res. 15, fov081 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    194.Chow, J., Tang, H. & Mazmanian, S. K. Pathobionts of the gastrointestinal microbiota and inflammatory disease. Curr. Opin. Immunol. 23, 473–480 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    195.Bonhoeffer, S., Lenski, R. E. & Ebert, D. The curse of the pharaoh: the evolution of virulence in pathogens with long living propagules. Proc. Biol. Sci. 263, 715–721 (1996).CAS 
    PubMed 
    Article 

    Google Scholar 
    196.Rafaluk-Mohr, C. The relationship between parasite virulence and environmental persistence: a meta-analysis. Parasitology 146, 897–902 (2019).PubMed 
    Article 

    Google Scholar 
    197.Ebert, D., Joachim Carius, H., Little, T. & Decaestecker, E. The evolution of virulence when parasites cause host castration and gigantism. Am. Nat. 164, S19–S32 (2004).PubMed 
    Article 

    Google Scholar 
    198.McCutcheon, J. P., Boyd, B. M. & Dale, C. The life of an insect endosymbiont from the cradle to the grave. Curr. Biol. 29, R485–R495 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    199.Moran, N. A. Accelerated evolution and Muller’s rachet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).CAS 
    PubMed 
    Article 

    Google Scholar 
    200.Moran, N. A., McCutcheon, J. P. & Nakabachi, A. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165–190 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    201.Wernegreen, J. J. Reduced selective constraint in endosymbionts: elevation in radical amino acid replacements occurs genome-wide. PLoS ONE 6, e28905 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    202.Wernegreen, J. J. Genome evolution in bacterial endosymbionts of insects. Nat. Rev. Genet. 3, 850–861 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    203.Mao, M., Yang, X. & Bennett, G. M. Evolution of host support for two ancient bacterial symbionts with differentially degraded genomes in a leafhopper host. Proc. Natl Acad. Sci. USA 115, E11691–E11700 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    204.Husnik, F. et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153, 1567–1578 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    205.Łukasik, P. et al. Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas. Proc. Natl Acad. Sci. USA 115, E226–E235 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    206.Keeling, P. J., McCutcheon, J. P. & Doolittle, W. F. Symbiosis becoming permanent: survival of the luckiest. Proc. Natl Acad. Sci. USA 112, 10101–10103 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    207.Karnkowska, A. et al. A eukaryote without a mitochondrial organelle. Curr. Biol. 26, 1274–1284 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    208.John, U. et al. An aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome. Sci. Adv. 5, eaav1110 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    209.Venkova, T., Yeo, C. C. & Espinosa, M. Editorial: The good, the bad, and the ugly: multiple roles of bacteria in human life. Front. Microbiol. 9, 1702 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    210.Cirstea, M., Radisavljevic, N. & Finlay, B. B. Good bug, bad bug: breaking through microbial stereotypes. Cell Host Microbe 23, 10–13 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    211.Durack, J. & Lynch, S. V. The gut microbiome: relationships with disease and opportunities for therapy. J. Exp. Med. 216, 20–40 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    212.Leonard, S. P. et al. Engineered symbionts activate honey bee immunity and limit pathogens. Science 367, 573–576 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    213.Wolinska, J. & King, K. C. Environment can alter selection in host–parasite interactions. Trends Parasitol. 25, 236–244 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    214.Kiers, E. T., Palmer, T. M., Ives, A. R., Bruno, J. F. & Bronstein, J. L. Mutualisms in a changing world: an evolutionary perspective. Ecol. Lett. 13, 1459–1474 (2010).Article 

    Google Scholar 
    215.Lafferty, K. D. The ecology of climate change and infectious diseases. Ecology 90, 888–900 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    216.Magalon, H., Nidelet, T., Martin, G. & Kaltz, O. Host growth conditions influence experimental evolution of life history and virulence of a parasite with vertical and horizontal transmission. Evolution 64, 2126–2138 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    217.Bull, J. J., Molineux, I. J. & Rice, W. R. Selection of benevolence in a host-parasite system. Evolution 45, 875–882 (1991).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    218.Gibson, A. K. et al. The evolution of reduced antagonism—a role for host–parasite coevolution. Evolution 69, 2820–2830 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    219.Kubinak, J. L. & Potts, W. K. Host resistance influences patterns of experimental viral adaptation and virulence evolution. Virulence 4, 410–418 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    220.Matthews, A. C., Mikonranta, L. & Raymond, B. Shifts along the parasite–mutualist continuum are opposed by fundamental trade-offs. Proc. Biol. Sci. 286, 20190236 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    221.Marchetti, M. et al. Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 8, e1000280 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    222.Ruby, E. G. et al. Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc. Biol. Sci. 102, 3004–3009 (2005).CAS 

    Google Scholar 
    223.Jeon, K. W. Genetic and physiological interactions in the amoeba-bacteria symbiosis. J. Eukaryot. Microbiol. 51, 502–508 (2004).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    224.Wang, X. et al. Cryptic prophages help bacteria cope with adverse environments. Nat. Commun. 1, 1–9 (2010).PubMed Central 

    Google Scholar 
    225.Bull, J. J. & Molineux, I. J. Molecular genetics of adaptation in an experimental model of cooperation. Evolution 46, 882–895 (1992).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    226.Kikuchi, Y., Hosokawa, T. & Fukatsu, T. An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J. 5, 446–460 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    227.Kikuchi, Y., Hosokawa, T. & Fukatsu, T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Env. Microbiol. 73, 4308–4316 (2007).CAS 
    Article 

    Google Scholar 
    228.Shapiro, J. W., Williams, E. S. C. P. & Turner, P. E. Evolution of parasitism and mutualism between filamentous phage M13 and Escherichia coli. PeerJ 4, e2060 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    229.Porter, S. S. & Simms, E. L. Selection for cheating across disparate environments in the legume-rhizobium mutualism. Ecol. Lett. 17, 1121–1129 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    230.Weese, D. J., Heath, K. D., Dentinger, B. T. M. & Lau, J. A. Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution 69, 631–642 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    231.Slater, S. C. et al. Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J. Bacteriol. 191, 2501–2511 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    232.Proença, J. T., Barral, D. C. & Gordo, I. Commensal-to-pathogen transition: one-single transposon insertion results in two pathoadaptive traits in Escherichia coli–macrophage interaction. Sci. Rep. 7, 4504 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    233.Hu, G. et al. Microevolution during serial mouse passage demonstrates FRE3 as a virulence adaptation gene in Cryptococcus neoformans. mBio 5, e00941-14 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    234.Chrostek, E. et al. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet. 9, e1003896 (2013).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    235.Sicard, M. et al. When mutualists are pathogens: an experimental study of the symbioses between Steinernema (entomopathogenic nematodes) and Xenorhabdus (bacteria). J. Evol. Biol. 17, 985–993 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    236.Margulis, L. Words as battle cries: symbiogenesis and the new field of endocytobiology. BioScience 40, 673–677 (1990).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    237.Didelot, X., Barker, M., Falush, D. & Priest, F. G. Evolution of pathogenicity in the Bacillus cereus group. Syst. Appl. Microbiol. 32, 81–90 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    238.Oishi, S., Moriyama, M., Koga, R. & Fukatsu, T. Morphogenesis and development of midgut symbiotic organ of the stinkbug Plautia stali (Hemiptera: Pentatomidae). Zool. Lett. 5, 16 (2019).Article 

    Google Scholar 
    239.Kang, Y. et al. HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLoS Pathog. 10, e1004232 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    240.Joy, J. B., Liang, R. H., McCloskey, R. M., Nguyen, T. & Poon, A. F. Y. Ancestral reconstruction. PLoS Comput. Biol. 12, e1004763 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    241.Rafaluk-Mohr, C., Ashby, B., Dahan, D. A. & King, K. C. Mutual fitness benefits arise during coevolution in a nematode-defensive microbe model. Evol. Lett. 2, 246–256 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    242.Ford, S. A., Williams, D., Paterson, S. & King, K. C. Co-evolutionary dynamics between a defensive microbe and a pathogen driven by fluctuating selection. Mol. Ecol. 26, 1778–1789 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    243.Hall, A. R., Ashby, B., Bascompte, J. & King, K. C. Measuring coevolutionary dynamics in species-rich communities. Trends Ecol. Evol. 35, 539–550 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    244.Betts, A., Rafaluk, C. & King, K. C. Host and parasite evolution in a tangled bank. Trends Parasitol. 32, 863–873 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    245.Partridge, S. R., Kwong, S. M., Firth, N. & Jensen, S. O. Mobile genetic elements associated with antimicrobial resistance. Clin. Microbiol. Rev. 31, e00088-17 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    246.Unterholzner, S. J., Poppenberger, B. & Rozhon, W. Toxin-antitoxin systems: biology, identification, and application. Mob. Genet. Elem. 3, e26219 (2013).Article 
    CAS 

    Google Scholar 
    247.Croucher, N. J. et al. Rapid pneumococcal evolution in response to clinical interventions. Science 331, 430–434 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    248.Wu, M. et al. Phylogenomics of the reproductive parasite wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2, E69 (2004).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    249.Frost, C. L. et al. The hypercomplex genome of an insect reproductive parasite highlights the importance of lateral gene transfer in symbiont biology. mBio 11, e02590-19 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    250.Bamford, D. H. Do viruses form lineages across different domains of life? Res. Microbiol. 154, 231–236 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    251.Casjens, S. et al. A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 35, 490–516 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    252.Casjens, S. Prophages and bacterial genomics: what have we learned so far? Mol. Microbiol. 49, 277–300 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar  More

  • in

    The sublethal effects of neonicotinoids on spiders are independent of their nutritional status

    1.Holmstrum, P. et al. Interactions between effects of environmental chemicals and natural stressors: A review. Sci. Total Environ. 408, 3746–3762 (2010).ADS 
    Article 
    CAS 

    Google Scholar 
    2.Wahl, O. & Ulm, K. Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia 59, 106–128 (1983).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    3.Schmehl, D. R., Teal, P. E. A., Frazier, J. L. & Grozinger, C. M. Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera). J. Insect Physiol. 71, 177–190 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Tosi, S., Nieh, J. C., Sgolastra, F., Cabbri, R. & Medrzycki, P. Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees. Proc. Biol. Sci. 284, 20171711 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    5.Stuligross, C. & Williams, N. M. Pesticide and resource stressors additively impair wild bee reproduction. Proc. Biol. Sci. 287, 20201390 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    6.Liess, M., Foit, K., Knillmann, S., Schäfer, R. B. & Liess, H.-D. Predicting the synergy of multiple stress effects. Sci. Rep. 6, 32965 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Goulson, D., Nicholls, E., Botias, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    8.Simpson, S. J. & Raubenheimer, D. The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity (Princeton University Press, 2012).
    Google Scholar 
    9.Simpson, S. J., Le Couteur, D. G. & Raubenheimer, D. Putting the balance back in diet. Cell 161, 18–23 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Wise, D. Food limitation of the spider Linyphia marginata: Experimental field studies. Ecology 56, 637–646 (1975).Article 

    Google Scholar 
    11.Bilde, T. & Toft, S. Quantifying food limitation of arthropod predators in the field. Oecologia 115, 54–58 (1998).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Wilder, S. M. & Rypstra, A. Diet quality affects mating behaviour and egg production in a wolf spider. Anim. Behav. 76, 439–445 (2008).Article 

    Google Scholar 
    13.Tanaka, K. & Itô, Y. Decrease in respiratory rate in a wolf spider, Pardosa astrigera (L. Koch), under starvation. Res. Popul. Ecol. 24, 360–374 (1982).Article 

    Google Scholar 
    14.O’Connor, K. I., Taylor, A. C. & Metcalfe, N. B. The stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon. J. Fish Biol. 57, 41–51 (2000).Article 

    Google Scholar 
    15.McCue, M. D. Specific dynamic action: A century of investigation. Comp. Biochem. Physiol. A. 144, 381394 (2006).Article 
    CAS 

    Google Scholar 
    16.Secor, S. M. Specific dynamic action: A review of the postprandial metabolic response. J. Comp. Physiol. B 179, 1–56 (2009).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Van Leeuwen, T. E., Rosenfeld, J. S. & Richards, J. G. Effects of food ration on SMR: Influence of food consumption on individual variation in metabolic rate in juvenile coho salmon (Onchorhynchus kisutch). J. Anim. Ecol. 81, 395–402 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Parthasarathy, B. & Somanathan, H. Body condition and food shapes group dispersal but not solitary dispersal in a social spider. Behav. Ecol. 29, 619–627 (2018).Article 

    Google Scholar 
    19.Koemel, N. A., Barnes, C. L. & Wilder, S. M. Metabolic and behavioral responses of predators to prey nutrient content. J. Insect Physiol. 116, 25–31 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Řezáč, M., Řezáčová, V. & Heneberg, P. Neonicotinoid insecticides limit the potential of spiders to re-colonize disturbed agroecosystems when using silk-mediated dispersal. Sci. Rep. 9, 12272 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    21.Řezáč, M., Řezáčová, V. & Heneberg, P. Contact application of neonicotinoids suppresses the predation rate in different densities of prey and induces paralysis of common farmland spiders. Sci. Rep. 9, 5724 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    22.Fagan, W. F. et al. Nitrogen in insects: implications for trophic complexity and species diversification. Am. Nat. 160, 784–802 (2002).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Raubenheimer, D., Mayntz, D., Simpson, S. J. & Tøft, S. Nutrient-specific compensation following diapause in a predator: Implications for intraguild predation. Ecology 88, 2598–2608 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Lease, H. M. & Wolf, B. O. Exoskeletal chitin scales iso¬metrically with body size in terrestrial insects. J. Morphol. 271, 759–768 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    25.Wilder, S. M., Norris, M., Lee, R. W., Raubenheimer, D. & Simpson, S. J. Arthropod food webs become increasingly lipid-limited at higher trophic levels. Ecol. Lett. 16, 895–902 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Salomon, M., Mayntz, D. & Lubin, Y. Colony nutrition skews reproduction in a social spider. Behav. Ecol. 19, 605–611 (2008).Article 

    Google Scholar 
    27.Jensen, K., Mayntz, D., Wang, T., Simpson, S. J. & Overgaard, J. Metabolic consequences of feeding and fasting on nutritionally different diets in the wolf spider Pardosa prativaga. J. Insect Physiol. 56, 1095–1100 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Jensen, K., Mayntz, D., Toft, S., Raubenheimer, D. & Simpson, S. J. Nutrient regulation in a predator, the wolf spider Pardosa prativaga. Anim. Behav. 81, 993–999 (2011).Article 

    Google Scholar 
    29.Wiggins, W. D. & Wilder, S. M. Mismatch between dietary requirements for lipid by a predator and availability of lipid in prey. Oikos 127, 1024–1032 (2018).CAS 
    Article 

    Google Scholar 
    30.Uetz, G. W., Bischoff, J. & Raver, J. Survivorship of wolf spiders (Lycosidae) reared on different diets. J. Arachnol. 20, 207–211 (1992).
    Google Scholar 
    31.Sigsgaard, L., Toft, S. & Villareal, S. Diet-dependent survival, development and fecundity of the spider Atypena formosana (Oi) (Araneae: Linyphiidae) implications for biological control in rice. Biocontrol Sci. Technol. 11, 233–244 (2001).Article 

    Google Scholar 
    32.Fisker, E. N. & Toft, S. Effects of chronic exposure to a toxic prey in a generalist predator. Physiol. Entomol. 29, 129–138 (2004).Article 

    Google Scholar 
    33.Jensen, K., Mayntz, D., Toft, S., Raubenheimer, D. & Simpson, S. J. Prey nutrient composition has different effects on Pardosa wolf spiders with dissimilar life histories. Oecologia 165, 577–583 (2011).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Wilder, S. M. Spider nutrition: An integrative perspective. Adv. Insect Physiol. 40, 87–136 (2011).Article 

    Google Scholar 
    35.Barnes, C. L., Hawlena, D. & Wilder, S. M. Predators buffer the effects of variation in prey nutrient content for nutrient deposition. Oikos 128, 360–367 (2019).Article 

    Google Scholar 
    36.Jensen, K. et al. Optimal foraging for specific nutrients in predatory beetles. Proc. R. Soc. B 279, 2212–2218 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Toft, S. & Macías-Hernández, N. Metabolic adaptations for isopod specialization in three species of Dysdera spiders from the Canary Islands. Physiol. Entomol. 42, 191–198 (2017).CAS 
    Article 

    Google Scholar 
    38.Barry, K. L. & Wilder, S. M. Macronutrient intake affects reproduction of a predatory insect. Oikos 122, 1058–1064 (2013).Article 

    Google Scholar 
    39.Wilder, S. M. & Schneider, J. M. Micronutrient consumption by female Argiope bruennichi affects offspring survival. J. Insect Physiol. 100, 128–132 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    40.Demaree, S. R., Gilbert, C. D., Mersmann, H. J. & Smith, S. B. Conjugated linoleic acid differentially modifies fatty acid composition in subcellular fractions of muscle and adipose tissue but not adiposity of postweaning pigs. J. Nutr. 132, 3272–3279 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Nagao, K. & Yanagita, T. Conjugated fatty acids in food and their health benefits. J. Biosci. Bioeng. 100, 152–157 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Hennessy, A. A., Ross, P. R., Fitzgerald, G. F. & Stanton, C. Sources and bioactive properties of conjugated dietary fatty acids. Lipids 51, 377–397 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Hawley, J., Simpson, S. J. & Wilder, S. M. Effects of prey macronutrient content on body composition and nutrient intake in a web-building spider. PLoS ONE 9, e99165 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    44.Whitehorn, P. R., O’Connor, S., Wackers, F. L. & Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352 (2012).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Dicks, L. Bees, lies and evidence-based policy. Nature 494, 283 (2013).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Rundlöf, M. et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521, 77–80 (2015).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    47.Tsvetkov, N. et al. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science 356, 1395–1397 (2017).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Woodcock, B. A. et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356, 1393–1395 (2017).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Song, F. et al. Specific loops D, E and F of nicotinic acetylcholine receptor β1 subunit may confer imidacloprid selectivity between Myzus persicae and its predatory enemy Pardosa pseudoannulata. Insect Biochem. Mol. Biol. 39, 833–841 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    50.Korenko, S., Sýkora, J., Řezáč, M. & Heneberg, P. Neonicotinoids suppress contact chemoreception in a common farmland spider. Sci. Rep. 10, 7019 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Benamú, M. et al. Nanostructural and mechanical property changes to spider silk as a consequence of insecticide exposure. Chemosphere 181, 241–249 (2017).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    52.Korenko, S., Saska, P., Kysilková, K., Řezáč, M. & Heneberg, P. Prey contaminated with neonicotinoids induces feeding deterrent behavior of a common farmland spider. Sci. Rep. 9, 15895 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    53.Park, Y. et al. Imidacloprid, a neonicotinoid insecticide, potentiates adipogenesis in 3T3-L1 adipocytes. J. Agric. Food Chem. 61, 255–259 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Sun, Q. et al. Imidacloprid promotes high fat diet-induced adiposity in female C57BL/6J mice and enhances adipogenesis in 3T3-L1 adipocytes via the AMPKα-mediated pathway. J. Agric. Food Chem. 65, 6572–6581 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Sun, Q. et al. Imidacloprid promotes high fat diet-induced adiposity and insulin resistance in male C57BL/6J mice. J. Agric. Food Chem. 64, 9293–9306 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.McCluney, K. E. & Sabo, J. L. Water availability directly determines per capita consumption at two trophic levels. Ecology 90, 1463–1469 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.McCluney, K. E. & Sabo, J. L. Tracing water sources of terrestrial animal populations with stable isotopes: Laboratory tests with crickets and spiders. PLoS ONE 5, e15696 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Leinbach, I. L., McCluney, K. E. & Sabo, J. L. Predator water balance alters intraguild predation in a streamside food web. Ecology 100, e02635 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Noldus, L. P., Spink, A. J. & Tegelenbosch, R. A. EthoVision: A versatile video tracking system for automation of behavioral experiments. Behav. Res. Methods Instrum. Comput. 33, 398–414 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Pétillon, J. J., Deruytter, D., Decae, A., Renault, D. & Bonte, D. Habitat use, but not dispersal limitations, as the mechanism behind the aggregated population structure of the mygalomorph species Atypus affinis. Anim. Biol. 62, 181–192 (2012).Article 

    Google Scholar 
    61.Radwan, M. A. & Mohamed, M. S. Imidacloprid induced alterations in enzyme activities and energy reserves of the land snail, Helix aspersa. Ecotoxicol. Environ. Saf. 95, 91–97 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Ribeiro, S., Sousa, J. P., Nogueira, A. J. A. & Soares, A. M. V. M. Effect of endosulfan and parathion on energy reserves and physiological parameters of the terrestrial isopod Porcellio dilatatus. Ecotoxicol. Environ. Saf. 49, 131–138 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Rambabu, P. J. & Rao, M. B. Effect of an organochlorine and three organophosphate pesticides on glucose, glycogen, lipid and protein contents in tissues of the freshwater snail, Bellamya dissimilis (Müller). Bull. Environ. Contam. Toxicol. 53, 142–148 (1994).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    64.Dutra, B. K., Fernandes, F. A., Lauffer, A. L. & Oliveira, G. T. Carbofuran-induced alterations in the energy metabolism and reproductive behaviors of Hyalella castroi (Crustacea, Amphipoda). Comp. Biochem. Physiol. Part C 149, 640–646 (2009).CAS 

    Google Scholar 
    65.Messiad, R., Habes, D. & Soltani, N. Reproductive effects of a neonicotinoid insecticide (Imidacloprid) in the German Cockroaches Blattella germanica L. (Dictyoptera, Blattellidae). J. Entomol. Zool. Stud. 3, 1–6 (2015).
    Google Scholar 
    66.Abdelsalam, S. A., Alzahrani, A. M., Elmenshawy, O. M., Sedky, A. & Abdel-Moneim, A. M. Biochemical and ultrastructural changes in the ovaries of red palm weevil, Rhynchophorus ferrugineus (Coleoptera: Curculionidae) following acute imidacloprid poisoning. J. Asia Pac. Entomol. 23, 709–714 (2020).Article 

    Google Scholar 
    67.Tufi, S., Stel, J. M., De Boer, J., Lamoree, M. H. & Leonards, P. E. G. Metabolomics to explore imidacloprid-induced toxicity in the central nervous system of the freshwater snail Lymnaea stagnalis. Environ. Sci. Technol. 49, 14529–14536 (2015).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Ewere, E. E., Reichelt-Brushett, A. & Benkerndorff, K. Imidacloprid and formulated product impacts the fatty acids and enzymatic activities in tissues of Sydney rock oysters, Saccostrea glomerata. Mar. Environ. Res. 151, 104765 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    69.Capowiez, Y., Rault, M., Mazzia, C. & Belzunces, L. Earthworm behavior as a biomarker: A case study using imidacloprid. Pedobiologia 47, 542–547 (2003).
    Google Scholar 
    70.Drobne, D. et al. Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Chemosphere 71, 1326–1334 (2008).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar  More

  • in

    Metagenomic shotgun sequencing reveals host species as an important driver of virome composition in mosquitoes

    1.Cadwell, K. The virome in host health and disease. Immunity 42, 805–813 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Paez-Espino, D. et al. Uncovering earth’s virome. Nature https://doi.org/10.1038/nature19094 (2016).Article 
    PubMed 

    Google Scholar 
    3.Shi, M. et al. The evolutionary history of vertebrate RNA viruses. Nature 556, 197–202 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    4.Dolja, V. V. & Koonin, E. V. Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer. Virus Res. 244, 36–52 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Li, C.-X. et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife 4, e05378 (2015).PubMed Central 
    Article 
    CAS 
    PubMed 

    Google Scholar 
    6.Shi, M. et al. Redefining the invertebrate RNA virosphere. Nature 540, 539–543 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Atoni, E. et al. Metagenomic Virome Analysis of Culex Mosquitoes from Kenya and China. Viruses 10, 30 (2018).PubMed Central 
    Article 
    CAS 
    PubMed 

    Google Scholar 
    8.Sadeghi, M. et al. Virome of > 12 thousand Culex mosquitoes from throughout California. Virology 523, 74–88 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    9.Zakrzewski, M. et al. Mapping the virome in wild-caught Aedes aegypti from Cairns and Bangkok. Nat. Publ. Group https://doi.org/10.1038/s41598-018-22945-y (2018).Article 

    Google Scholar 
    10.Xia, H. et al. Comparative metagenomic profiling of viromes associated with four common mosquito species in China. Virol. Sin. 33, 59–66 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Frey, K. G. et al. Bioinformatic characterization of mosquito viromes within the eastern United States and Puerto Rico: ciscovery of novel viruses. Evolut. Bioinform. 12s2, EBO.S38518 (2016).Article 

    Google Scholar 
    12.Chandler, J. A., Liu, R. M. & Bennett, S. N. RNA shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Front. Microbiol. 06, 403 (2015).Article 

    Google Scholar 
    13.Chandler, J. A. et al. Metagenomic shotgun sequencing of a Bunyavirus in wild-caught Aedes aegypti from Thailand informs the evolutionary and genomic history of the Phleboviruses. Virology 464–465, 312–319 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    14.Cholleti, H. et al. Discovery of novel viruses in mosquitoes from the Zambezi valley of Mozambique. PLoS ONE 11, e0162751 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    15.Scarpassa, V. M. et al. An insight into the sialotranscriptome and virome of Amazonian anophelines. BMC Genom. https://doi.org/10.1186/s12864-019-5545-0 (2019).Article 

    Google Scholar 
    16.Hameed, M. et al. A viral metagenomic analysis reveals rich viral abundance and diversity in mosquitoes from pig farms. Transbound. Emerg. Dis. 67, 328–343 (2019).PubMed 
    Article 

    Google Scholar 
    17.Fauver, J. R. et al. West African Anopheles gambiae mosquitoes harbor a taxonomically diverse virome including new insect-speci. Virology 498, 288–299 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    18.Xiao, P. et al. Metagenomic sequencing from mosquitoes in China reveals a variety of insect and human viruses. Front. Cell. Infect. Microbiol. 8, 131–211 (2018).Article 
    CAS 

    Google Scholar 
    19.Shi, C. et al. Stable distinct core eukaryotic viromes in different mosquito species from Guadeloupe, using single mosquito viral metagenomics. Microbiome https://doi.org/10.1186/s40168-019-0734-2 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.World Health Organization. A global brief on vector-borne diseases. (2014).21.Vasilakis, N. & Tesh, R. B. Insect-specific viruses and their potential impact on arbovirus transmission. Curr. Opin. Virol. 15, 69–74 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Goenaga, S. et al. Potential for co-infection of a mosquito-specific flavivirus, Nhumirim virus, to block West Nile virus transmission in mosquitoes. Viruses 7, 5801–5812 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Hall-Mendelin, S. et al. The insect-specific Palm Creek virus modulates West Nile virus infection in and transmission by Australian mosquitoes. Parasit. Vectors 9, 414 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Colmant, A. M. G. et al. The recently identified flavivirus Bamaga virus is transmitted horizontally by Culex mosquitoes and interferes with West Nile virus replication in vitro and transmission in vivo. PLoS Negl. Trop. Dis. 12, e0006886 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Romo, H., Kenney, J. L., Blitvich, B. J. & Brault, A. C. Restriction of Zika virus infection and transmission in Aedes aegypti mediated by an insect-specific flavivirus. Emerg. Microbes Infect 7, 181 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Schultz, M. J., Frydman, H. M. & Connor, J. H. Dual Insect specific virus infection limits Arbovirus replication in Aedes mosquito cells. Virology 518, 406–413 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Thongsripong, P. et al. Mosquito vector diversity across habitats in central Thailand endemic for dengue and other arthropod-borne diseases. PLoS Negl. Trop. Dis. 7, e2507 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Kukutla, P., Steritz, M. & Xu, J. Depletion of ribosomal RNA for mosquito gut metagenomic RNA-seq. JoVE https://doi.org/10.3791/50093 (2013).Article 
    PubMed 

    Google Scholar 
    29.Rattanarithikul, R., Harrison, B. A. & Panthusiri, P. Coleman RE (2005) Illustrated keys to the mosquitoes of Thailand I. Background; geographic distribution; lists of genera, subgenera, and species; and a key to the genera. Southeast Asian J. Trop. Med. Public Health 36 Suppl 1, 1–80 (2005).PubMed 

    Google Scholar 
    30.Rattanarithikul, R. et al. Illustrated keys to the mosquitoes of Thailand. II. Genera Culex and Lutzia. Southeast Asian J. Trop. Med. Public Health 36 Suppl 2, 1–97 (2005).PubMed 

    Google Scholar 
    31.Rattanarithikul, R., Harrison, B. A., Panthusiri, P., Peyton, E. L. & Coleman, R. E. Illustrated keys to the mosquitoes of Thailand III. Genera Aedeomyia, Ficalbia, Mimomyia, Hodgesia, Coquillettidia, Mansonia, and Uranotaenia. Southeast Asian J. Trop. Med. Public Health 37 Suppl 1, 1–85 (2006).PubMed 

    Google Scholar 
    32.Rattanarithikul, R., Harrison, B. A., Harbach, R. E., Panthusiri, P. & Coleman, R. E. Illustrated keys to the mosquitoes of Thailand. IV. Anopheles. Southeast Asian J. Trop. Med. Public Health 37 Suppl 2, 1–128 (2006).PubMed 

    Google Scholar 
    33.Rattanarithikul, R., Harbach, R. E., Harrison, B. A., Panthusiri, P. & Coleman, R. E. Illustrated keys to the mosquitoes of Thailand V. Genera Orthopodomyia, Kimia, Malaya, Topomyia, Tripteroides, and Toxorhynchites. Southeast Asian J. Trop. Med. Public Health 38, 1–65 (2007).PubMed 

    Google Scholar 
    34.Rattanarithikul, R. et al. Illustrated keys to the mosquitoes of Thailand. VI. Tribe Aedini. Southeast Asian J. Trop. Med. Public Health 41 Suppl 1, 1–225 (2010).PubMed 

    Google Scholar 
    35.Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    37.Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Katoh, K., Rozewicki, J. & Yamada, K. D. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. https://doi.org/10.1093/bib/bbx108 (2017).Article 
    PubMed Central 
    PubMed 

    Google Scholar 
    39.Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164–1165 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Kozlov, A. M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. RAxML-NG: A fast, scalable, and user-friendly tool for maximum likelihood phylogenetic inference. bioRxiv 447110 (2018).42.Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES science gateway for interface of large phylogenetic trees. 1–8 (2010).43.Letunic, I. & Bork, P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. https://doi.org/10.1093/nar/gkz239 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat Methods 9, 357–359 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    45.Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    46.Ryan, F. P. Human endogenous retroviruses in multiple sclerosis: potential for novel neuro-pharmacological research. Curr. Neuropharmacol. 9, 360–369 (2011).47.Wood, D. E. & Salzberg, S. L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15, R46 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Kopylova, E., Noe, L. & Touzet, H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211–3217 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    49.Simmonds, P. et al. ICTV virus taxonomy profile: Flaviviridae. J. Gen. Virol. 98, 2–3 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Kyaw, A. K. et al. Virus research. Virus Res. 247, 120–124 (2018).Article 
    CAS 

    Google Scholar 
    51.Valles, S. M. et al. ICTV virus taxonomy profile: Iflaviridae. J. Gen. Virol. 98, 527–528 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Kobayashi, D. et al. Isolation and characterization of a new iflavirus from Armigeres spp. mosquitoes in the Philippines. J. Gen. Virol. 98, 2876–2881 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Viruses, I. C. O. T. O., King, A. M. Q., Adams, M. J., Lefkowitz, E. & Carstens, E. B. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses (Elsevier, Amsterdam, 2011).
    Google Scholar 
    54.Hillman, B. I. & Cai, G. The family narnaviridae: Simplest of RNA viruses. Adv. Virus Res. 86, 149–176 (2013).PubMed 
    Article 

    Google Scholar 
    55.Turina, M. et al. ICTV virus taxonomy profile: Ourmiavirus. J. Gen. Virol. 98, 129–130 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Yong, C. Y., Yeap, S. K., Omar, A. R. & Tan, W. S. Advances in the study of nodavirus. PeerJ 5, e3841 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    57.Sahul Hameed, A. S. et al. ICTV virus taxonomy profile: Nodaviridae. J. Gen. Virol. 100, 3–4 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    58.Sanborn, M. et al. Metagenomic analysis reveals three novel and prevalent mosquito biruses from a single pool of Aedes vexans nipponii collected in the Republic of Korea. Viruses 11, 222 (2019).CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    59.Olendraite, I. et al. ICTV virus taxonomy profile: Polycipiviridae. J. Gen. Virol. 100, 554–555 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Wichgers Schreur, P. J., Kormelink, R. & Kortekaas, J. Genome packaging of the Bunyavirales. Curr. Opin. Virol. 33, 151–155 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    61.Marklewitz, M., Zirkel, F., Kurth, A., Drosten, C. & Junglen, S. Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family. Proc. Natl. Acad. Sci. U.S.A. 112, 7536–7541 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Walker, P. J. et al. ICTV virus taxonomy profile: Rhabdoviridae. J. Gen. Virol. 99, 447–448 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Sun, Q. et al. Complete genome sequence of Menghai rhabdovirus, a novel mosquito-borne rhabdovirus from China. Adv. Virol. 162, 1103–1106 (2017).CAS 

    Google Scholar 
    64.Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. & Werren, J. H. How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol Lett 281, 215–220 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Flegontov, P. et al. Paratrypanosoma is a novel early-branching trypanosomatid. Curr Biol 23, 1787–1793 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    66.Kaur, D. et al. Occurrence of Setaria digitata in a cow. J Parasit Dis 39, 477–478 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    67.Heneberg, P. et al. Intermediate hosts of the trematode Collyriclum faba (Plagiochiida: Collyriclidae) identified by an integrated morphological and genetic approach. Parasit. Vectors 8, 85 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Enabulele, E. E., Lawton, S. P., Walker, A. J. & Kirk, R. S. Molecular and morphological characterization of the cercariae of Lecithodendrium linstowi (Dollfus, 1931), a trematode of bats, and incrimination of the first intermediate snail host Radix balthica. Parasitology 145, 307–312 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Greiman, S. E. et al. Real-time PCR detection and phylogenetic relationships of Neorickettsia spp. in digeneans from Egypt, Philippines, Thailand, Vietnam and the United States. Parasitol. Int. 66, 1003–1007 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Lantova, L. & Volf, P. Mosquito and sand fly gregarines of the genus Ascogregarina and Psychodiella (Apicomplexa: Eugregarinorida, Aseptatorina)—Overview of their taxonomy, life cycle, host specificity and pathogenicity. Infect. Genet. Evol. 28, 616–627 (2014).PubMed 
    Article 

    Google Scholar 
    71.Roychoudhury, S. et al. Comparison of the morphology of oocysts and the phylogenetic analysis of four Ascogregarina species (Eugregarinidae: Lecudinidae) as inferred from small subunit ribosomal DNA sequences. Parasitol. Int. 56, 113–118 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Muslim, A., Fong, M.-Y., Mahmud, R., Lau, Y.-L. & Sivanandam, S. Armigeres subalbatus incriminated as a vector of zoonotic Brugia pahangi filariasis in suburban Kuala Lumpur Peninsular Malaysia. Parasites Vectors 6, 219 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Hiscox, A. et al. Armigeres subalbatus colonization of damaged pit latrines: A nuisance and potential health risk to residents of resettlement villages in Laos. Med. Vet. Entomol. 30, 95–100 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    74.Chaves, L. F., Imanishi, N. & Hoshi, T. Population dynamics of Armigeres subalbatus (Diptera: Culicidae) across a temperate altitudinal gradient. Bull. Entomol. Res. 105, 589–597 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    75.Ohba, S.-Y., Van Soai, N., Van Anh, D. T., Nguyen, Y. T. & Takagi, M. Study of mosquito fauna in rice ecosystems around Hanoi, northern Vietnam. Acta Trop. 142, 89–95 (2015).PubMed 
    Article 

    Google Scholar 
    76.Tsuda, Y., Takagi, M., Suwonkerd, W., Sugiyama, A. & Wada, Y. Comparisons of rice field mosquito (Diptera: Culicidae) abundance among areas with different agricultural practices in northern Thailand. J. Med. Entom. 35, 845–848 (1998).CAS 
    Article 

    Google Scholar 
    77.Ohba, S.-Y. et al. Mosquitoes and their potential predators in rice agroecosystems of the Mekong Delta, southern Vietnam. J. Am. Mosq. Control Assoc. 27, 384–392 (2011).PubMed 
    Article 

    Google Scholar 
    78.Su, C.-L. et al. Molecular epidemiology of Japanese encephalitis virus in mosquitoes in Taiwan during 2005–2012. PLoS Negl. Trop. Dis. 8, e3122 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    79.Keiser, J. et al. Effect of irrigated rice agriculture on Japanese encephalitis, including challenges and opportunities for integrated vector management. Acta Trop. 95, 40–57 (2005).PubMed 
    Article 

    Google Scholar 
    80.Apiwathnasorn, C., Samung, Y., Prummongkol, S., Asavanich, A. & Komalamisra, N. Surveys for natural host plants of Mansonia mosquitoes inhabiting Toh Daeng peat swamp forest, Narathiwat Province, Thailand. Southeast Asian J. Trop. Med. Public Health 37, 279–282 (2006).PubMed 

    Google Scholar 
    81.Surtees, G., Simpson, D. I. H., Bowen, E. T. W. & Grainger, W. E. Ricefield development and arbovirus epidemiology, Kano Plain, Kenya. Trans. R. Soc. Trop. Med. Hyg. 64, 511–518 (1970).CAS 
    PubMed 
    Article 

    Google Scholar 
    82.Kwa, B. H. Environmental change, development and vector-borne disease: Malaysia’s experience with filariasis, scrub typhus and dengue. Environ. Dev. Sustain. 10, 209–217 (2008).Article 

    Google Scholar 
    83.Cook, S. et al. Molecular evolution of the insect-specific flaviviruses. J. Gen. Virol. 93, 223–234 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    84.Parry, R. & Asgari, S. Aedes anphevirus: an insect-specific virus distributed worldwide in Aedes aegypti mosquitoes that has complex interplays with Wolbachia and Dengue Virus Infection in Cells. J. Virol. 92, e00224–18 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    85.Shi, M. et al. High-resolution metatranscriptomics reveals the ecological dynamics of mosquito-associated RNA viruses in western Australia. J. Virol. 91, e00680–17 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    86.Thongsripong, P. et al. Mosquito vector-associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod-borne diseases. Ecol. Evol. 8, 1352–1368 (2018).PubMed 
    Article 

    Google Scholar 
    87.Eisenhofer, R. et al. Contamination in low microbial biomass microbiome studies: Issues and recommendations. Trends Microbiol. 27, 105–117 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    88.Salter, S. J. et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 12, 1–12 (2014).MathSciNet 
    Article 
    CAS 

    Google Scholar 
    89.Pollock, J., Glendinning, L., Wisedchanwet, T. & Watson, M. The madness of microbiome: attempting to find consensus ‘best practice’ for 16S microbiome studies. Appl. Environ. Microbiol. 84, e02627–17 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    90.Blair, C. D., Olson, K. E. & Bonizzoni M. The widespread occurrence and potential biological roles of endogenous viral elements in insect genomes. Curr. Issues Mol. Biol. 34, 13–30 (2020).PubMed 
    Article 

    Google Scholar  More

  • in

    Salt-induced recruitment of specific root-associated bacterial consortium capable of enhancing plant adaptability to salt stress

    1.Julkowska MM, Testerink C. Tuning plant signaling and growth to survive salt. Trends Plant Sci. 2015;20:586–94.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Li H, Zhao Q, Huang H. Current states and challenges of salt-affected soil remediation by cyanobacteria. Sci Total Environ. 2019;669:258–72.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    3.FAO. Extent of salt-affected soils. 2020. http://www.fao.org/soils-portal/soil-management/management-of-some-problem-soils/salt-affected-soils/more-information-on-salt-affected-soils/en/. Accessed 14 June 2020.4.Jamil A, Riaz S, Ashraf M, Foolad MR. Gene expression profiling of plants under salt stress. Crit Rev Plant Sci. 2011;30:435–58.Article 

    Google Scholar 
    5.Ouhibi C, Attia H, Rebah F, Msilini N, Chebbi M, Aarrouf J, et al. Salt stress mitigation by seed priming with UV-C in lettuce plants: Growth, antioxidant activity and phenolic compounds. Plant Physiol Biochem. 2014;83:126–33.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.McFarlane DJ, George RJ, Barrett-Lennard EG, Gilfedder M. Salinity in dryland agricultural systems: challenges and opportunities. In: Farooq M, Siddique KHM, editors. Innovations in dryland agriculture. 1st ed. Switzerland: Springer Nature; 2016. p. 521–47.
    Google Scholar 
    7.Yang Y, Guo Y. Elucidating the molecular mechanisms mediating plant salt-stress responses. N. Phytol. 2018;217:523–39.CAS 
    Article 

    Google Scholar 
    8.Zörb C, Geilfus CM, Dietz KJ. Salinity and crop yield. Plant Biol. 2019;21:31–38.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    9.Flood PJ, Hancock AM. The genomic basis of adaptation in plants. Curr Opin Plant Biol. 2017;36:88–94.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Yuan F, Leng B, Wang B. Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt? Front Plant Sci. 2016;7:977.PubMed 
    PubMed Central 

    Google Scholar 
    11.Yang Y, Guo Y. Unraveling salt stress signaling in plants. J Integr Plant Biol. 2018;60:796–804.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Kazan K, Lyons R. The link between flowering time and stress tolerance. J Exp Bot. 2015;67:47–60.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    13.Zhu JK. Abiotic stress signaling and responses in plants. Cell. 2016;167:313–24.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Lowry DB, Hall MC, Salt DE, Willis JH. Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. N. Phytol. 2009;183:776–88.Article 

    Google Scholar 
    15.Ilangumaran G, Smith DL. Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci. 2017;8:1768.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Rodriguez PA, Rothballer M, Chowdhury SP, Nussbaumer T, Gutjahr C, Falter-Braun P. Systems biology of plant microbiome interactions. Mol Plant. 2019;12:804–21.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Berendsen RL, Pieterse CM, Bakker PA. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Mhlongo MI, Piater LA, Madala NE, Labuschagne N, Dubery IA. The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Front Plant Sci. 2018;9:112.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Finkel OM, Castrillo G, Paredes SH, González IS, Dangl JL. Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol. 2017;38:155–63.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Kwak MJ, Kong HG, Choi K, Kwon SK, Song JY, Lee J, et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol. 2018;36:1100–9.CAS 
    Article 

    Google Scholar 
    21.Jha B, Gontia I, Hartmann A. The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil. 2012;356:265–77.CAS 
    Article 

    Google Scholar 
    22.Qin S, Zhang YJ, Yuan B, Xu PY, Xing K, Wang J, et al. Isolation of ACC deaminase-produ0cing habitat-adapted symbiotic bacteria associated with halophyte Limonium sinense (Girard) Kuntze and evaluating their plant growth-promoting activity under salt stress. Plant Soil. 2014;374:753–66.CAS 
    Article 

    Google Scholar 
    23.Soldan R, Mapelli F, Crotti E, Schnell S, Daffonchio D, Marasco R, et al. Bacterial endophytes of mangrove propagules elicit early establishment of the natural host and promote growth of cereal crops under salt stress. Microbiol Res. 2019;223:33–43.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    24.Bal HB, Nayak L, Das S, Adhya TK. Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil. 2013;366:93–105.CAS 
    Article 

    Google Scholar 
    25.Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A. Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep. 2016;6:34768.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Dong ZY, Rao MPN, Wang HF, Fang BZ, Liu YH, Li L, et al. Transcriptomic analysis of two endophytes involved in enhancing salt stress ability of Arabidopsis thaliana. Sci Total Environ. 2019;686:107–17.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Yaish MW, Al-Lawati A, Jana GA, Patankar HV, Glick BR. Impact of soil salinity on the structure of the bacterial endophytic community identified from the roots of caliph medic (Medicago truncatula). PLoS One. 2016;11:e0159007.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    28.Yang H, Hu J, Long X, Liu Z, Rengel Z. Salinity altered root distribution and increased diversity of bacterial communities in the rhizosphere soil of Jerusalem artichoke. Sci Rep. 2016;6:20687.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Thiem D, Gołębiewski M, Hulisz P, Piernik A, Hrynkiewicz K. How does salinity shape bacterial and fungal microbiomes of Alnus glutinosa roots? Front Microbiol. 2018;9:651.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Paul D, Lade H. Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev. 2014;34:737–52.Article 

    Google Scholar 
    31.Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol. 2006;57:233–66.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Sasse J, Martinoia E, Northen T. Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci. 2018;23:25–41.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Badri DV, Vivanco JM. Regulation and function of root exudates. Plant Cell Environ. 2009;32:666–81.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones CM, et al. Loss in microbial diversity affects nitrogen cycling in soil. ISME J. 2013;7:1609–19.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    35.Niu B, Paulson JN, Zheng X, Kolter R. Simplified and representative bacterial community of maize roots. Proc Natl Acad Sci USA. 2017;114:E2450–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Vargas R, Pankova E, Balyuk A, Krasilnikov P, Khasankhanova G, editors. Handbook for saline soil management. Food and Agriculture Organization of the United Nations and Lomonosov Moscow State University, Rome, Italy, 2018, pp 8–11.37.McNamara NP, Black HIJ, Beresford NA, Parekh NR. Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Appl Soil Ecol. 2003;24:117–32.Article 

    Google Scholar 
    38.Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, et al. Functional overlap of the Arabidopsis leaf and root microbiota. Nature. 2015;528:364–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Carrión VJ, Perez-Jaramillo J, Cordovez V, Tracanna V, de Hollander M, Ruiz-Buck D, et al. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science. 2019;366:606–12.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    40.Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Zhang J, Liu YX, Zhang N, Hu B, Jin T, Xu H, et al. NRT1. 1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol. 2019;37:676–84.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–200.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Edgar RC. Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinforma (Oxf, Engl). 2018;34:2371–5.CAS 
    Article 

    Google Scholar 
    45.Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2010;26:266–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA. 2013;110:6548–53.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    50.Javůrková VG, Kreisinger J, Procházka P, Požgayová M, Ševčíková K, Brlík V, et al. Unveiled feather microcosm: feather microbiota of passerine birds is closely associated with host species identity and bacteriocin-producing bacteria. ISME J. 2019;13:2363–76.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    51.Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Community ecology package. R package version 2.5-6. https://cran.r-project.org. Accessed 1 Sep 2019.52.Cáceres MD, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology. 2009;90:3566–74.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Louca S, Parfrey LW, Doebeli M. Decoupling function and taxonomy in the global ocean microbiome. Science. 2016;353:1272–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Santhanam R, Weinhold A, Goldberg J, Oh Y, Baldwin IT. Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci USA. 2015;112:E5013–20.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Dudenhöffer J-H, Scheu S, Jousset A. Systemic enrichment of antifungal traits in the rhizosphere microbiome after pathogen attack. J Ecol. 2016;104:1566–75.Article 
    CAS 

    Google Scholar 
    56.Kong HG, Kim BK, Song GC, Lee S, Ryu C-M. Aboveground whitefly infestation-mediated reshaping of the root microbiota. Front Microbiol. 2016;7:1314.PubMed 
    PubMed Central 

    Google Scholar 
    57.Berendsen RL, Vismans G, Yu K, Song Y, de Jonge R, Burgman WP, et al. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 2018;12:1496–507.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    58.Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Pieterse CM, de Jonge R, Berendsen RL. The soil-borne supremacy. Trends Plant Sci. 2016;21:171–3.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Lämke J, Bäurle I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 2017;18:124.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    61.Cominelli E, Conti L, Tonelli C, Galbiati M. Challenges and perspectives to improve crop drought and salinity tolerance. N. Biotechnol. 2013;30:355–61.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, et al. Stress tolerance in plants via habitat adapted symbiosis. ISME J. 2008;2:404–16.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Hamilton EW III, Frank DA. Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology. 2001;82:2397–402.Article 

    Google Scholar 
    64.Cipollini D, Rigsby CM, Barto EK. Microbes as targets and mediators of allelopathy in plants. J Chem Ecol. 2012;38:714–27.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Ahmed V, Verma MK, Gupta S, Mandhan V, Chauhan NS. Metagenomic profiling of soil microbes to mine salt stress tolerance genes. Front Microbiol. 2018;9:159.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Troost TA, Kooi BW, Kooijman SALM. When do mixotrophs specialize? Adaptive dynamics theory applied to a dynamic energy budget model. Math Biosci. 2005;193:159–82.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    67.Venceslau SS, Lino RR, Pereira IA. The Qrc membrane complex, related to the alternative complex III, is a menaquinone reductase involved in sulfate respiration. J Biol Chem. 2010;285:22774–83.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Numan M, Bashir S, Khan Y, Mumtaz R, Shinwari ZK, Khan AL, et al. Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review. Microbiol Res. 2018;209:21–32.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    69.Kumar M, Etesami H, Kumar V, editors. Saline soil-based agriculture by halotolerant microorganisms. Singapore: Springer Nature Singapore Pte Ltd; 2019.
    Google Scholar 
    70.Etesami H, Glick BR. Halotolerant plant growth–promoting bacteria: Prospects for alleviating salinity stress in plants. Environ Exp Bot. 2020;23:104124.Article 
    CAS 

    Google Scholar 
    71.van der Heijden MG, Schlaeppi K. Root surface as a frontier for plant microbiome research. Proc Natl Acad Sci USA. 2015;112:2299–300.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    72.Bakhshandeh E, Gholamhosseini M, Yaghoubian Y, Pirdashti H. Plant growth promoting microorganisms can improve germination, seedling growth and potassium uptake of soybean under drought and salt stress. Plant Growth Regul. 2020;90:123–36.CAS 
    Article 

    Google Scholar 
    73.Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. Defining the core Arabidopsis thaliana root microbiome. Nature. 2012;488:86–90.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.van Elsas JD, Chiurazzi M, Mallon CA, Elhottovā D, Krištůfek V, Salles JF. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci USA. 2012;109:1159–64.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun. 2016;7:10541.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Matos A, Kerkhof L, Garland JL. Effects of microbial community diversity on the survival of Pseudomonas aeruginosa in the wheat rhizosphere. Micro Ecol. 2005;49:257–64.CAS 
    Article 

    Google Scholar 
    77.Hol WHG, de Boer W, Termorshuizen AJ, Meyer KM, Schneider JHM, et al. Reduction of rare soil microbes modifies plant–herbivore interactions. Ecol Lett. 2010;13:292–301.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    78.Saleem M, Hu J, Jousset A. More than the sum of its parts: microbiome biodiversity as a driver of plant growth and soil health. Annu Rev Ecol Evol Syst. 2019;50:145–68.Article 

    Google Scholar 
    79.Fan P, Chen D, He Y, Zhou Q, Tian Y, Gao L. Alleviating salt stress in tomato seedlings using Arthrobacter and Bacillus megaterium isolated from the rhizosphere of wild plants grown on saline–alkaline lands. Int J Phytoremediat. 2016;18:1113–21.CAS 
    Article 

    Google Scholar 
    80.Misra S, Dixit VK, Mishra SK, Chauhan PS. Demonstrating the potential of abiotic stress-tolerant Jeotgalicoccus huakuii NBRI 13E for plant growth promotion and salt stress amelioration. Ann Microbiol. 2019;69:419–34.CAS 
    Article 

    Google Scholar 
    81.Gest H. The discovery of microorganisms by Robert Hooke and Antoni van Leeuwenhoek, fellows of the Royal Society. Notes Rec R Soc Lond. 2004;58:187–201.PubMed 
    Article 
    PubMed Central 

    Google Scholar  More

  • in

    Olfactory signals and fertility in olive baboons

    1.Andersson, M. Sexual Selection (Princeton University Press, 1994).
    Google Scholar 
    2.van Schaik, C. P., van Noordwijk, M. A. & Nunn, C. L. Sex and social evolution in primates. In Comparative Primate Socioecology (ed. Lee, P. C.) 204–240 (Cambridge University Press, Cambridge, 2000).
    Google Scholar 
    3.Nunn, C. L. The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim. Behav. 58, 246–299 (1999).Article 

    Google Scholar 
    4.Pagel, M. The evolution of conspicuous oestrous advertisement in Old World monkeys. Anim. Behav. 47, 1333–1341 (1994).Article 

    Google Scholar 
    5.Kücklich, M., Weiß, B. M., Birkemeyer, C., Einspanier, A. & Widding, A. Chemical cues of female fertility states in a non-human primate. Sci. Rep. 9, 131716 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    6.Maestripieri, D. & Roney, J. Primate copulation calls and postcopulatory female choice. Behav. Ecol. 16, 106–113 (2004).Article 

    Google Scholar 
    7.Semple, S. & McComb, K. Perception of female reproductive state from vocal cues in a mammal species. Proc. R Soc. Lond. B 267, 707–712 (2000).CAS 
    Article 

    Google Scholar 
    8.Street, S. E., Cross, C. P. & Brown, G. R. Exaggerated sexual swellings in female nonhuman primates are reliable signals of female fertility and body condition. Anim. Behav. 112, 203–212 (2016).Article 

    Google Scholar 
    9.Tiddi, B., Wheeler, B. C. & Heistermann, M. Female behavioral proceptivity functions as a probabilistic signal of fertility, not female quality, in a New World primate. Horm. Behav. 73, 148–155 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Aujard, F., Heistermann, M., Thierry, B. & Hodges, J. K. Functional significance of behavioral, morphological, and endocrine correlates across the ovarian cycle in semifree ranging female Tonkean macaques. Am. J. Primatol. 46, 285–309 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Engelhardt, A., Hodges, J. K., Niemitz, C. & Heistermann, M. Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Horm. Behav. 47, 195–204 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Heistermann, M. et al. Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am. J. Primatol. 70, 44–53 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Garcia, C., Shimizu, K. & Huffman, M. Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata). Am. J. Primatol. 71, 868–879 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Heistermann, M. et al. Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proc. Biol. Sci. B 268, 2445–2451 (2001).CAS 
    Article 

    Google Scholar 
    15.Ostner, J. et al. What Hanuman langur males know about female reproductive status. Am. J. Primatol. 68, 701–712 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Bielert, C. & Anderson, C. M. Baboon sexual swellings and male response: A possible operational mammalian supernormal stimulus and response interaction. Int. J. Primatol. 6, 377–393 (1985).Article 

    Google Scholar 
    17.Brauch, K. et al. Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Horm. Behav. 52, 375–383 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Higham, J. P., MacLarnon, A. M., Ross, C., Heistermann, M. & Semple, S. Baboon sexual swellings: Information content of size and color. Horm. Behav. 53, 452–462 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Higham, J. P., Semple, S., MacLarnon, A., Heistermann, M. & Ross, C. Female reproductive signals, and male mating behavior in the olive baboon. Horm. Behav. 55, 60–67 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Thomas, M. L. Detection of female mating status using chemical signals and cues. Biol. Rev. Camb. Philos. Soc. 86, 1–13 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Dixson, A. F. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings (Oxford University Press, 2012).
    Google Scholar 
    22.Dulac, C. & Torello, A. T. Molecular detection of pheromone signals in mammals: From genes to behaviour. Nat. Rev. Neurosci. 4, 551–562 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Gilad, Y., Wiebe, V., Prezeworski, M., Lancet, D. & Pääbo, S. Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS. Biol. 2, 0120–0125 (2004).CAS 
    Article 

    Google Scholar 
    24.Negus, V. The Comparative Anatomy and Physiology of the Nose and Paranasal Sinuses (Livingston, 1958).
    Google Scholar 
    25.Dominy, N. J. & Lucas, P. W. Ecological importance of trichromatic vision to primates. Nature 410, 363–366 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Fornalé, F., Vaglio, S., Spiezio, C. & Prato Previde, E. Red-green colour vision in three catarrhine primates. Commun. Integr. Biol. 5, 583–589 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Gerald, M. S. How color may guide the primate world: Possible relationships between sexual selection and sexual dichromatism. In Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions (ed. Jones, C. B.) (American Society of Primatologists, 2003).
    Google Scholar 
    28.Porter, R. H. & Moore, J. D. Human kin recognition by olfactory cues. Physiol. Behav. 27, 493–495 (1981).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Geissman, T. & Hulftegger, A. M. Olfactory communication in gibbons? In Current Primatology: Social Development, Learning and Behaviour (eds Roeder, J. J. et al.) 199–206 (Université Louis Pasteur Press, 1994).
    Google Scholar 
    30.Wedekind, C., Seebeck, T., Bettens, F. & Paepke, A. J. MHC-dependent mate preferences in humans. Proc. Biol. Sci. B 260, 245–249 (1995).CAS 
    Article 

    Google Scholar 
    31.Wedekind, C. & Füri, S. Body odour preferences in men and women: Do they aim for specific MHC combinations or simply heterozygosity?. Proc. Biol. Sci. B 264, 1471–1479 (1997).CAS 
    Article 

    Google Scholar 
    32.Smith, T. et al. The existence of the vomeronasal organ in postnatal chimpanzees and evidence for its homology to that of humans. J. Anat. 198, 77–82 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Jacob, S., McClintock, M. K., Zelano, B. & Ober, C. Paternally inherited HLA alleles are associated with women’s choice of male odor. Nat. Genet. 30, 175–179 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Klailova, M. & Lee, P. C. Wild western lowland gorillas signal selectively using odor. PLoS ONE 9, e99554 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    35.Masi, S. & Bouret, S. Odor signals in wild western lowland gorillas: An involuntary and extra-group communication hypothesis. Physiol. Behav. 145, 123–126 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Henkel, S. & Setchell, J. M. Group and kin recognition via olfactory cues in chimpanzees (Pan troglodytes). Proc. Biol. Sci. B 285, 20181527 (2018).
    Google Scholar 
    37.Weiß, B. M. et al. Chemical composition of axillary odorants reflects social and individual attributes in rhesus macaques. Behav. Ecol. Sociobiol. 72, 65 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Jänig, S., Weiß, B. M., Birkemeyer, C. & Widding, A. Comprative chemical analysis of body odor in great apes. Am. J. Primatol. 81, e22976 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Setchell, J. M. et al. Chemical composition of scent-gland secretions in an Old World monkey (Mandrillus sphinx): Influence of sex, male status, and individual identity. Chem. Sens. 35, 205–220 (2010).CAS 
    Article 

    Google Scholar 
    40.Vaglio, S. et al. Sternal gland scent-marking signals sex, age, rank and group identity in captive mandrills. Chem. Sens. 41, 177–186 (2016).
    Google Scholar 
    41.Clarke, P. M., Barrett, L. & Henzi, S. P. What role do olfactory cues play in chacma baboon mating?. Am. J. Primatol. 71, 493–502 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Crawford, J. C., Boulet, M. & Drea, C. M. Smelling wrong: Hormonal contraception in lemurs alters critical female odour cues. Proc. Biol. Sci. B 278, 122–130 (2011).CAS 

    Google Scholar 
    43.Scordato, E. S., Dubay, G. & Drea, C. M. Chemical composition of scent marks in the ringtailed lemur (Lemur catta): Glandular differences, seasonal variation, and individual signatures. Chem. Sens. 32, 493–504 (2007).CAS 
    Article 

    Google Scholar 
    44.Rahaman, H. & Parthasarathy, M. D. The role of olfactory signals in the mating behaviour of bonnet monkeys, Macaca radiata. Commun. Behav. Biol. 6, 97–104 (1971).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Michael, R. P. & Keverne, E. B. Pheromones in the communication of sexual status in primates. Nature 218, 746–749 (1968).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Michael, R. P. & Keverne, E. B. Primate sex pheromones of vaginal origin. Nature 225, 84–85 (1970).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Michael, R. P. Hormonal steroids and sexual communication in primates. J. Steroid. Biochem. 6, 161–170 (1975).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Goldfoot, D. A., Kravetz, M. A., Goy, R. W. & Freeman, S. K. Lack of effect of vaginal lavages and aliphatic acids on ejaculatory responses in rhesus monkeys: Behavioral and chemical analyses. Horm. Behav. 7, 1–27 (1976).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Havlíček, J., Dvořáková, R., Bartoš, L. & Flegr, J. Non-advertised does not mean concealed: Body odour changes across the human menstrual cycle. Ethology 112, 81–90 (2006).Article 

    Google Scholar 
    50.Doty, R. L., Ford, M., Preti, G. & Huggins, G. R. Changes in the intensity and pleasantness of human vaginal odors during the menstrual cycle. Science 190, 1316–1318 (1975).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Kuukasjarvi, S. et al. Attractiveness of women’s body odors over the menstrual cycle: The role of oral contraceptives and receiver sex. Behav. Ecol. 15, 579–584 (2004).Article 

    Google Scholar 
    52.Singh, D. & Bronstad, P. M. Female body odour is a potential cue to ovulation. Proc. R. Soc. Lond. B 268, 797–801 (2001).CAS 
    Article 

    Google Scholar 
    53.Cerda-Molina, A. L., Hernández-López, L., Rojas-Maya, S., Murcia-Mejía, C. & Mondragón-Ceballos, R. Male-induced sociosexual behaviour by vaginal secretions in Macaca arctoides. Int. J. Primatol. 27, 791–807 (2006).Article 

    Google Scholar 
    54.Robinson, J. G. Intrasexual competition and mate choice in primates. Am. J. Primatol. 3, 131–144 (1982).Article 

    Google Scholar 
    55.Penn, D. J. et al. Individual and gender fingerprints in human body odour. J. R. Soc. Interface 4, 331–340 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Smith, T. & Abbott, D. Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus). Am. J. Primatol. 46, 265–284 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Spence-Aizenberg, A., Kimball, B. A., Williams, L. E. & Fernandez-Duque, E. Chemical composition of glandular secretions from a pair-living monogamous primate: Sex, age, and gland differences in captive and wild owl monkeys (Aotus spp.). Am. J. Primatol. 80, e22730 (2018).Article 

    Google Scholar 
    58.Setchell, J. M. Sexual selection and the differences between the sexes in mandrills (Mandrillus sphinx). Yearb. Phys. Anthropol. 159, S105–S129 (2016).Article 

    Google Scholar 
    59.Higham, J. P., Heistermann, M., Ross, C., Semple, S. & MacIarnon, A. The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons. Primates 49, 295–299 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Hasson, O. Towards a general theory of biological signalling. J. Theor. Biol. 185, 139–156 (1997).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Packer, C., Tatar, M. & Collins, A. Reproductive cessation in female mammals. Nature 392, 807–811 (1998).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Melnick, D. C. & Pearl, M. C. Cercopithecines in multimale groups: Genetic diversity and population structure. In Primate Societies (eds Smuts, B. B. et al.) 121–134 (University of Chicago Press, 1987).
    Google Scholar 
    63.Honoré, E. K. & Tardif, S. D. Reproductive biology of baboons. In The Baboon in Biomedical Research (eds VandeBerg, J. L. et al.) 89–110 (Springer-Verlag, 2009).
    Google Scholar 
    64.Pomerantz, O. & Terkel, J. Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). Am. J. Primatol. 71, 687–695 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Bercovitch, F. B. Reproductive Tactics in Adult Female and Adult Male Olive Baboons. (Ph.D. thesis, University of California, 1985).66.Hendrickx, A. G. & Kraemer, D. C. Observation of the menstrual cycle, optimal mating time, and preimplantation embryos of the baboon. J. Reprod. Fert. S6, 119–128 (1969).
    Google Scholar 
    67.Koyama, T., De La Pena, A. & Hagino, N. Plasma estrogen, progestin, and luteinizing hormone during the normal menstrual cycle in the baboon: Role of luteinizing hormone. Am. J. Obstet. Gynecol. 127, 67–71 (1977).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Shaikh, A. A., Celaya, C. L., Gomez, I. & Shaikh, S. A. Temporal relationship of hormonal peaks to ovulation and sex skin deturgescence in the baboon. Primates 23, 444–452 (1982).CAS 
    Article 

    Google Scholar 
    69.Vaglio, S. et al. Female copulation calls vary with male ejaculation in captive olive baboons. Behaviour 157, 807–822 (2020).Article 

    Google Scholar 
    70.Shambayati, B. Cytopathology (Oxford University Press, 2011).
    Google Scholar 
    71.Wilcox, A. J., Weingberg, C. R. & Baird, D. D. Timing of sexual intercourse in relation to ovulation: Effects on the probability of conception, survival of the pregnancy and sex of the baby. N. Engl. J. Med. 333, 189–194 (1995).Article 

    Google Scholar 
    72.Walker, D. & Vaglio, S. Sampling and analysis of animal scent signals. J. Vis. Exp. 168, e60902 (2021).
    Google Scholar 
    73.El‐Sayed, A. The Pherobase: Database of Pheromones and Semiochemicals. www.pherobase.com (2016).74.Oksanen, J. et al. VEGAN: Community Ecology Package. R Package Version 2.5-5 (2019).75.R Studio Team R Studio: Integrated Development for R (2019).76.R Core Team R: A language and Environment for Statistical Computing (2018).77.StataCorp. Stata Statistical Software, 16th Release (2019).78.Mundry, R. & Sommer, C. Discriminant function analysis with nonindependent data: Consequences and an alternative. Anim. Behav. 74, 965–976 (2007).Article 

    Google Scholar 
    79.Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S (Springer, 2002).
    Google Scholar 
    80.Breslow, N. E. & Clayton, D. G. Approximate inference in generalized linear mixed models. J. Am. Stat. Ass. 88, 9–25 (1993).MATH 

    Google Scholar 
    81.Bell, B. A., Morgan, G. B., Schoeneberger, J. A. & Loudermilk, B. L. Dancing the sample size limbo with mixed models: How low can you go? SAS Global Forum, Paper 197 (2010).82.Heymann, E. W. The neglected sense-olfaction in primate behavior, ecology, and evolution. Am. J. Primatol. 68, 519–524 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    83.Hayes, R., Morelli, T. & Wright, P. Anogenital gland secretions of Lemur catta and Propithecus verreauxi coquereli: A preliminary chemical examination. Am. J. Primatol. 63, 49–62 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Janda, E. D., Perry, K., Hankinson, E., Walker, D. & Vaglio, S. Sex differences in scent-marking in captive red-ruffed lemurs. Am. J. Primatol. 81, 60–68 (2019).Article 

    Google Scholar 
    85.Smith, T., Tomlinson, A., Mlotkiewicz, J. & Abbott, D. Female marmoset monkeys (Callithrix jacchus) can be identified from the chemical composition of their scent marks. Chem. Sens. 26, 449–458 (2001).CAS 
    Article 

    Google Scholar 
    86.Hurst, J. L., Robertson, D., Tolladay, U. & Beynon, J. Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim. Behav. 55, 1289–1297 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    87.Belcher, A. M. et al. Proteins: biologically relevant components of the scent marks of a primate (Saguinus fuscicollis). Chem. Sens. 15, 431–446 (1990).CAS 
    Article 

    Google Scholar 
    88.Doty, R. L. Olfactory communication in humans. Chem. Sens. 6, 351–376 (1981).Article 

    Google Scholar 
    89.Curtis, R. F., Ballantine, J. A., Keverne, E. B., Bonsall, R. W. & Michael, R. P. Identification of primate sexual pheromones and the properties of synthetic attractants. Nature 232, 396–398 (1971).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    90.Jha, S. K., Marina, N., Liu, C. & Hayashi, K. Human body odor discrimination by GC-MS spectra data mining. Anal. Methods 7, 9549–9561 (2015).CAS 
    Article 

    Google Scholar 
    91.Balcerzak, L., Gibka, J., Sikora, M., Kula, J. & Strub, D. J. Minor constituents of essential oils and aromatic extracts. Oximes derived from natural flavor and fragrance raw materials: Sensory evaluation, spectral and gas chromatographic characteristics. Food Chem. 301, 125283 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    92.Baker, M. Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). Am. J. Primatol. 38, 263–270 (1996).Article 

    Google Scholar 
    93.Wyatt, T. Pheromones and Animal Behaviour. Chemical Signal and Signatures (Cambridge University Press, 2014).
    Google Scholar 
    94.DelBarco-Trillo, J., Harelimana, I. H., Goodwin, T. E. & Drea, C. M. Chemical differences between voided and bladder urine in the aye-aye (Daubentonia madagascariensis): Implications for olfactory communication studies. Am. J. Primatol. 75, 695–702 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    95.Smith, T. Individual olfactory signatures in common marmosets (Callithrix jacchus). Am. J. Primatol. 68, 585–604 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    96.Drea, C. M. Design, delivery and perception of conditiondependent chemical signals in strepsirrhine primates: Implications for human olfactory communication. Phil. Trans. R. Soc. B 375, 20190264 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    97.Poirier, A. C. et al. On the trail of primate scent signals: A field analysis of callitrichid scent-gland secretions by portable gas chromatography-mass spectrometry. Am. J. Primatol. 1, e23236 (2021).
    Google Scholar 
    98.Mason, R. T. & Parker, M. R. Social behaviour and pheromonal communication in reptiles. J. Comp. Physiol. A 196, 729–749 (2010).CAS 
    Article 

    Google Scholar 
    99.Shirasu, M. & Touhara, K. The scent of disease: Volatile organic compounds of the human body related to disease and disorder. J. Biochem. 150, 257–266 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    100.Rivera, A. J., Stumpf, R. M., Wilson, B., Leigh, S. & Salyers, A. A. Baboon vaginal microbiota: An overlooked aspect of primate physiology. Am. J. Primatol. 72, 467–474 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    101.Pener, M. P. & Simpson, S. J. Locust phase polyphenism: An update. Adv. Insect Physiol. 36, 1–272 (2009).Article 

    Google Scholar 
    102.Andersson, J., Borg-Karlson, A. K. & Wiklund, C. Antiaphrodisiacs in pierid butterflies: A theme with variation!. J. Chem. Ecol. 29, 1489–1499 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    103.Ramirez, S. R. et al. Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333, 1742–1746 (2011).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    104.Rigaill, L., Higham, J. P., Lee, P. C., Blin, A. & Garcia, C. Multimodal sexual signaling and mating behavior in olive baboons (Papio anubis). Am. J. Primatol. 75, 774–787 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    105.Candolin, U. The use of multiple cues in mate choice. Biol. Rev. Camb. Philos. Soc. 78, 575–595 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    106.Johnstone, R. A., Reynolds, J. D. & Deutsch, J. C. Mutual mate choice and sex differences in choosiness. Evolution 50, 1382–1391 (1996).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    107.Johnstone, R. A. Multiple displays in animal communication: “Backup signals” and “multiple messages”. Phil. Trans. R. Soc. B 351, 329–338 (1996).ADS 
    Article 

    Google Scholar 
    108.Greene, L. K. et al. Mix it and fix it: Functions of composite olfactory signals in ring-tailed lemurs. R. Soc. Open Sci. 3, 160076 (2016).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    109.Mitro, S., Gordon, A. R., Olsson, M. J. & Lundström, J. N. The smell of age: Perception and discrimination of body odors of different ages. PLoS ONE 7(5), e38110 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    110.Beauchamp, G. K. & Yamazaki, K. Chemical signalling in mice. Biochem. Soc. Trans. 31, 147–151 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    111.Kean, E. F., Muller, C. T. & Chadwick, E. A. Otter scent signals age, sex, and reproductive status. Chem. Sens. 36, 555–564 (2011).CAS 
    Article 

    Google Scholar 
    112.MacDonald, E. A., Fernandez-Duque, E., Evans, S. & Hagey, L. R. Sex, age, and family differences in the chemical composition of owl monkey (Aotus nancymaae) subcaudal scent secretions. Am. J. Primatol. 70, 12–18 (2007).Article 
    CAS 

    Google Scholar 
    113.Osada, K. et al. The scent of age. Proc. R. Soc. Lond. B 270, 929–933 (2003).CAS 
    Article 

    Google Scholar 
    114.White, A. M., Swaisgood, R. R. & Zhang, H. Chemical communication in the giant panda (Ailuropoda melanoleuca): The role of age in the signaller and assessor. J. Zool. 259, 171–178 (2006).Article 

    Google Scholar 
    115.Anderson, C. M. Female age: Male preference and reproductive success in primates. Int. J. Primatol. 7, 305–326 (1986).Article 

    Google Scholar 
    116.Cant, A. C. & Young, A. J. Resolving social conflict among females without overt aggression. Phil. Trans. R. Soc. B 368, 20130076 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    117.Alberts, S. C., Altmann, J. & Wilson, M. L. Mate guarding constrains foraging activity of male baboons. Anim. Behav. 51, 1269–1277 (1996).Article 

    Google Scholar 
    118.Brennan, P. A. & Kendrick, K. M. Mammalian social odours: attraction and individual recognition. Phil. Trans. R. Soc. B 361, 2061–2078 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    119.Wyatt, T. Pheromones and Animal Behaviour (Cambridge University Press, 2003).
    Google Scholar 
    120.Thom, M. D. & Hurst, J. L. Individual recognition by scent. Ann. Zool. Fenn. 41, 765–787 (2004).
    Google Scholar 
    121.Setchell, J. M., Lee, P. C., Wickings, E. J. & Dixson, A. F. Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). Am. J. Phys. Anthropol. 115, 349–360 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    122.Palagi, E. & Dapporto, L. Beyond odor discrimination: Demonstrating individual recognition by scent in Lemur catta. Chem. Sens. 31, 437–443 (2006).Article 

    Google Scholar 
    123.Epple, G., Kuderling, I. & Belcher, A. M. Some communicatory functions of scent marking in the cotton-top tamarin Saguinus oedipus oedipus. J. Chem. Ecol. 14, 503–515 (1988).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    124.Laska, M., Genzel, D. & Wieser, A. The number of functional olfactory receptor genes and the relative size of olfactory brain structures are poor predictors of olfactory discrimination performance with enantiomers. Chem. Sens. 30, 171–175 (2005).CAS 
    Article 

    Google Scholar  More

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    Individual and collective foraging in autonomous search agents with human intervention

    Loose coupling and human intervention promote collective foraging successWe first determined group search performance by assessing the average search time, consumption time, and total targets found in each movement condition with and without intervention.Results showed that search performance as measured by mean trial time was better with loose coupling and human intervention, as seen in the lowest average trial times in Fig. 3. Movement type had a reliable effect on performance without human intervention, F(1,59) = 27.65, p  More

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    Combined effects of crude oil exposure and warming on eggs and larvae of an arctic forage fish

    1.IPCC. The Ocean and Cryosphere in a changing Climate—Summary for Policymakers (2019).2.Carmack, E. et al. Toward quantifying the increasing role of oceanic heat in sea ice loss in the new arctic. Bull. Am. Meteorol. Soc. 96, 2079–2105 (2015).ADS 
    Article 

    Google Scholar 
    3.Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315 (2008).PubMed 
    Article 

    Google Scholar 
    4.Borgå, K. The Arctic ecosystem: a canary in the coal mine for global multiple stressors. Environ. Toxicol. Chem. 38, 487–488 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    5.Lind, S., Ingvaldsen, R. B. & Furevik, T. Arctic warming hotspot in the northern Barents Sea linked to declining sea-ice import. Nat. Clim. Change 8, 634–639 (2018).ADS 
    Article 

    Google Scholar 
    6.Onarheim, I. H., Eldevik, T., Smedsrud, L. H. & Stroeve, J. C. Seasonal and regional manifestation of Arctic Sea ice loss. J. Clim. 31, 4917–4932 (2018).ADS 
    Article 

    Google Scholar 
    7.Screen, J. A. & Simmonds, I. Increasing fall-winter energy loss from the Arctic Ocean and its role in Arctic temperature amplification. Geophys. Res. Lett. 37, 1–5 (2010).Article 

    Google Scholar 
    8.Onarheim, I. H. & Årthun, M. Toward an ice-free Barents Sea. Geophys. Res. Lett. 44, 8387–8395 (2017).ADS 
    Article 

    Google Scholar 
    9.Champine, R. D., Morris, R. & Elder, S. The melting Arctic is now open for business. National Geographic Magazine (2019).10.Orourke, R. et al. Changes in the Arctic: Background and Issues for Congress 129 (DIANE Publishing, 2020).
    Google Scholar 
    11.Eriksen, E., Huserbråten, M., Gjøsæter, H., Vikebø, F. & Albretsen, J. Polar cod egg and larval drift patterns in the Svalbard archipelago. Polar Biol. https://doi.org/10.1007/s00300-019-02549-6 (2019).Article 

    Google Scholar 
    12.Eguíluz, V. M., Fernández-Gracia, J., Irigoien, X. & Duarte, C. M. A quantitative assessment of Arctic shipping in 2010–2014. Sci. Rep. 6, 30682 (2016).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    13.Ellis, B., & Brigham, L. Arctic Marine Shipping Assessment 2009 Report. (2009).14.Pörtner, H.-O. & Farrell, A. P. Physiology and climate change. Science 322, 690–692 (2008).PubMed 
    Article 

    Google Scholar 
    15.Pollino, C. A. & Holdway, D. A. Toxicity testing of crude oil and related compounds using early life stages of the crimson-spotted rainbowfish (Melanotaenia fluviatilis). Ecotoxicol. Environ. Saf. 52, 180–189 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Miller, B. & Kendall, A. W. Early Life History of Marine Fishes (University of California Press, 2009). https://doi.org/10.1525/9780520943766.
    Google Scholar 
    17.Dahlke, F. T. et al. Northern cod species face spawning habitat losses if global warming exceeds 1.5°C. Sci. Adv. 4, 8821 (2018).ADS 
    Article 
    CAS 

    Google Scholar 
    18.Petersen, G. I. & Kristensen, P. Bioaccumulation of lipophilic substances in fish early life stages. Environ. Toxicol. Chem. 17, 1385–1395 (1998).CAS 
    Article 

    Google Scholar 
    19.Dahlke, F. T., Wohlrab, S., Butzin, M. & Pörtner, H.-O. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369, 65–70 (2020).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    20.Jung, J.-H. et al. Differential toxicokinetics determines the sensitivity of two marine embryonic fish exposed to Iranian heavy crude oil. Environ. Sci. Technol. 49, 13639–13648 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Ingvarsdóttir, A. et al. Effects of different concentrations of crude oil on first feeding larvae of Atlantic herring (Clupea harengus). J. Mar. Syst. 93, 69–76 (2012).Article 

    Google Scholar 
    22.Pasparakis, C., Esbaugh, A. J., Burggren, W. & Grosell, M. Physiological impacts of deepwater horizon oil on fish. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 224, 108558 (2019).CAS 
    Article 

    Google Scholar 
    23.Steiner, N. S. et al. Impacts of the changing ocean-sea ice system on the key forage fish arctic cod (Boreogadus saida) and subsistence fisheries in the western Canadian arctic—evaluating linked climate, ecosystem and economic (CEE) models. Front. Mar. Sci. 6, 179 (2019).Article 

    Google Scholar 
    24.Kortsch, S., Primicerio, R., Fossheim, M., Dolgov, A. V. & Aschan, M. Climate change alters the structure of arctic marine food webs due to poleward shifts of boreal generalists. Proc. R. Soc. B Biol. Sci. 282, 20151546 (2015).Article 

    Google Scholar 
    25.Harter, B. B., Elliott, K. H., Divoky, G. J. & Davoren, G. K. Arctic cod (Boreogadus saida) as prey: fish length-energetics relationships in the Beaufort Sea and Hudson Bay. Arctic 66, 191–196 (2013).Article 

    Google Scholar 
    26.Graham, M. & Hop, H. Aspects of reproduction and larval biology of Arctic cod (Boreogadus saida). Arctic 48, 130–135 (1995).Article 

    Google Scholar 
    27.Gradinger, R. R. & Bluhm, B. A. In-situ observations on the distribution and behavior of amphipods and Arctic cod (Boreogadus saida) under the sea ice of the High Arctic Canada Basin. Polar Biol. 27, 595–603 (2004).Article 

    Google Scholar 
    28.Laurel, B. J., Copeman, L. A., Spencer, M. & Iseri, P. Comparative effects of temperature on rates of development and survival of eggs and yolk-sac larvae of Arctic cod (Boreogadus saida) and walleye pollock (Gadus chalcogrammus). ICES J. Mar. Sci. 75, 2403–2412 (2018).Article 

    Google Scholar 
    29.ICES. Report of the Arctic Fisheries Working Group. 859 http://www.ices.dk/sites/pub/Publication%20Reports/Expert%20Group%20Report/acom/2018/AFWG/00-AFWG%202018%20Report.pdf (2018).30.Eriksen, E., Ingvaldsen, R. B., Nedreaas, K. & Prozorkevich, D. The effect of recent warming on polar cod and beaked redfish juveniles in the Barents Sea. Reg. Stud. Mar. Sci. 2, 105–112 (2015).Article 

    Google Scholar 
    31.Astthorsson, O. S. Distribution, abundance and biology of polar cod, Boreogadus saida, in Iceland–East Greenland waters. Polar Biol. 39, 995–1003 (2016).Article 

    Google Scholar 
    32.Divoky, G. J., Lukacs, P. M. & Druckenmiller, M. L. Effects of recent decreases in arctic sea ice on an ice-associated marine bird. Prog. Oceanogr. 136, 151–161 (2015).ADS 
    Article 

    Google Scholar 
    33.Hansen, M. O., Nielsen, T. G., Stedmon, C. A. & Munk, P. Oceanographic regime shift during 1997 in Disko Bay, Western Greenland. Limnol. Oceanogr. 57, 634–644 (2012).ADS 
    Article 

    Google Scholar 
    34.Nahrgang, J. et al. Gender specific reproductive strategies of an Arctic key species (Boreogadus saida) and implications of climate change. PLoS ONE 9, e98452 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    35.Huserbråten, M. B. O., Eriksen, E., Gjøsæter, H. & Vikebø, F. Polar cod in jeopardy under the retreating Arctic sea ice. Commun. Biol. 2, 1–8 (2019).Article 

    Google Scholar 
    36.Nahrgang, J. et al. Early life stages of an arctic keystone species (Boreogadus saida) show high sensitivity to a water-soluble fraction of crude oil. Environ. Pollut. 218, 605–614 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    37.Laurel, B. J. et al. Embryonic crude oil exposure impairs growth and lipid allocation in a keystone arctic forage fish. iScience 19, 1101–1113 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Politis, S. N. et al. Temperature effects on gene expression and morphological development of European eel, Anguilla anguilla larvae. PLoS ONE 12, e0182726 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    39.O’Dea, R. E., Lagisz, M., Hendry, A. P. & Nakagawa, S. Developmental temperature affects phenotypic means and variability: a meta-analysis of fish data. Fish Fish. 20, 1005–1022 (2019).Article 

    Google Scholar 
    40.Réalis-Doyelle, E., Pasquet, A., De Charleroy, D., Fontaine, P. & Teletchea, F. Strong effects of temperature on the early life stages of a cold stenothermal fish species, brown trout (Salmo trutta L.). PLoS ONE 11, e0155487 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    41.Réalis-Doyelle, E., Pasquet, A., Fontaine, P. & Teletchea, F. How climate change may affect the early life stages of one of the most common freshwater fish species worldwide: the common carp (Cyprinus carpio). Hydrobiologia 805, 365–375 (2018).Article 
    CAS 

    Google Scholar 
    42.Hicken, C. E. et al. Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. Proc. Natl. Acad. Sci. 108, 7086–7090 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    43.Carls, M. G., Rice, S. D. & Hose, J. E. Sensitivity of fish embryos to weathered crude oil: Part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval pacific herring (Clupea pallasi). Environ. Toxicol. Chem. 18, 481–493 (1999).CAS 
    Article 

    Google Scholar 
    44.Incardona, J. P. Molecular mechanisms of crude oil developmental toxicity in fish. Arch. Environ. Contam. Toxicol. 73, 19–32 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Sørhus, E. et al. Novel adverse outcome pathways revealed by chemical genetics in a developing marine fish. Elife 6, e20707 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Incardona, J. P. & Scholz, N. L. The influence of heart developmental anatomy on cardiotoxicity-based adverse outcome pathways in fish. Aquat. Toxicol. 177, 515–525 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Perrichon, P. et al. Combined effects of elevated temperature and Deepwater Horizon oil exposure on the cardiac performance of larval mahi–mahi, Coryphaena hippurus. PLoS ONE 13, e0203949 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    48.Pasparakis, C. et al. Combined effects of oil exposure, temperature and ultraviolet radiation on buoyancy and oxygen consumption of embryonic mahi–mahi, Coryphaena hippurus. Aquat. Toxicol. 191, 113–121 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    49.Pasparakis, C., Mager, E. M., Stieglitz, J. D., Benetti, D. & Grosell, M. Effects of Deepwater Horizon crude oil exposure, temperature and developmental stage on oxygen consumption of embryonic and larval mahi–mahi (Coryphaena hippurus). Aquat. Toxicol. 181, 113–123 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    50.Gunderson, A. R., Armstrong, E. J. & Stillman, J. H. Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Annu. Rev. Mar. Sci. 8, 357–378 (2016).ADS 
    Article 

    Google Scholar 
    51.McNicholl, D. G., Davoren, G. K., Majewski, A. R. & Reist, J. D. Isotopic niche overlap between co-occurring capelin (Mallotus villosus) and polar cod (Boreogadus saida) and the effect of lipid extraction on stable isotope ratios. Polar Biol. 41, 423–432 (2018).Article 

    Google Scholar 
    52.Kühn, S. et al. Plastic ingestion by juvenile polar cod (Boreogadus saida) in the Arctic Ocean. Polar Biol. 41, 1269–1278 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Bouchard, C. & Fortier, L. Circum-arctic comparison of the hatching season of polar cod Boreogadus saida: a test of the freshwater winter refuge hypothesis. Prog. Oceanogr. 90, 105–116 (2011).ADS 
    Article 

    Google Scholar 
    54.Laurel, B. J., Spencer, M., Iseri, P. & Copeman, L. A. Temperature-dependent growth and behavior of juvenile Arctic cod (Boreogadus saida) and co-occurring North Pacific gadids. Polar Biol. 39, 1127–1135 (2016).Article 

    Google Scholar 
    55.Drost, H. E. et al. Upper thermal limits of the hearts of Arctic cod Boreogadus saida : adults compared with larvae: boreogadus saida thermal limits. J. Fish Biol. 88, 718–726 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    56.Bender, M. L. et al. Effects of chronic dietary petroleum exposure on reproductive development in polar cod (Boreogadus saida). Aquat. Toxicol. 180, 196–208 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    57.Bender, M. L. et al. Effects of acute exposure to dispersed oil and burned oil residue on long-term survival, growth, and reproductive development in polar cod (Boreogadus saida). Mar. Environ. Res. 140, 468–477 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    58.Boehm, P. D., Neff, J. M. & Page, D. S. Assessment of polycyclic aromatic hydrocarbon exposure in the waters of Prince William Sound after the Exxon Valdez oil spill: 1989–2005. Mar. Pollut. Bull. 54, 339–356 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    59.Sammarco, P. W. et al. Distribution and concentrations of petroleum hydrocarbons associated with the BP/Deepwater Horizon Oil Spill, Gulf of Mexico. Mar. Pollut. Bull. 73, 129–143 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    60.Berenshtein, I. et al. Invisible oil beyond the Deepwater Horizon satellite footprint. Sci. Adv. 6, eaaw8863 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.Incardona, J. P. et al. Cardiac arrhythmia is the primary response of embryonic pacific herring (Clupea pallasi) exposed to crude oil during weathering. Environ. Sci. Technol. 43, 201–207 (2009).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    62.Incardona, J. P. et al. Exxon Valdez to Deepwater Horizon: comparable toxicity of both crude oils to fish early life stages. Aquat. Toxicol. Amst. Neth. 142–143, 303–316 (2013).Article 
    CAS 

    Google Scholar 
    63.de Soysa, T. Y. et al. Macondo crude oil from the Deepwater Horizon oil spill disrupts specific developmental processes during zebrafish embryogenesis. BMC Biol. 10, 40 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Incardona, J. P. et al. Very low embryonic crude oil exposures cause lasting cardiac defects in salmon and herring. Sci. Rep. 5, 13499 (2015).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Heintz, R. A. et al. Delayed effects on growth and marine survival of pink salmon Oncorhynchus gorbuscha after exposure to crude oil during embryonic development. Mar. Ecol. Prog. Ser. 208, 205–216 (2000).ADS 
    Article 

    Google Scholar 
    66.Sorheim, K. R. & Moldestad, M. O. Weathering properties of the Goliat Kobbe and two Goliat Blend of Kobbe and Realgrunnen crude oils. (2008).67.Sørensen, L., Melbye, A. G. & Booth, A. M. Oil droplet interaction with suspended sediment in the seawater column: influence of physical parameters and chemical dispersants. Mar. Pollut. Bull. 78, 146–152 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    68.Sørensen, L. et al. Accumulation and toxicity of monoaromatic petroleum hydrocarbons in early life stages of cod and haddock. Environ. Pollut. 251, 212–220 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    69.Meador, J. P. & Nahrgang, J. Characterizing crude oil toxicity to early-life stage fish based on a complex mixture: Are we making unsupported assumptions?. Environ. Sci. Technol. 53, 11080–11092 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Sørensen, L. et al. Oil droplet fouling and differential toxicokinetics of polycyclic aromatic hydrocarbons in embryos of Atlantic haddock and cod. PLoS ONE 12, e0180048 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    71.Carls, M. G. et al. Fish embryos are damaged by dissolved PAHs, not oil particles. Aquat. Toxicol. 88, 121–127 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Hansen, B. H. et al. Developmental effects in fish embryos exposed to oil dispersions—the impact of crude oil micro-droplets. Mar. Environ. Res. 150, 104753 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    73.Olsvik, P. A., Berntssen, M. H. G., Hylland, K., Eriksen, D. Ø. & Holen, E. Low impact of exposure to environmentally relevant doses of 226Ra in Atlantic cod (Gadus morhua) embryonic cells. J. Environ. Radioact. 109, 84–93 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    74.Sundby, S. & Kristiansen, T. The principles of buoyancy in marine fish eggs and their vertical distributions across the world oceans. PLoS ONE 10, e0138821 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    75.Spencer, M. L., Vestfals, C. D., Mueter, F. J. & Laurel, B. J. Ontogenetic changes in the buoyancy and salinity tolerance of eggs and larvae of polar cod (Boreogadus saida) and other gadids. Polar Biol. 18, 1141–1158. https://doi.org/10.1007/s00300-020-02620-7 (2020).Article 

    Google Scholar 
    76.Pasparakis, C., Wang, Y., Stieglitz, J. D., Benetti, D. D. & Grosell, M. Embryonic buoyancy control as a mechanism of ultraviolet radiation avoidance. Sci. Total Environ. 651, 3070–3078 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    77.Kent, D., Drost, H. E., Fisher, J., Oyama, T. & Farrell, A. P. Laboratory rearing of wild Arctic cod Boreogadus saida from egg to adulthood: rearing boreogadus saida from egg to adulthood. J. Fish Biol. 88, 1241–1248 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    78.Jordaan, A., Hayhurst, S. E. & Kling, L. J. The influence of temperature on the stage at hatch of laboratory reared Gadus morhua and implications for comparisons of length and morphology. J. Fish Biol. 68, 7–24 (2006).Article 

    Google Scholar 
    79.Porter, S. M. & Bailey, K. M. The effect of early and late hatching on the escape response of walleye pollock (Theragra chalcogramma) larvae. J. Plankton Res. 29, 291–300 (2007).Article 

    Google Scholar 
    80.Spicer, J. I., Tills, O., Truebano, M. & Rundle, S. D. Developmental plasticity and heterokairy. In Development and Environment (eds Burggren, W. & Dubansky, B.) 73–96 (Springer, 2018). https://doi.org/10.1007/978-3-319-75935-7_4.
    Google Scholar 
    81.Bouchard, C. et al. Climate warming enhances polar cod recruitment, at least transiently. Prog. Oceanogr. 156, 121–129 (2017).Article 

    Google Scholar 
    82.Koenker, B. L., Laurel, B. J., Copeman, L. A. & Ciannelli, L. Effects of temperature and food availability on the survival and growth of larval Arctic cod (Boreogadus saida) and walleye pollock (Gadus chalcogrammus). ICES J. Mar. Sci. 75, 2386–2402 (2018).Article 

    Google Scholar 
    83.Bouchard, C. & Fortier, L. The importance of Calanus glacialis for the feeding success of young polar cod: a circumpolar synthesis. Polar Biol. https://doi.org/10.1007/s00300-020-02643-0 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    84.Balazy, K., Trudnowska, E., Wichorowski, M. & Błachowiak-Samołyk, K. Large versus small zooplankton in relation to temperature in the Arctic shelf region. Polar Res. 37, 1427409 (2018).Article 

    Google Scholar 
    85.Weydmann, A. et al. Shift towards the dominance of boreal species in the Arctic: inter-annual and spatial zooplankton variability in the West Spitsbergen Current. Mar. Ecol. Prog. Ser. 501, 41–52 (2014).ADS 
    Article 

    Google Scholar 
    86.Marsh, J. M., Mueter, F. J. & Quinn, T. J. Environmental and biological influences on the distribution and population dynamics of polar cod (Boreogadus saida) in the US Chukchi Sea. Polar Biol. https://doi.org/10.1007/s00300-019-02561-w (2019).Article 

    Google Scholar 
    87.Lange, R. & Marshall, D. Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects. Sci. Rep. 7, 6281 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    88.Liess, M., Foit, K., Knillmann, S., Schäfer, R. B. & Liess, H.-D. Predicting the synergy of multiple stress effects. Sci. Rep. 6, 32965 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    89.du Sert, N. P. et al. Reporting animal research: explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol. 18, e3000411 (2020).Article 
    CAS 

    Google Scholar 
    90.Holst, J. C. & McDonald, A. FISH-LIFT: a device for sampling live fish with trawls. Fish. Res. 48, 87–91 (2000).Article 

    Google Scholar 
    91.Hall, T. E., Smith, P. & Johnston, I. A. Stages of embryonic development in the Atlantic cod Gadus morhua. J. Morphol. 259, 255–270 (2004).PubMed 
    Article 

    Google Scholar 
    92.Houde, E. D. Mortality. In Fishery Science (ed. Fuiman, L. A.) (Wiley, 1989).
    Google Scholar 
    93.Sørensen, L., Silva, M. S., Booth, A. M. & Meier, S. Optimization and comparison of miniaturized extraction techniques for PAHs from crude oil exposed Atlantic cod and haddock eggs. Anal. Bioanal. Chem. 408, 1023–1032 (2016).PubMed 
    Article 
    CAS 

    Google Scholar 
    94.Sørensen, L., Meier, S. & Mjøs, S. A. Application of gas chromatography/tandem mass spectrometry to determine a wide range of petrogenic alkylated polycyclic aromatic hydrocarbons in biotic samples. Rapid Commun. Mass Spectrom. 30, 2052–2058 (2016).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    95.Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 45e–445 (2001).Article 

    Google Scholar 
    96.Riley, P. & Skirrow, G. Chemical Oceanography 56–74 (Academic Press, 1975).
    Google Scholar 
    97.Laurel, B. J., Copeman, L. A., Hurst, T. P. & Parrish, C. C. The ecological significance of lipid/fatty acid synthesis in developing eggs and newly hatched larvae of Pacific cod (Gadus macrocephalus). Mar. Biol. 157, 1713–1724 (2010).CAS 
    Article 

    Google Scholar 
    98.Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    99.Wassenberg, D. M. & Di Giulio, R. T. Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ. Health Perspect. 112, 1658–1664 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    100.R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, version 2018). https://www.R-project.org/.101.Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & Van Willigen, B. nlme: Linear and Nonlinear Mixed Effects Models. (2020).102.Pinheiro, J. & Bates, D. Fitting linear mixed-effects models. In Mixed-Effects Models in S and S-Plus 133–199 (Springer, 2000).103.Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).
    Google Scholar 
    104.Folt, C. L., Chen, C. Y., Moore, M. V. & Burnaford, J. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 44, 864–877 (1999).ADS 
    Article 

    Google Scholar 
    105.Wasserstein, R. L., Schirm, A. L. & Lazar, N. A. Moving to a world beyond “p < 0.05”. Am. Stat. 73, 1–19 (2019).MathSciNet  Article  Google Scholar  106.Amrheim, V., Greenland, S. & McShane, B. Time to retire statistical significance Nature2019.pdf. Nature 567, 305–307 (2019).ADS  Article  CAS  Google Scholar  More