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    Rethinking the complexity and uncertainty of spatial networks applied to forest ecology

    Bonan, G. B. Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449. https://doi.org/10.1126/science.1155121 (2008).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Le Quere, C. et al. Global carbon budget 2016. Earth Syst. Sci. Data 8, 605–649. https://doi.org/10.5194/essd-8-605-2016 (2016).ADS 
    Article 

    Google Scholar 
    DavidMorales-Hidalgo, D., Oswalt, S. N. & Somanathan, E. Status and trends in global primary forest, protected areas, and areas designated for conservation of biodiversity from the Global Forest Resources Assessment 2015. Forest Ecol. Manag. 352, 68–77. https://doi.org/10.1016/j.foreco.2015.06.011 (2015).Article 

    Google Scholar 
    Kauppi, P. E., Sandstrom, V. & Lipponen, A. Forest resources of nations in relation to human well-being. PLoS One 13, e0196248. https://doi.org/10.1371/journal.pone.0196248 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Anderegg, W. R. L. et al. Climate-driven risks to the climate mitigation potential of forests. Science 368, 1327. https://doi.org/10.1126/science.aaz7005 (2020).CAS 
    Article 

    Google Scholar 
    Wilson, M. C. et al. Habitat fragmentation and biodiversity conservation: Key findings and future challenges. Landsc. Ecol. 31, 219–227. https://doi.org/10.1007/s10980-015-0312-3 (2016).Article 

    Google Scholar 
    Haddad, N. M. et al. Habitat fragmentation and its lasting impact on earth’s ecosystems. Sci. Adv. 1, e1500052. https://doi.org/10.1126/sciadv.1500052 (2015).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Holl, K. D. Restoring tropical forests from the bottom up. Science 355, 455–456. https://doi.org/10.1126/science.aam5432 (2017).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Audino, L. D., Murphy, S. J., Zambaldi, L., Louzada, J. & Comita, L. S. Drivers of community assembly in tropical forest restoration sites: Role of local environment, landscape, and space. Ecol. Appl. 27, 1731–1745. https://doi.org/10.1002/eap.1562 (2017).Article 
    PubMed 

    Google Scholar 
    Temperton, V. M., Hobbs, R. J., Nuttle, T. & Halle, S. in Assembly Rules and Restoration Ecology: Bridging the Gap Between Theory and Practice [Science and Practice of Ecological Restoration]. i–xv, 1–439 (2004).Young, T. P., Chase, J. M. & Huddleston, R. T. Community succession and assembly: Comparing, contrasting and combining paradigms in the context of ecological restoration. Ecol. Restor. 19, 5–18 (2001).Article 

    Google Scholar 
    Vellend, M. The Theory of Ecological Communities (Princeton University Press, 2016).
    Google Scholar 
    HilleRisLambers, J., Adler, P. B., Harpole, W. S., Levine, J. M. & Mayfield, M. M. Rethinking community assembly through the lens of coexistence theory. Annu. Rev. Ecol. Evol. Syst. 43(43), 227–248. https://doi.org/10.1146/annurev-ecolsys-110411-160411 (2012).Article 

    Google Scholar 
    Connell, J. H. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In Dynamics of Populations (eds Den Boer, P. J. & Gradwell, G. R.) (Centre for Agricultural Publishing and Documentation, 1971).
    Google Scholar 
    Janzen, D. H. Herbivores and the number of tree species in tropical forests. Am. Nat. 104, 501. https://doi.org/10.1086/282687 (1970).Article 

    Google Scholar 
    Schmid, J. S., Taubert, F., Wiegand, T., Sun, I. F. & Huth, A. Network science applied to forest megaplots: Tropical tree species coexist in small-world networks. Sci. Rep. https://doi.org/10.1038/s41598-020-70052-8 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, H. X. et al. Prevalence of inter-tree competition and its role in shaping the community structure of a natural Mongolian scots pine (Pinus sylvestris var. mongolica) forest. Forests https://doi.org/10.3390/f8030084 (2017).Article 

    Google Scholar 
    Hubbell, S. P. et al. Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283, 554–557. https://doi.org/10.1126/science.283.5401.554 (1999).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Janik, D. et al. Breaking through beech: A three-decade rise of sycamore in old-growth European forest. Forest Ecol. Manag. 366, 106–117. https://doi.org/10.1016/j.foreco.2016.02.003 (2016).Article 

    Google Scholar 
    Svatek, M., Rejzek, M., Kvasnica, J., Repka, R. & Matula, R. Frequent fires control tree spatial pattern, mortality and regeneration in argentine open woodlands. Forest Ecol. Manag. 408, 129–136. https://doi.org/10.1016/j.foreco.2017.10.048 (2018).Article 

    Google Scholar 
    Giammarchi, F. et al. Effects of the lack of forest management on spatiotemporal dynamics of a subalpine Pinus cembra forest. Scand. J. Forest Res. 32, 142–153. https://doi.org/10.1080/02827581.2016.1207802 (2017).Article 

    Google Scholar 
    Janik, D. et al. Patterns of Fraxinus angustifolia in an alluvial old-growth forest after declines in flooding events. Eur. J. Forest Res. 135, 215–228. https://doi.org/10.1007/s10342-015-0925-8 (2016).Article 

    Google Scholar 
    Bagchi, R. et al. Defaunation increases the spatial clustering of lowland western amazonian tree communities. J. Ecol. 106, 1470–1482. https://doi.org/10.1111/1365-2745.12929 (2018).Article 

    Google Scholar 
    Zhang, L. Y., Dong, L. B., Liu, Q. & Liu, Z. G. Spatial patterns and interspecific associations during natural regeneration in three types of secondary forest in the central part of the greater Khingan mountains, Heilongjiang province, China. Forests https://doi.org/10.3390/f11020152 (2020).Article 

    Google Scholar 
    Obiang, N. L. E. et al. Determinants of spatial patterns of canopy tree species in a tropical evergreen forest in Gabon. J. Veg. Sci. 30, 929–939. https://doi.org/10.1111/jvs.12778 (2019).Article 

    Google Scholar 
    Wiegand, T. et al. Spatially explicit metrics of species diversity, functional diversity, and phylogenetic diversity: Insights into plant community assembly processes. Annu. Rev. Ecol. Evol. Syst. 48(48), 329–351. https://doi.org/10.1146/annurev-ecolsys-110316-022936 (2017).Article 

    Google Scholar 
    Gabriel, E. Spatial point patterns: Methodology and applications with R. Math. Geosci. 49, 815–817. https://doi.org/10.1007/s11004-016-9670-x (2017).CAS 
    Article 
    MATH 

    Google Scholar 
    Baddeley, A., Rubak, R. & Turner, R. Spatial Point Patterns, Methodology and Applications with R (CRC Press, 2016).MATH 

    Google Scholar 
    Wiegand, T. & Moloney, K. A. Rings, circles, and null-models for point pattern analysis in ecology. Oikos 104, 209–229. https://doi.org/10.1111/j.0030-1299.2004.12497.x (2004).Article 

    Google Scholar 
    Plotkin, J. B., Chave, J. M. & Ashton, P. S. Cluster analysis of spatial patterns in Malaysian tree species. Am. Nat. 160, 629–644. https://doi.org/10.1086/342823 (2002).Article 
    PubMed 

    Google Scholar 
    Ripley, B. D. Modeling spatial patterns. J. R. Stat. Soc. B 39, 172–212 (1977).
    Google Scholar 
    He, F. L. & Gaston, K. J. Estimating species abundance from occurrence. Am. Nat. 156, 553–559. https://doi.org/10.1086/303403 (2000).Article 
    PubMed 

    Google Scholar 
    Diggle, P. Statistical Analysis of Spatial Point Patterns (Academic Press, 1983).MATH 

    Google Scholar 
    Pielou, E. C. The use of point-to-plant distances in the study of the pattern of plant-populations. J. Ecol. 47, 607–613. https://doi.org/10.2307/2257293 (1959).Article 

    Google Scholar 
    Losapio, G., Montesinos-Navarro, A. & Saiz, H. Perspectives for ecological networks in plant ecology. Plant Ecol. Divers. 12, 87–102. https://doi.org/10.1080/17550874.2019.1626509 (2019).Article 

    Google Scholar 
    Fuller, M. M., Wagner, A. & Enquist, B. J. Using network analysis to characterize forest structure. Nat. Resour. Model. 21, 225–247. https://doi.org/10.1111/j.1939-7445.2008.00004.x (2008).MathSciNet 
    Article 

    Google Scholar 
    Montoya, J. M., Pimm, S. L. & Sole, R. V. Ecological networks and their fragility. Nature 442, 259–264. https://doi.org/10.1038/nature04927 (2006).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Proulx, S. R., Promislow, D. E. L. & Phillips, P. C. Network thinking in ecology and evolution. Trends Ecol. Evol. 20, 345–353. https://doi.org/10.1016/j.tree.2005.04.004 (2005).Article 
    PubMed 

    Google Scholar 
    Nakagawa, Y., Yokozaw, M. & Hara, T. Complex network analysis reveals novel essential properties of competition among individuals in an even-aged plant population. Ecol. Complex 26, 95–116. https://doi.org/10.1016/j.ecocom.2016.03.005 (2016).Article 

    Google Scholar 
    Wiegand, T. & Moloney, K. A. Handbook of Spatial Point Pattern Analysis in Ecology (CRC Press, 2013).Book 

    Google Scholar 
    Barthelemy, M. Spatial networks. Phys. Rep. Rev. Sect. Phys. Lett. 499, 1–101. https://doi.org/10.1016/j.physrep.2010.11.002 (2011).MathSciNet 
    CAS 
    Article 

    Google Scholar 
    Keren, S. Modeling tree species count data in the understory and canopy layer of two mixed old-growth forests in the Dinaric region. Forests https://doi.org/10.3390/f11050531 (2020).Article 

    Google Scholar 
    Podlaski, R. Models of the fine-scale spatial distributions of trees in managed and unmanaged forest patches with Abies alba Mill. and Fagus sylvatica L. Forest Ecol. Manag. 439, 1–8 (2019).Article 

    Google Scholar 
    Levin, S. A. Theoretical ecology—Principles and applications, 3rd edition. Science 316, 1699–1700. https://doi.org/10.1126/science.1141870 (2007).CAS 
    Article 

    Google Scholar 
    Martinez-Lopez, V., Garcia, C., Zapata, V., Robledano, F. & De la Rua, P. Intercontinental long-distance seed dispersal across the Mediterranean basin explains population genetic structure of a bird-dispersed shrub. Mol. Ecol. 29, 1408–1420. https://doi.org/10.1111/mec.15413 (2020).Article 
    PubMed 

    Google Scholar 
    Dale, M. R. T. & Fortin, M. J. From graphs to spatial graphs. Annu. Rev. Ecol. Evol. Syst. 41, 21–38. https://doi.org/10.1146/annurev-ecolsys-102209-144718 (2010).Article 

    Google Scholar 
    Silva, C. A. et al. Treetop: A shiny-based application and R package for extracting forest information from LiDAR data for ecologists and conservationists. Methods Ecol. Evol. 13, 1164–1176. https://doi.org/10.1111/2041-210x.13830 (2022).Article 

    Google Scholar 
    Tatsumi, S., Yamaguchi, K. & Furuya, N. Forestscanner: A mobile application for measuring and mapping trees with LiDAR-equipped iPhone and iPad. Methods Ecol. Evol. https://doi.org/10.1111/2041-210x.13900 (2022).Article 

    Google Scholar 
    Ferraz, A., Saatchi, S. S., Longo, M. & Clark, D. B. Tropical tree size-frequency distributions from airborne LiDAR. Ecol. Appl. 30, e02154. https://doi.org/10.1002/eap.2154 (2020).Article 
    PubMed 

    Google Scholar 
    Bianchi, E., Bugmann, H., Hobi, M. L. & Bigler, C. Spatial patterns of living and dead small trees in subalpine Norway spruce forest reserves in Switzerland. Forest Ecol. Manag. 494, 119315. https://doi.org/10.1016/j.foreco.2021.119315 (2021).Article 

    Google Scholar 
    Tatsumi, S., Owari, T., Yin, M. F. & Ning, L. Z. Neighborhood analysis of underplanted Korean pine demography in larch plantations: Implications for uneven-aged management in northeast china. Forest Ecol. Manag. 322, 10–18. https://doi.org/10.1016/j.foreco.2014.03.022 (2014).Article 

    Google Scholar 
    Cornett, M. W., Reich, P. B. & Puettmann, K. J. Canopy feedbacks and microtopography regulate conifer seedling distribution in two Minnesota conifer-deciduous forests. Ecoscience 4, 353–364. https://doi.org/10.1080/11956860.1997.11682414 (1997).Article 

    Google Scholar 
    Wang, X. F., Zheng, G., Yun, Z. X. & Moskal, L. M. Characterizing tree spatial distribution patterns using discrete aerial LiDAR data. Remote Sens. Basel 12, 712. https://doi.org/10.3390/rs12040712 (2020).ADS 
    Article 

    Google Scholar 
    Matérn, B. Spatial variation: Stochastic models and their application to some problems in forest surveys and other sampling investigations. Meddelanden från Statens Skogsforskningsinstitut 49, 1–144 (1960).MathSciNet 

    Google Scholar 
    Matérn, B. Spatial Variation. Lecture Notes in Statistics Vol. 36 (Springer, 1986).Book 

    Google Scholar 
    Thomas, M. A generalisation of Poisson’s binomial limit for use in ecology. Biometrika 36, 18–25 (1949).MathSciNet 
    CAS 
    Article 

    Google Scholar 
    Lotwick, H. W. Simulation of some spatial hard core models, and the complete packing problem. J. Stat. Comput. Simul. 15, 295–314 (1982).MathSciNet 
    Article 

    Google Scholar 
    Strauss, D. J. A model for clustering. Biometrika 62, 467–475 (1975).MathSciNet 
    Article 

    Google Scholar 
    Cressie Noel, A. C. Statistics for Spatial Data (Wiley-Interscience, 1993).Book 

    Google Scholar 
    Besag, J. E. Contribution to the discussion of the paper by Ripley. J. R. Stat. Soc. 39, 193–195 (1977).MathSciNet 

    Google Scholar  More

  • in

    Dynamics of microbial community and enzyme activities during preparation of Agaricus bisporus compost substrate

    Royse DJ. A global perspective on the high five: Agaricus, Pleurotus, Lentinula, Auricularia and Flammulina. In: Singh M, editor. Proceedings of the 8th International Conference on Mushroom Biology and Mushroom Products. New Delhi; 2014. p. 1–6.Vos AM, Heijboer A, Boschker HTS, Bonnet B, Lugones LG, Wosten HAB. Microbial biomass in compost during colonization of Agaricus bisporus. AMB Express. 2017; 7:12.Jurak E, Punt AM, Arts W, Kabel MA, Gruppen H. Fate of carbohydrates and lignin during composting and mycelium growth of Agaricus bisporus on wheat straw based compost. PLoS ONE. 2015;10:e0138909.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Beyer DM. Basic procedures for Agaricus mushroom growing PennState Extension: the Pennsylvania State University. 2003. https://extension.psu.edu/basic-procedures-for-agaricus-mushroom-growing.Wang L, Mao J, Zhao H, Li M, Wei Q, Zhou Y, et al. Comparison of characterization and microbial communities in rice straw- and wheat straw-based compost for Agaricus bisporus production. J Ind Microbiol Biotechnol. 2016;43:1249–60.CAS 
    PubMed 
    Article 

    Google Scholar 
    Adams JDW, Frostick LE. Investigating microbial activities in compost using mushroom (Agaricus bisporus) cultivation as an experimental system. Bioresour Technol. 2008;99:1097–102.CAS 
    PubMed 
    Article 

    Google Scholar 
    Liu L, Wang S, Guo X, Zhao T, Zhang B. Succession and diversity of microorganisms and their association with physicochemical properties during green waste thermophilic composting. Waste Manage. 2018;73:101–12.CAS 
    Article 

    Google Scholar 
    Reyes-Torres M, Oviedo-Ocana ER, Dominguez I, Komilis D, Sanchez A. A systematic review on the composting of green waste: feedstock quality and optimization strategies. Waste Manage. 2018;77:486–99.CAS 
    Article 

    Google Scholar 
    Pardo‐Giménez A, González JEP, Zied DC. Casing materials and techniques in Agaricus bisporus cultivation. In: Zied DC, Pardo‐Giménez A, editors. Edible and medicinal mushrooms technology and applications. Chichester, UK: Wiley; 2017. p. 149–74.Baars JJP, Scholtmeijer K, Sonnenberg ASM, van Peer A. Critical factors involved in primordia building in Agaricus bisporus: a review. Molecules. 2020;25:2984.Vieira FR, Pecchia JA. Bacterial community patterns in the Agaricus bisporus cultivation system, from compost raw materials to mushroom caps. Microb Ecol. 2021;84:20–32.PubMed 
    Article 

    Google Scholar 
    Kristensen JB, Thygesen LG, Felby C, Jorgensen H, Elder T. Cell-wall structural changes in wheat straw pretreated for bioethanol production. Biotechnol Biofuels. 2008;1:1–9.Article 

    Google Scholar 
    Jurak E, Patyshakuliyeva A, de Vries RP, Gruppen H, Kabel MA. Compost grown Agaricus bisporus lacks the ability to degrade and consume highly substituted xylan fragments. PLoS ONE. 2015;10:e0134169.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ryckeboer J, Mergaert J, Vaes K, Klammer S, De Clercq D, Coosemans J, et al. A survey of bacteria and fungi occurring during composting and self-heating processes. Ann Microbiol. 2003;53:349–410.
    Google Scholar 
    Kutzner HJ. Microbiology of composting. In: Rehm H-J, Reed G, editors. Biotechnology. 11c. 2nd ed. Verlag: Wiley-VCH; 2000. p. 35–100.Carrasco J, Garcia-Delgado C, Lavega R, Tello ML, De Toro M, Barba-Vicente V, et al. Holistic assessment of the microbiome dynamics in the substrates used for commercial champignon (Agaricus bisporus) cultivation. Microb Biotechnol. 2020;13:1933–47.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vieira FR, Pecchia JA. Bacterial community patterns in the Agaricus bisporus cultivation system, from compost raw materials to mushroom caps. Microb Ecol. 2021;82. https://doi.org/10.1007/s00248-021-1833-5.Vieira FR, Pecchia JA. An exploration into the bacterial community under different pasteurization conditions during substrate preparation (composting–Phase II) for Agaricus bisporus cultivation. Microb Ecol. 2018;75:318–30.CAS 
    PubMed 
    Article 

    Google Scholar 
    Cao GT, Song TT, Shen YY, Jin QL, Feng WL, Fan LJ, et al. Diversity of bacterial and fungal communities in wheat straw compost for Agaricus bisporus cultivation. Hortscience. 2019;54:100–9.CAS 
    Article 

    Google Scholar 
    Wiegant WM. Growth characteristics of the thermophilic fungus Scytalidium thermophilum in relation to production of mushroom compost. Appl Environ Microbiol. 1992;58:1301–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fermor T, Randle P, Smith J. Compost as a substrate and its preparation. In: Flegg PB, Spencer DM, Wood D, editors. The biology and technology of the cultivated mushroom. Chichester, UK: John Wiley & Sons, Ltd; 1985. p. 81–109.Straatsma G, Samson RA, Olijnsma TW, Op den Camp HJM, Gerrits JPG, Griensven LJLDV. Ecology of thermophilic fungi in mushroom compost, with emphasis on Scytalidium thermophilum and growth stimulation of Agaricus bisporus mycelium. Appl Environ Microbiol. 1994;60:454–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ross RC, Harris PJ. An investigation into the selective nature of mushroom compost. Sci Hortic. 1983;19:55–64.Article 

    Google Scholar 
    Coello-Castillo MM, Sanchez JE, Royse DJ. Production of Agaricus bisporus on substrates pre-colonized by Scytalidium thermophilum and supplemented at casing with protein-rich supplements. Bioresour Technol. 2009;100:4488–92.CAS 
    PubMed 
    Article 

    Google Scholar 
    Szekely A, Sipos R, Berta B, Vajna B, Hajdu C, Marialigeti K. DGGE and T-RFLP analysis of bacterial succession during mushroom compost production and sequence-aided T-RFLP profile of mature compost. Microb Ecol. 2009;57:522–33.PubMed 
    Article 

    Google Scholar 
    Kertesz M, Safianowicz K, Bell TL. New insights into the microbial communities and biological activities that define mushroom compost. Sci Cultiv Edible Fungi. 2016;19:161–5.
    Google Scholar 
    McGee CF, Byrne H, Irvine A, Wilson J. Diversity and dynamics of the DNA and cDNA-derived bacterial compost communities throughout the Agaricus bisporus mushroom cropping process. Ann Microbiol. 2017;67:751–61.CAS 
    Article 

    Google Scholar 
    McGee CF, Byrne H, Irvine A, Wilson J. Diversity and dynamics of the DNA- and cDNA-derived compost fungal communities throughout the commercial cultivation process for Agaricus bisporus. Mycologia. 2017;109:475–84.CAS 
    PubMed 
    Article 

    Google Scholar 
    Yeates C, Gillings MR. Rapid purification of DNA from soil for molecular biodiversity analysis. Lett Appl Microbiol. 1998;27:49–53.CAS 
    Article 

    Google Scholar 
    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 
    PubMed Central 
    Article 

    Google Scholar 
    White TJ, Bruns T, Lee S, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. New York: Academic Press; 1990. p. 315–22.
    Google Scholar 
    Lever MA, Torti A, Eickenbusch P, Michaud AB, Santl-Temkiv T, Jorgensen BB. A modular method for the extraction of DNA and RNA, and the separation of DNA pools from diverse environmental sample types. Front Microbiol. 2015;6:476.Muyzer G, Waal ECD, Uitterlinden AG. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol. 1993;59:695–700.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA. 2011;108:4516–22.CAS 
    PubMed 
    Article 

    Google Scholar 
    R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation For Statistical Computing; 2019.Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina aplicon data. Nat Meth. 2016;13:581–3.CAS 
    Article 

    Google Scholar 
    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. Nucl Acids Res. 2012;41:D590–6.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2010;27:592–3.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wright ES. Using DECIPHER v2.0 to analyze big biological sequence data in R. R J. 2016;8:352–9.Article 

    Google Scholar 
    McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dixon P. VEGAN, a package of R functions for community ecology. J Veget Sci. 2003;14:927–30.Article 

    Google Scholar 
    Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer; 2016.Sharma HS, Kilpatrick M. Mushroom (Agaricus bisporus) compost quality factors for predicting potential yield of fruiting bodies. Can J Microbiol. 2000;46:515–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Seaby DA. Mushroom (Agaricus bisporus) yield modelling for the bag method of mushroom production using commercial yields and from micro plots. Sci Cultiv Edible Fungi. 1995;14:409–16.
    Google Scholar 
    O’Donoghue DC. Relationship between some compost factors and their effects on yield of Agaricus. Mushroom Sci. 1965;6:245–54.
    Google Scholar 
    Andersen B, Sorensen JL, Nielsen KF, van den Ende BG, de Hoog S. A polyphasic approach to the taxonomy of the Alternaria infectoria species-group. Fungal Genet Biol. 2009;46:642–56.CAS 
    PubMed 
    Article 

    Google Scholar 
    van den Brink J, Samson RA, Hagen F, Boekhout T, de Vries RP. Phylogeny of the industrial relevant, thermophilic genera Myceliophthora and Corynascus. Fungal Divers. 2012;52:197–207.Article 

    Google Scholar 
    Souza TP, Marques SC, Santos D, Dias ES. Analysis of thermophilic fungal populations during phase II of composting for the cultivation of Agaricus subrufescens. World J Microbiol Biotechnol. 2014;30:2419–25.PubMed 
    Article 

    Google Scholar 
    Vajna B, Szili D, Nagy A, Márialigeti K. An improved sequence-aided T-RFLP analysis of bacterial succession during oyster mushroom substrate preparation. Microb Ecol. 2012;64:702–13.CAS 
    PubMed 
    Article 

    Google Scholar 
    Du R, Yan J, Li S, Zhang L, Zhang S, Li J, et al. Cellulosic ethanol production by natural bacterial consortia is enhanced by Pseudoxanthomonas taiwanensis. Biotechnol Biofuels. 2015;8:10.Kato S, Haruta S, Cui ZJ, Ishii M, Igarashi Y. Stable coexistence of five bacterial strains as a cellulose-degrading community. Appl Environ Microbiol. 2005;71:7099–106.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Haruta S, Cui Z, Huang Z, Li M, Ishii M, Igarashi Y. Construction of a stable microbial community with high cellulose-degradation ability. Appl Microbiol Biotechnol. 2002;59:529–34.CAS 
    PubMed 
    Article 

    Google Scholar 
    Vajna B, Adrienn N, Sajben-Nagy E, Manczinger L, Szijártó N, Kádár Z, et al. Microbial community structure changes during oyster mushroom substrate preparation. Appl Microbiol Biotechnol. 2010;86:367–75.CAS 
    PubMed 
    Article 

    Google Scholar 
    Karadag D, Özkaya B, Ölmez E, Nissilä ME, Çakmakçı M, Yıldız Ş, et al. Profiling of bacterial community in a full-scale aerobic composting plant. Int Biodeter Biodeg. 2013;77:85–90.CAS 
    Article 

    Google Scholar 
    Rathinam NK, Gorky, Bibra M, Salem DR, Sani RK. Bioelectrochemical approach for enhancing lignocellulose degradation and biofilm formation in Geobacillus strain WSUCF1. Bioresour Technol. 2020;295:122271.Song TT, Shen YY, Jin QL, Feng WL, Fan LJ, Cao GT, et al. Bacterial community diversity, lignocellulose components, and histological changes in composting using agricultural straws for Agaricus bisporus production. PeerJ. 2021;9:e10452.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhang X, Zhong Y, Yang S, Zhang W, Xu M, Ma A, et al. Diversity and dynamics of the microbial community on decomposing wheat straw during mushroom compost production. Bioresour Technol. 2014;170:183–95.CAS 
    PubMed 
    Article 

    Google Scholar 
    Goodfellow M, Maldonado LA, Quintana ET. Reclassification of Nonomuraea flexuosa (Meyer 1989) Zhang et al. 1998 as Thermopolyspora flexuosa gen. nov., comb. nov., nom. rev. Int J Syst Evol Microbiol. 2005;55:1979–83.CAS 
    PubMed 
    Article 

    Google Scholar 
    Lin SB, Stutzenberger FJ. Purification and characterization of the major beta-1,4-endoglucanase from Thermomonospora curvata. J Appl Bacteriol. 1995;79:447–53.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kukolya J, Nagy I, Láday M, Tóth E, Oravecz O, Márialigeti K, et al. Thermobifida cellulolytica sp. nov., a novel lignocellulose-decomposing actinomycete. Int J Syst Evol Microbiol. 2002;52:1193–9.CAS 
    PubMed 

    Google Scholar 
    Weon H-Y, Lee S-Y, Kim B-Y, Noh H-J, Schumann P, Kim J-S, et al. Ureibacillus composti sp. nov. and Ureibacillus thermophilus sp. nov., isolated from livestock-manure composts. Int J Syst Evol Microbiol. 2007;57:2908–11.CAS 
    PubMed 
    Article 

    Google Scholar 
    Poli A, Laezza G, Gul-Guven R, Orlando P, Nicolaus B. Geobacillus galactosidasius sp. nov., a new thermophilic galactosidase-producing bacterium isolated from compost. Syst Appl Microbiol. 2011;34:419–23.CAS 
    PubMed 
    Article 

    Google Scholar 
    Gavande PV, Basak A, Sen S, Lepcha K, Murmu N, Rai V, et al. Functional characterization of thermotolerant microbial consortium for lignocellulolytic enzymes with central role of Firmicutes in rice straw depolymerization. Sci Rep. 2021;11:3032.Xu JQ, Lu YY, Shan GC, He XS, Huang JH, Li QL. Inoculation with compost-born thermophilic complex microbial consortium induced organic matters degradation while reduced nitrogen loss during co-composting of dairy manure and sugarcane leaves. Waste Biomass Valor. 2019;10:2467–77.CAS 
    Article 

    Google Scholar 
    Yoon JH, Kang SJ, Im WT, Lee ST, Oh TK. Chelatococcus daeguensis sp nov., isolated from wastewater of a textile dye works, and emended description of the genus Chelatococcus. Int J Syst Evol Microbiol. 2008;58:2224–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhou C, Liu Z, Huang Z-L, Dong M, Yu X-L, Ning P. A new strategy for co-composting dairy manure with rice straw: addition of different inocula at three stages of composting. Waste Manage. 2015;40:38–43.CAS 
    Article 

    Google Scholar 
    Gómez A. New technology in Agaricus bisporus cultivation. In: Zied DC, Pardo-Giménez A, editors. Edible and medicinal mushrooms. Chichester, UK: John Wiley & Sons; 2017. p. 211–20.von Minnigerode HF, editor. Method for controlling and regulating the composting process. Proceedings of the Eleventh International Scientific Congress on the Cultivation of Edible Fungi. Sydney, Australia: The International Society for Mushroom Science; 1981.Jurak E, Gruppen H, Kabel MA, Eggink G, Meyer AS, van der Maarel MJEC, et al. How mushrooms feed on compost: conversion of carbohydrates and lignin in industrial wheat straw based compost enabling the growth of Agaricus bisporus. Wageningen University—Graduate School VLAG; 2015.Miller FC, Macauley BJ, Harper ER. Investigation of various gases, pH and redox potential in mushroom composting Phase-I stacks. Aust J Exper Agric. 1991;31:415–25.Article 

    Google Scholar 
    Miller FC, Harper ER, Macauley BJ, Gulliver A. Composting based on moderately thermophilic and aerobic conditions for the production of commercial growing compost. Aust J Exper Agric. 1990;30:287–96.Article 

    Google Scholar 
    Carrasco J, Preston GM. Growing edible mushrooms: a conversation between bacteria and fungi. Environ Microbiol. 2020;22:858–72.PubMed 
    Article 

    Google Scholar  More

  • in

    In vitro larval rearing method of eusocial bumblebee Bombus terrestris for toxicity test

    Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. P. R. Soc. B 274, 303–313 (2007).
    Google Scholar 
    Potts, S. G. et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010).PubMed 

    Google Scholar 
    Gallai, N., Salles, J. M., Settele, J. & Vaissiere, B. E. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 (2009).
    Google Scholar 
    Ollerton, J. Pollinator diversity: Distribution, ecological function, and conservation. Annu. Rev. Ecol. Evol. Syst. 48, 353–376 (2017).
    Google Scholar 
    Biesmeijer, J. C. et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Kosior, A. et al. The decline of the bumble bees and cuckoo bees (Hymenoptera : Apidae : Bombini) of Western and Central Europe. Oryx 41, 79–88 (2007).
    Google Scholar 
    Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. U. S. A. 108, 662–667 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cameron, S. A., Lim, H. C., Lozier, J. D., Duennes, M. A. & Thorp, R. Test of the invasive pathogen hypothesis of bumble bee decline in North America. Proc. Natl. Acad. Sci. U. S. A. 113, 4386–4391 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gill, R. J., Ramos-Rodriguez, O. & Raine, N. E. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    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 

    Google Scholar 
    Stanley, D. A. et al. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528, 548–550 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Baron, G. L., Raine, N. E. & Brown, M. J. F. General and species-specific impacts of a neonicotinoid insecticide on the ovary development and feeding of wild bumblebee queens. P. R. Soc. B 284, 20170123 (2017).
    Google Scholar 
    Siviter, H., Folly, A. J., Brown, M. J. F. & Leadbeater, E. Individual and combined impacts of sulfoxaflor and Nosema bombi on bumblebee (Bombus terrestris) larval growth. Proc. Biol. Sci. 287, 20200935 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blacquière, T., Smagghe, G., van Gestel, C. A. M. & Mommaerts, V. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21, 973–992 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    Richardson, L. L. et al. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proc. Biol. Sci. 282, 20142471 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    McAulay, M. K. & Forrest, J. R. K. How do sunflower pollen mixtures affect survival of queenless microcolonies of bumblebees (Bombus impatiens)?. Arthropod Plant Interact. 13, 517–529 (2019).
    Google Scholar 
    European Food Safety Authority. Guidance on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J. 11, 3295 (2013).Besard, L. et al. Compatibility of traditional and novel acaricides with bumblebees (Bombus terrestris): a first laboratory assessment of toxicity and sublethal effects. Pest Manag. Sci. 66, 786–793 (2010).CAS 
    PubMed 

    Google Scholar 
    Elston, C., Thompson, H. M. & Walters, K. F. A. Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris) micro-colonies. Apidologie 44, 563–574 (2013).CAS 

    Google Scholar 
    Barbosa, W. F., De Meyer, L., Guedes, R. N. C. & Smagghe, G. Lethal and sublethal effects of azadirachtin on the bumblebee Bombus terrestris (Hymenoptera: Apidae). Ecotoxicology 24, 130–142 (2015).CAS 
    PubMed 

    Google Scholar 
    Dance, C., Botías, C. & Goulson, D. The combined effects of a monotonous diet and exposure to thiamethoxam on the performance of bumblebee micro-colonies. Ecotoxicol. Environ. Saf. 139, 194–201 (2017).CAS 
    PubMed 

    Google Scholar 
    Schmehl, D. R., Tome, H. V. V., Mortensen, A. N., Martins, G. F. & Ellis, J. D. Protocol for the in vitro rearing of honey bee (Apis mellifera L.) workers. J. Apic. Res. 55, 113–129 (2016).Pereboom, J. J. M., Velthuis, H. H. W. & Duchateau, M. J. The organisation of larval feeding in bumblebees (Hymenoptera, Apidae) and its significance to caste differentiation. Insectes Soc. 50, 127–133 (2003).
    Google Scholar 
    Dorigo, A. S., Rosa-Fontana, A. D., Soares-Lima, H. M., Galaschi-Teixeira, J. S., Nocelli, R. C. F. & Malaspina, O. In Vitro larval rearing protocol for the stingless bee species Melipona scutellaris for toxicological studies. PLoS One 14. https://doi.org/10.1371/journal.pone.0213109 (2019).Botina, L. L. et al. Toxicological assessments of agrochemical effects on stingless bees (Apidae, Meliponini). MethodsX 7, 100906 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Black, B. C., Hollingworth, R. M., Ahammadsahib, K. I., Kukel, C. D. & Donovan, S. Insecticidal Action and Mitochondrial Uncoupling Activity of AC-303,630 and Related Halogenated Pyrroles. Pestic. Biochem. Physiol. 50, 115–128 (1994).CAS 

    Google Scholar 
    Wakita, T. et al. The discovery of dinotefuran: a novel neonicotinoid. Pest Manag. Sci. 59, 1016–1022 (2003).CAS 
    PubMed 

    Google Scholar 
    Shafiei, M., Moczek, A. P. & Nijhout, H. F. Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Physiol. Entomol. 26, 173–180 (2001).
    Google Scholar 
    Stieper, B. C., Kupershtok, M., Driscoll, M. V. & Shingleton, A. W. Imaginal discs regulate developmental timing in Drosophila melanogaster. Dev. Biol. 321, 18–26 (2008).CAS 
    PubMed 

    Google Scholar 
    Nijhout, H. F. & Williams, C. Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. J. Exp. Biol. 61, 481–491 (1974).Cnaani, J., Robinson, G. E. & Hefetz, A. The critical period for caste determination in Bombus terrestris and its juvenile hormone correlates. J. Comp. Physiol. A 186, 1089–1094 (2000).CAS 
    PubMed 

    Google Scholar 
    Goulson, D. et al. Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?. Anim. Behav. 64, 123–130 (2002).
    Google Scholar 
    Syromyatnikov, M., Nesterova, E., Smirnova, T. & Popov, V. Methylene blue can act as an antidote to pesticide poisoning of bumble bee mitochondria. Sci. Rep. 11, 14710 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Raghavendra, K. et al. Chlorfenapyr: a new insecticide with novel mode of action can control pyrethroid resistant malaria vectors. Malar. J. 10, 16 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Cao, Y. et al. HPLC/UV analysis of chlorfenapyr residues in cabbage and soil to study the dynamics of different formulations. Sci. Total Environ. 350, 38–46 (2005).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Costa, E. M. et al. Toxicity of insecticides used in the Brazilian melon crop to the honey bee Apis mellifera under laboratory conditions. Apidologie 45, 34–44 (2014).CAS 

    Google Scholar 
    Cresswell, J. E., Robert, F.-X.L., Florance, H. & Smirnoff, N. Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Pest Manag. Sci. 70, 332–337 (2014).CAS 
    PubMed 

    Google Scholar 
    Czerwinski, M. A. & Sadd, B. M. Detrimental interactions of neonicotinoid pesticide exposure and bumblebee immunity. J Exp Zool A Ecol Integr Physiol 327, 273–283 (2017).CAS 
    PubMed 

    Google Scholar 
    Mobley, M. W. & Gegear, R. J. One size does not fit all: Caste and sex differences in the response of bumblebees (Bombus impatiens) to chronic oral neonicotinoid exposure. PLoS ONE 13, e0200041 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Simmons, W. R. & Angelini, D. R. Chronic exposure to a neonicotinoid increases expression of antimicrobial peptide genes in the bumblebee Bombus impatiens. Sci. Rep. 7, 44773 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Doublet, V., Labarussias, M., de Miranda, J. R., Moritz, R. F. A. & Paxton, R. J. Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ. Microbiol. 17, 969–983 (2015).CAS 
    PubMed 

    Google Scholar 
    Eiri, D. M., Suwannapong, G., Endler, M. & Nieh, J. C. Nosema ceranae can infect honey bee larvae and reduces subsequent adult longevity. PLoS One 10, (2015).Dai, P., Jack, C. J., Mortensen, A. N. & Ellis, J. D. Acute toxicity of five pesticides to Apis mellifera larvae reared in vitro. Pest Manag. Sci. 73, 2282–2286 (2017).CAS 
    PubMed 

    Google Scholar 
    du Rand, E. E. et al. Proteomic and metabolomic analysis reveals rapid and extensive nicotine detoxification ability in honey bee larvae. Insect Biochem. Mol. Biol. 82, 41–51 (2017).PubMed 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (2021). R Core Team (2021). URL https://www.R-project.org/. More

  • in

    Stable ocean redox during the main phase of the Great Ordovician Biodiversification Event

    Stigall, A. L., Edwards, C. T., Freeman, R. L. & Rasmussen, C. M. Ø. Coordinated biotic and abiotic change during the Great Ordovician Biodiversification Event: Darriwilian assembly of early Paleozoic building blocks. Palaeogeogr. Palaeoclimatol. Palaeoecol. 530, 249–270 (2019).
    Google Scholar 
    Alroy, J. Colloquium paper: dynamics of origination and extinction in the marine fossil record. Proc. Natl. Acad. Sci. USA 105, 11536–11542 (2008). Suppl 1.CAS 

    Google Scholar 
    Servais, T., Cascales-Miñana, B. & Harper, D. A. T. The Great Ordovician Biodiversification Event (GOBE) is not a single event. Paleontological Res. 25, 315–328 (2021).Miller, A. I. & Foote, M. Calibrating the Ordovician Radiation of marine life: implications for Phanerozoic diversity trends. Paleobiology 22, 304–309 (1996).CAS 

    Google Scholar 
    Sepkoski, J. J. A compendium of marine fossil genera. vol. 2002 (Paleontological Research Institution, 2002).Zhan, R. & Harper, D. A. T. Biotic diachroneity during the Ordovician Radiation: evidence from South China. Lethaia 39, 211–226 (2006).
    Google Scholar 
    Fan, J. et al. A high-resolution summary of Cambrian to Early Triassic marine invertebrate biodiversity. Science 367, 272–277 (2020).CAS 

    Google Scholar 
    Deng, Y. et al. Timing and patterns of the Great Ordovician Biodiversification Event and Late Ordovician mass extinction: Perspectives from South China. Earth-Sci. Rev. 220, 103743 (2021).
    Google Scholar 
    Kröger, B., Franeck, F. & Rasmussen, C. M. Ø. The evolutionary dynamics of the early Palaeozoic marine biodiversity accumulation. Proc. R. Soc. B: Biol. Sci. 286, 3–8 (2019).
    Google Scholar 
    Rasmussen, C. M. Ø., Kröger, B., Nielsen, M. L. & Colmenar, J. Cascading trend of Early Paleozoic marine radiations paused by Late Ordovician extinctions. Proc. Natl. Acad. Sci. USA 116, 7207–7213 (2019).CAS 

    Google Scholar 
    Sepkoski, J. J. A factor analytic description of the phanerozoic marine fossil record. Paleobiology 7, 36–53 (1981).
    Google Scholar 
    Sepkoski, J. J. & Sheehan, P. M. Diversification, Faunal Change, and Community Replacement during the Ordovician Radiations. in Biotic interactions in recent and fossil benthic communities (eds. Tevesz, M. J. S. & McCall, P. L.) 673–717 (Plenum Press, 1983).Harper, D. A. T. The Ordovician biodiversification: Setting an agenda for marine life. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 148–166 (2006).
    Google Scholar 
    Stigall, A. L., Bauer, J. E., Lam, A. R. & Wright, D. F. Biotic immigration events, speciation, and the accumulation of biodiversity in the fossil record. Global Planet. Change 148, 242–257 (2017).
    Google Scholar 
    Copper, P. Coral Reefs Reports Ancient reef ecosystem expansion and collapse. Coral Reefs 13, 3–11 (1994).
    Google Scholar 
    Trotter, J. A., Williams, I. S., Barnes, C. R., Lécuyer, C. & Nicoll, R. S. Did Cooling Oceans Trigger Ordovician Biodiversification? Evidence from Conodont Thermometry. Science 321, 550–554 (2008).CAS 

    Google Scholar 
    Lindström, M. The Ordovician climate based on the study of carbonate rocks. in Aspects of the Ordovician System, Paleontological Contribution of the University of Oslo (ed. Bruton, D. L.) vol. 295 81–88 (Universitetsforlaget, 1984).Rasmussen, C. M. Ø., Nielsen, A. T. & Harper, D. A. T. Ecostratigraphical interpretation of lower Middle Ordovician East Baltic sections based on brachiopods. Geological Mag. 146, 717–731 (2009).
    Google Scholar 
    Dabard, M. P. et al. Sea-level curve for the Middle to early Late Ordovician in the Armorican Massif (western France): Icehouse third-order glacio-eustatic cycles. Palaeogeogr. Palaeoclimatol. Palaeoecol. 436, 96–111 (2015).
    Google Scholar 
    Rasmussen, C. M. Ø. et al. Onset of main Phanerozoic marine radiation sparked by emerging Mid Ordovician icehouse. Sci. Rep. 6, 1–9 (2016).
    Google Scholar 
    Deutsch, C., Ferrel, A., Seibel, B., Pörtner, H.-O. & Huey, R. B. Climate change tightens a metabolic constraint on marine habitats. Science 348, 1132–1135 (2015).CAS 

    Google Scholar 
    Penn, J. L., Deutsch, C., Payne, J. L. & Sperling, E. A. Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction. Science 362, eaat1327 (2018).
    Google Scholar 
    Saltzman, M. R., Edwards, C. T., Adrain, J. M. & Westrop, S. R. Persistent oceanic anoxia and elevated extinction rates separate the Cambrian and Ordovician radiations. Geology 43, 807–811 (2015).CAS 

    Google Scholar 
    Edwards, C. T., Saltzman, M. R., Royer, D. L. & Fike, D. A. Oxygenation as a driver of the Great Ordovician Biodiversification Event. Nature Geoscience 10, 925–929 (2017).CAS 

    Google Scholar 
    Sperling, E. A., Knoll, A. H. & Girguis, P. R. The ecological physiology of earth’s second oxygen revolution. Ann. Rev. Ecol. Evolut. Syst. 46, 215–235 (2015).
    Google Scholar 
    Dahl, T. W. et al. Reorganisation of Earth’s biogeochemical cycles briefly oxygenated the oceans 520 Myr ago. Geochem. Perspect. Lett. 210–220 (2017).Dahl, T. W. et al. Atmosphere-ocean oxygen and productivity dynamics during early animal radiations. Proc. Natl. Acad. Sci. 116, 19352–19361 (2019).CAS 

    Google Scholar 
    Nursall, J. R. Oxygen as a prerequisite to the origin of the metazoa. Nature 183, 1170–1172 (1959).Knoll, A. H. Biological and Biogeochemical Preludes to the Ediacaran Radiation. In Origin and Early Evolution of the Metazoa (eds. Lipps, J. H. & Signor, P. W.) 53–84 (Springer US, 1992).Brennecka, G. A., Herrmann, A. D., Algeo, T. J. & Anbar, A. D. Rapid expansion of oceanic anoxia immediately before the end-Permian mass extinction. Proc. Natl. Acad. Sci. 108, 17631–17634 (2011).CAS 

    Google Scholar 
    Lau, K. V. et al. Marine anoxia and delayed Earth system recovery after the end-Permian extinction. Proc. Natl. Acad. Sci. USA 113, 2360–2365 (2016).CAS 

    Google Scholar 
    Zhang, F. et al. Congruent Permian-Triassic δ238U records at Panthalassic and Tethyan sites: Confirmation of global-oceanic anoxia and validation of the U-isotope paleoredox proxy. Geology 46, 327–330 (2018).CAS 

    Google Scholar 
    Andersen, M. B., Stirling, C. H. & Weyer, S. Uranium isotope fractionation. Rev. Mineral. Geochem. 82, 799–850 (2017).CAS 

    Google Scholar 
    Chen, X. et al. Diagenetic effects on uranium isotope fractionation in carbonate sediments from the Bahamas. Geochimica et Cosmochimica Acta 237, 294–311 (2018).CAS 

    Google Scholar 
    Zhang, F. et al. Uranium isotopes in marine carbonates as a global ocean paleoredox proxy: A critical review. Geochimica et Cosmochimica Acta 287, 27–49 (2020).CAS 

    Google Scholar 
    Stylo, M. et al. Uranium isotopes fingerprint biotic reduction. Proc. Natl. Acad. Sci. 112, 5619–5624 (2015).CAS 

    Google Scholar 
    Basu, A. et al. Microbial U isotope fractionation depends on the U(VI) reduction rate. Environ. Sci. Technol. 54, 2295–2303 (2020).CAS 

    Google Scholar 
    Dunk, R. M., Mills, R. A. & Jenkins, W. J. A reevaluation of the oceanic uranium budget for the Holocene. Chem. Geol. 190, 45–67 (2002).CAS 

    Google Scholar 
    Dahl, T. W. et al. Uranium isotopes distinguish two geochemically distinct stages during the later Cambrian SPICE event. Earth Planet. Sci. Lett. 401, 313–326 (2014).CAS 

    Google Scholar 
    Tissot, F. L. H. & Dauphas, N. Uranium isotopic compositions of the crust and ocean: Age corrections, U budget and global extent of modern anoxia. Geochimica et Cosmochimica Acta 167, 113–143 (2015).CAS 

    Google Scholar 
    Romaniello, S. J., Herrmann, A. D. & Anbar, A. D. Uranium concentrations and 238U/235U isotope ratios in modern carbonates from the Bahamas: Assessing a novel paleoredox proxy. Chem. Geology 362, 305–316 (2013).CAS 

    Google Scholar 
    Chen, X., Romaniello, S. J., Herrmann, A. D., Samankassou, E. & Anbar, A. D. Biological effects on uranium isotope fractionation (238U/235U) in primary biogenic carbonates. Geochimica et Cosmochimica Acta 240, 1–10 (2018).CAS 

    Google Scholar 
    Tissot, F. L. H. et al. Controls of eustasy and diagenesis on the 238U/235U of carbonates and evolution of the seawater (234U/238U) during the last 1.4 Myr. Geochimica et Cosmochimica Acta 242, 233–265 (2018).CAS 

    Google Scholar 
    Lindskog, A. & Eriksson, M. E. Megascopic processes reflected in the microscopic realm: sedimentary and biotic dynamics of the Middle Ordovician “orthoceratite limestone” at Kinnekulle, Sweden. Gff 139, 163–183 (2017).
    Google Scholar 
    Jaanusson, V. Aspects of carbonate sedimentation in the Ordovician of Baltoscandia. Lethaia 6, 11–34 (1973).
    Google Scholar 
    Bergström, S. M., Chen, X., Gutiérrez-marco, J. C. & Dronov, A. The new chronostratigraphic classification of the Ordovician System and its relations to major regional series and stages and to δ13C chemostratigraphy. Lethaia 42, 97–107 (2008).
    Google Scholar 
    Lindskog, A., Lindskog, A. M., Johansson, J. V., Ahlberg, P. & Eriksson, M. E. The Cambrian–Ordovician succession at Lanna, Sweden: stratigraphy and depositional environments. Estonian J. Earth Sci 67, 133 (2018).
    Google Scholar 
    Bábek, O. et al. Redox geochemistry of the red ‘orthoceratite limestone’ of Baltoscandia: Possible linkage to mid-Ordovician palaeoceanographic changes. Sedimentary Geology 420, 105934 (2021).
    Google Scholar 
    Azmy, K. et al. Carbon-isotope stratigraphy of the Lower Ordovician succession in Northeast Greenland: Implications for correlations with St. George Group in western Newfoundland (Canada) and beyond. Sedimentary Geology 225, 67–81 (2010).CAS 

    Google Scholar 
    Bartlett, R. et al. Abrupt global-ocean anoxia during the Late Ordovician–early Silurian detected using uranium isotopes of marine carbonates. Proc Natl Acad Sci USA 115, 5896–5901 (2018).CAS 

    Google Scholar 
    Dahl, T. W., Hammarlund, E. U., Rasmussen, C. M. Ø., Bond, D. P. G. & Canfield, D. E. Sulfidic anoxia in the oceans during the Late Ordovician mass extinctions – insights from molybdenum and uranium isotopic global redox proxies. Earth-Sci. Rev. 220, 103748 (2021).CAS 

    Google Scholar 
    Del Rey, Á., Havsteen, J., Bizzarro, M., Connelly, J. & Dahl, T. W. Untangling the diagenetic history of Uranium isotopes in marine carbonates: a case study tracing d238U of late Silurian oceans using calcitic brachiopod shells. Geochimica et Cosmochimica Acta 2020, 93–110.Rasmussen, J. A., Thibault, N. & Mac Ørum Rasmussen, C. Middle Ordovician astrochronology decouples asteroid breakup from glacially-induced biotic radiations.Nat Commun12, 6430 (2021).CAS 

    Google Scholar 
    Ainsaar, L. et al. Middle and Upper Ordovician carbon isotope chemostratigraphy in Baltoscandia: A correlation standard and clues to environmental history. Palaeogeogr. Palaeoclimatol. Palaeoecol. 294, 189–201 (2010).
    Google Scholar 
    Wu, R., Calner, M. & Lehnert, O. Integrated conodont biostratigraphy and carbon isotope chemostratigraphy in the Lower-Middle Ordovician of southern Sweden reveals a complete record of the MDICE. Geological Mag. 154, 334–353 (2017).CAS 

    Google Scholar 
    Lindskog, A., Eriksson, M. E., Bergström, S. M. & Young, S. A. Lower–Middle Ordovician carbon and oxygen isotope chemostratigraphy at Hällekis, Sweden: implications for regional to global correlation and palaeoenvironmental development. Lethaia 52, 204–219 (2019).
    Google Scholar 
    Rasmussen, C. M. Ø., Hansen, J. & Harper, D. A. T. Baltica: A mid Ordovivian diversity hotspot. Historical Biology 19, 255–261 (2007).
    Google Scholar 
    Zhang, J. Lithofacies and stratigraphy of the Ordovician Guniutan Formation in its type area, China. Geol. J. 31, 201–215 (1996).
    Google Scholar 
    Eriksson, M. E. et al. Biotic dynamics and carbonate microfacies of the conspicuous Darriwilian (Middle Ordovician) ‘Täljsten’ interval, south-central Sweden. Palaeogeogr. Palaeoclimatol. Palaeoecol. 367–368, 89–103 (2012).
    Google Scholar 
    Lindström, M., Jun-Yuan, C. & Jun-Ming, Z. Section at Daping reveals Sino-Baltoscandian parallelism of facies in the Ordovician. Geologiska Föreningen i Stockholm Förhandlingar 113, 189–205 (1991).
    Google Scholar 
    Edward, O. et al. A Baltic perspective on the early to early late ordovician δ13 C and δ18 O Records and its paleoenvironmental significance. Paleoceanog and Paleoclimatol 37, e2021PA004309 (2022).Pörtner, H. Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88, 137–146 (2001).
    Google Scholar 
    Gueguen, B. et al. The chromium isotope composition of reducing and oxic marine sediments. Geochimica et Cosmochimica Acta 184, 1–19 (2016).CAS 

    Google Scholar 
    Weyer, S. et al. Natural fractionation of 238U/235U. Geochimica et Cosmochimica Acta 72, 345–359 (2008).CAS 

    Google Scholar 
    Condon, D. J., McLean, N., Noble, S. R. & Bowring, S. A. Isotopic composition (238U/235U) of some commonly used uranium reference materials. Geochimica et Cosmochimica Acta 74, 7127–7143 (2010).CAS 

    Google Scholar 
    Wang, X., Planavsky, N. J., Reinhard, C. T., Hein, J. R. & Johnson, T. M. A cenozoic seawater redox record derived from 238U/235U in ferromanganese crusts. Am. J. Sci. 315, 64–83 (2016).
    Google Scholar 
    Trotter, J. A., Williams, I. S., Barnes, C. R., Männik, P. & Simpson, A. New conodont δ18O records of Silurian climate change: Implications for environmental and biological events. Palaeogeogr. Palaeoclimatol. Palaeoecol. 443, 34–48 (2016).
    Google Scholar 
    Scotese, C. R. Atlas of Silurian and Middle-Late Ordovician Paleogeographic Maps (Mollweide Projection), Maps 73-80, Volumes 5, The Early Paleozoic, PALEOMAP Atlas for ArcGIS, PALEOMAP Project, Evanston, IL. (2014). More

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    Author Correction: Species traits and reduced habitat suitability limit efficacy of climate change refugia in streams

    Correction to: Nature Ecology & Evolution https://doi.org/10.1038/s41559-019-0970-7, published online 2 September 2019.The Journal would like to note that the authors first made contact in September 2019 to raise the concerns that follow, and the Journal apologizes both for the delay in relaying these corrections publicly and for the changed instances that prevent making corrections to the original article itself. What follows is the Author correction.In the version of this article initially published, we made several errors in our R analysis code, and in the text and figures. First, the number of species with negative net dispersal velocity (net DV) were incorrectly calculated, resulting in slight changes in Fig. 2 and Supplementary Fig. 6, and in the text. The amended figures are provided below (Figs. 1–7). Changes to the text under the ‘DVs’ subsection of Results are: “When considering the mainstem pathway, we estimate that the mobile subpopulations of 134 (old version: 124) and 185 (old version: 174) (RCP 4.5 and 8.5, respectively) species will experience dispersal deficits in at least 50% of their southern Appalachian range, whereas these estimates increase to 229 (old version: 226) and 231 (old version: 232) species for the stationary subpopulation. Slow-climate-velocity tributaries reduce the number of species experiencing dispersal deficits by 99.3% (old version: 99.2%) and 90.3% (old version: 16.9%) (RCP 4.5 and 8.5, respectively) for the mobile component and 17.9% (old version: 90.8%) and 12.1% (old version: 12.9%) for the stationary component (Fig. 2a,b).” The two large discrepancies in dispersal deficit values (90.3% vs. 16.9%; 17.9% vs. 90.8%) were solely consequences of original text errors (16.9% and 90.8% values were erroneously switched), and not differences in calculations; therefore, the results did not change.Fig. 1Figure 2, original and corrected.Full size imageFig. 2Figure 3c,d, original and corrected.Full size imageFig. 3Figure 4, original and corrected.Full size imageFig. 4Figure 5, original and corrected.Full size imageFig. 5Supplementary Figure 6, original.Full size imageFig. 5Supplementary Figure 6, corrected.Full size imageFig. 6Supplementary Figure 8, original.Full size imageFig. 6Supplementary Figure 8, corrected.Full size imageFig. 7Supplementary Figure 9, original.Full size imageFig. 7Supplementary Figure 9, corrected.Full size imageSecond, we made errors when plotting Fig. 3c,d. Boxplots of mean change in habitat suitability were plotted instead of median change as specified in the caption; further, whiskers did not include the entire range of values. The amended figure is provided below. We would like to correct associated errors in text; specific changes are: “Our ENMs estimate a median 15.1% (old version: mean 14.1%) reduction (range −42.5% to +16.6% [old version: −51.6% to +2.4%] across 233 species) in habitat suitability associated with the tributary pathway compared with only a 3.8% (old version: 1.6%) reduction (−11.0% to +12.3% [old version: −7.9% to +1.8%]) for the mainstem pathway due to differing non-temperature habitat conditions (Fig. 3a,b).”Third, we made errors when plotting Fig. 4 and Supplementary Fig. 8. Specifically, net DV values were incorrectly rescaled; one extinct species was erroneously included in the plot; and the number of species in each quadrant was counted incorrectly. The amended figures are shown below. We would like to add a sentence (“The y-axes are inverse hyperbolic sine (asinh)-transformed”) to the caption of Fig. 4 to describe the y-axis scaling in the amended figures. There were two other text errors in the caption. The phrase “Mean net DV” should have been “Median net DV,” whereas the phrase “mean habitat suitability” should have read “median change in habitat suitability.” Therefore, the corrected Fig. 4 caption should read: “Species-level mismatch between net DV and upstream habitat suitability. a–d, Median net DV of mobile (a,b) and stationary subpopulations under the RCP 8.5 scenario plotted as a function of median change in habitat suitability for mainstem (a,c) and tributary (b,d) dispersal pathways. Each point represents a species and is computed as the median response across all projected occupied reaches. Red and blue numbers correspond to the number of species in each of the four quadrants. The y-axes are inverse hyperbolic sine (asinh)-transformed. e–h, Four species highlighting the diversity in dispersal-based and habitat suitability-based vulnerability: streamline chub (e); brook trout (f); flathead catfish (g); blacknose dace (h). Credit: David Neely (e–h)”. These corrections did not change our inferences.Fourth, there were errors in rescaling and plotting net DV values and in the calculation of quadrant percentages in Fig. 5 and Supplementary Fig. 9. The amended figures are shown below. We would like to add two sentences at the end of Fig. 5 caption to provide greater detail on plotting methods: “The y-axes of the scatterplots are inverse hyperbolic sine (asinh)-transformed. For clarity, the scatterplots show net DV values ≥ −13,000 and ≤ 130, and change in habitat suitability values ≤ 100, representing >99.5% of all observations.” There was one other text error in the caption: the phrase “mean habitat suitability” should have read “mean change in habitat suitability.” Therefore, the corrected Fig. 4 caption should read: “Community-level mismatch between net DV and upstream habitat suitability. a–d, Mean net DV of mobile (a,b) and stationary (c,d) subpopulations under the RCP 8.5 scenario plotted as a function of mean change in habitat suitability for mainstem (a,c) and tributary (b,d) dispersal pathways. Each point (scatterplot) and reach (map) is computed as the mean response for all species projected to occur within the reach. Quadrant numbers represent percentage of reaches in the quadrant. Colours associated with the upper-right quadrant correspond to ‘safe’ reaches where community members can keep pace with ISVs and habitat suitability increases. Colours associated with the lower-left quadrant correspond to ‘vulnerable’ reaches where community members cannot keep pace with ISVs and habitat suitability declines. The y-axes of the scatterplots are inverse hyperbolic sine (asinh)-transformed. For clarity, the scatterplots show net DV values ≥ −13,000 and ≤ 130, and change in habitat suitability values ≤ 100, representing >99.5% of all observations.” These corrections did not change our inferences.Fifth, there was an error in the last sentence of the “Calculating net DVs” subsection in Methods: “Last, we calculated the mean net DV for each species (species-specific DV) by averaging net DVs at all occupied reaches, as well as the community-wide net DV at each stream reach (reach-specific DV) by averaging the net DVs of all species at each reach.” This sentence should have read “Last, we calculated the median net DV for each species (species-specific DV) across all occupied reaches, as well as the mean community-wide net DV at each stream reach (reach-specific DV) by averaging the net DVs of all species at each reach.”Corrections of calculation errors yielded results that were similar to those in the original analysis whereas corrections of plotting and text errors did not affect our original inferences. Therefore, these errors did not change the overall results and conclusions of the article. We sincerely apologize for any misunderstanding and inconvenience caused by these errors. More

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    Drosophila suzukii preferentially lays eggs on spherical surfaces with a smaller radius

    Little, C. M., Chapman, T. W. & Hillier, N. K. Plasticity is key to success of Drosophila suzukii (Diptera: Drosophilidae) invasion. J. Insect Sci. 20, 5. https://doi.org/10.1093/jisesa/ieaa034 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tait, G. et al. Drosophila suzukii (Diptera: Drosophilidae): A decade of research towards a sustainable integrated pest management program. J. Economic Entomol. 114, 1950–1974. https://doi.org/10.1093/jee/toab158 (2021).Article 

    Google Scholar 
    Walsh, D. B. et al. Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. J. Integ. Pest Manag. 2, G1–G7. https://doi.org/10.1603/IPM10010 (2011).Article 

    Google Scholar 
    Hamby, K. A. et al. Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J. Pest Sci. 89, 605–619. https://doi.org/10.1007/s10340-016-0756-5 (2016).Article 

    Google Scholar 
    Stewart, T. J., Wang, X. G., Molinar, A. & Daane, K. M. Factors limiting peach as a potential host for Drosophila suzukii (Diptera: Drosophilidae). J. Economic Entomol. 107, 1771–1779. https://doi.org/10.1603/EC14197 (2014).Article 

    Google Scholar 
    Keesey, I. W., Knaden, M. & Hansson, B. S. Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit. J. Chem. Ecol. 41, 121–128. https://doi.org/10.1007/s10886-015-0544-3 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Poyet, M. et al. The wide potential trophic niche of the Asiatic fruit fly Drosophila suzukii: The key of its invasion success in temperate Europe?. PLoS ONE 10, e0152785. https://doi.org/10.1371/journal.pone.0142785 (2015).CAS 
    Article 

    Google Scholar 
    Lee, J. C. et al. Characterization and manipulation of fruit susceptibility to Drosophila suzukii. J. Pest Sci. 89, 771–780. https://doi.org/10.1007/s10340-015-0692-9 (2016).Article 

    Google Scholar 
    Entling, W., Anslinger, S., Jarausch, B., Michl, G. & Hoffmann, C. Berry skin resistance explains oviposition preferences of Drosophila suzukii at the level of grape cultivars and single berries. J. Pest Sci. 92, 477–484. https://doi.org/10.1007/s10340-018-1040-7 (2019).Article 

    Google Scholar 
    Guo, L. et al. Identification of potential mechanosensitive ion channels involved in texture discrimination during Drosophila suzukii egg-laying behavior. Insect Mol. Biol. 29, 444–451. https://doi.org/10.1111/imb.12654 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kidera, H. & Takahashi, K. H. Chemical cues from competitors change the oviposition preference of Drosophila suzukii. Entomol. Exp. Appl. 168, 304–310. https://doi.org/10.1111/eea.12889 (2020).CAS 
    Article 

    Google Scholar 
    Little, C. M., Dixon, P. L., Chapman, T. W. & Hillier, N. K. Role of fruit characters and colour on host selection of boreal fruits and berries by Drosophila suzukii (Diptera: Drosophilidae). Can. Entomol. 152, 546–562. https://doi.org/10.4039/tce.2020.1 (2020).Article 

    Google Scholar 
    Tait, G. et al. Reproductive site selection: evidence of an oviposition cue in a highly adaptive Dipteran, Drosophila suzukii (Diptera: Drosophilidae). Environ. Entomol. 49, 355–363. https://doi.org/10.1093/ee/nvaa005 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Tonina, L. et al. Texture features explain the susceptibility of grapevine cultivars to Drosophila suzukii (Diptera: Drosophilidae) infestation in ripening and drying grapes. Sci. rep. 10, 10245. https://doi.org/10.1038/s41598-020-66567-9 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wernicke, M., Lethmayer, C. & Bluemel, S. Laboratory trials to investigate potential repellent/oviposition deterrent effects of selected substances on Drosophila suzukii adults. Bull. Insectol 73, 249–255 (2020).
    Google Scholar 
    Durkin, S. M. et al. Behavioral and genomic sensory adaptation underlying the pest activity of Drosophila suzukii. Mol. Biol. Evol. 38, 2532–2546. https://doi.org/10.1093/molbev/msab048 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dweck, H. K. M., Talross, G. J. S., Wang, W. & Carlson, J. R. Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii. Elife 10, e64317. https://doi.org/10.7554/eLife.64317 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Elsensohn, J. E., Aly, M. F. K., Schal, C. & Burrack, H. J. Social signals mediate oviposition site selection in Drosophila suzukii. Sci. Rep. 11, 3796. https://doi.org/10.1038/s41598-021-83354-2 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kienzle, R. & Rohlfs, M. Mind the wound!—fruit injury ranks higher than, and interacts with, heterospecific cues for Drosophila suzukii oviposition. Insects 12, 424. https://doi.org/10.3390/insects12050424 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sato, A., Tanaka, K. M., Yew, J. Y. & Takahashi, A. Drosophila suzukii avoidance of microbes in oviposition choice. R. Soc. Open Sci. 8, 201601. https://doi.org/10.1098/rsos.201601 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stockton, D. G., Cha, D. H. & Loeb, G. M. Does habituation affect the efficacy of semiochemical oviposition repellents developed against Drosophila suzukii?. Environ. Entomol. 50, 1322–1331. https://doi.org/10.1093/ee/nvab099 (2021).CAS 
    Article 
    PubMed 

    Google Scholar 
    Wöhner, T. et al. Insights into the susceptibility of raspberries to Drosophila suzukii oviposition. J. Appl Entomol. 145, 182–190. https://doi.org/10.1111/jen.12839 (2021).CAS 
    Article 

    Google Scholar 
    Baena, R. et al. Ripening stages and volatile compounds present in strawberry fruits are involved in the oviposition choice of Drosophila suzukii (Diptera: Drosophilidae). Crop Prot. 153, 105883. https://doi.org/10.1016/j.cropro.2021.105883 (2022).CAS 
    Article 

    Google Scholar 
    R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2022).Broström, G. & Holmberg, H. Generalized linear models with clustered data: Fixed and random effects models. Comput. Stat. Data Anal. 55, 3123–3134. https://doi.org/10.1016/j.csda.2011.06.011 (2011).MathSciNet 
    Article 
    MATH 

    Google Scholar 
    Asplen, M. K. et al. Invasion biology of spotted wing Drosophila (Drosophila suzukii): A global perspective and future priorities. J. Pest Sci. 88, 469–494. https://doi.org/10.1007/s10340-015-0681-z (2015).Article 

    Google Scholar 
    Knapp, L., Mazzi, D. & Finger, R. The economic impact of Drosophila suzukii: Perceived costs and revenue losses of Swiss cherry, plum and grape growers. Pest Management Sci. 77, 978–1000. https://doi.org/10.1002/ps.6110 (2020).CAS 
    Article 

    Google Scholar 
    Ishii, S. Studies on the host preference of the cowpea weevil (Callosobruchus chinensis L.). Bull. Natl. Inst. Agric. Sci. Ser. C 1, 185–156 (1952).
    Google Scholar 
    Katsoyannos, B. I. & Pittara, I. S. Effect of size of artificial oviposition substrates and presence of natural host fruits on the selection of oviposition site by Dacus oleae. Entmol. Exp. Appl. 34, 326–332 (1983).Article 

    Google Scholar 
    McDonald, P. T. & McInnis, D. O. Ceratitis capitata: Effect of host fruit size on the number of eggs per clutch. Entomol. Exp. Appl. 37, 207–211 (1985).Article 

    Google Scholar 
    Pittara, I. S. & Katsoyannos, B. I. Effect of shape, size and color on selection of oviposition sites by Chaetorellia australis. Entomol. Exp. Appl. 63, 105–113 (1992).Article 

    Google Scholar 
    Greenberg, S. M., Sappington, T. W., Sétamou, M. & Coleman, R. J. Influence of different cotton fruit sizes on boll weevil (Coleoptera: Curculionidae) oviposition and survival to adulthood. Environ. Entomol. 33, 443–449. https://doi.org/10.1603/0046-225X-33.2.443 (2004).Article 

    Google Scholar 
    Showler, A. T. Relationship of different cotton square sizes to boll weevil (Coleoptera: Curculionidae) feeding and oviposition in field conditions. J. Econ. Entomol. 98, 1572–1579. https://doi.org/10.1603/0022-0493-98.5.1572 (2005).Article 
    PubMed 

    Google Scholar 
    Charnov, E. L., Los-den Hartogh, R. L., Jones, W. T. & van den Assem, J. Sex ratio evolution in a variable environment. Nature 289, 27–33 (1981).ADS 
    CAS 
    Article 

    Google Scholar 
    Avidov, Z., Berlinger, M. J. & Applebaum, S. W. Physiological aspects of host specificity in the Bruchidae: III. Effect of curvature and surface area on oviposition of Callosobruchus chinensis L.. Anim. Behav. 13, 178–180 (1965).Article 

    Google Scholar 
    Sambaraju, K. R. & Phillips, T. W. Effects of physical and chemical factors on oviposition by Plodia interpunctella (Lepidoptera: Pyralidae). Ann. Entomol. Soc. Am. 101, 955–963 (2008).Article 

    Google Scholar 
    Schmidt, J. M. & Smith, J. J. B. Correlations between body angles and substrate curvature in the parasitoid wasp Trichogramma minutum: A possible mechanism of host radius measurement. J. Exp. Biol. 125, 271–285 (1986).Article 

    Google Scholar 
    Jois, S. et al. Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male Drosophila. Sci. Rep. 12, 1–12. https://doi.org/10.1038/s41598-022-10247-3 (2022).CAS 
    Article 

    Google Scholar 
    Crava, C. M. et al. Structural and transcriptional evidence of mechanotransduction in the Drosophila suzukii ovipositor. J. Insect Physiol. 125, 104088. https://doi.org/10.1016/j.jinsphys.2020.104088 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sampson, B. J. et al. Novel aspects of Drosophila suzukii (Diptera: Drosophilidae) biology and an improved method for culturing this invasive species with a modified D. melanogaster diet. Florida Entomol. 99, 774–780. https://doi.org/10.1653/024.099.0433 (2016).Article 

    Google Scholar  More

  • in

    Ecological and evolutionary dynamics of multi-strain RNA viruses

    Gupta, S. Chaos, persistence, and evolution of strain structure in antigenically diverse infectious agents. Science 280, 912–915 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kucharski, A. J., Andreasen, V. & Gog, J. R. Capturing the dynamics of pathogens with many strains. J. Math. Biol. 72, 1–24 (2016).PubMed 
    Article 

    Google Scholar 
    Lourenço, J. & Recker, M. Natural, persistent oscillations in a spatial multi-strain disease system with application to dengue. PLoS Comput. Biol. 9, e1003308 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gog, J. R. & Grenfell, B. T. Dynamics and selection of many-strain pathogens. Proc. Natl Acad. Sci. USA 99, 17209–17214 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Recker, M., Pybus, O. G., Nee, S. & Gupta, S. The generation of influenza outbreaks by a network of host immune responses against a limited set of antigenic types. Proc. Natl Acad. Sci. USA 104, 7711–7716 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jang, Y., Seo, T. & Seo, S. H. Higher virulence of swine H1N2 influenza viruses containing avian-origin HA and 2009 pandemic PA and NP in pigs and mice. Arch. Virol. 165, 1141–1150 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Salvesen, H. A. & Whitelaw, C. B. A. Current and prospective control strategies of influenza A virus in swine. Porcine Health Manage. 7, 23 (2021).Article 

    Google Scholar 
    Ma, W., Kahn, R. E. & Richt, J. A. The pig as a mixing vessel for influenza viruses: human and veterinary implications. J. Mol. Genet. Med. 03, 158–166 (2009).CAS 
    Article 

    Google Scholar 
    Mancera Gracia, J. C., Pearce, D. S., Masic, A. & Balasch, M. Influenza A virus in swine: epidemiology, challenges and vaccination strategies. Front. Vet. Sci. 7, 647 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Van Regenmortel, M. H. V. Virus species and virus identification: past and current controversies. Infect. Genet. Evol. 7, 133–144 (2007).PubMed 
    Article 
    CAS 

    Google Scholar 
    Lazebnik, T. & Bunimovich-Mendrazitsky, S. Generic approach for mathematical model of multi-strain pandemics. PLoS ONE 17, e0260683 (2022).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wikramaratna, P. S., Sandeman, M., Recker, M. & Gupta, S. The antigenic evolution of influenza: drift or thrift? Phil. Trans. R. Soc. B 368, 20120200 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pitzer, V. E. et al. Modeling rotavirus strain dynamics in developed countries to understand the potential impact of vaccination on genotype distributions. Proc. Natl Acad. Sci. USA 108, 19353–19358 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Grenfell, B. T. et al. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303, 327–332 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Paploski, I. A. D. et al. Temporal dynamics of co-circulating lineages of porcine reproductive and respiratory syndrome virus. Front. Microbiol. 10, 2486 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ferguson, N. M., Galvani, A. P. & Bush, R. M. Ecological and immunological determinants of influenza evolution. Nature 422, 428–433 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bishop, S. C., Axford, R. F. E., Nicholas, F. W. & Owen, J. B. Breeding for Disease Resistance in Farm Animals 3rd edn (CABI, 2010); https://doi.org/10.1079/9781845935559.0000Domingo, E. & Schuster, P. in Quasispecies: From Theory to Experimental Systems (eds Domingo, E. & Schuster, P.) 1–22 (Springer, 2015); https://doi.org/10.1007/82_2015_453Lythgoe, K. A., Gardner, A., Pybus, O. G. & Grove, J. Short-sighted virus evolution and a germline hypothesis for chronic viral infections. Trends Microbiol. 25, 336–348 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chen, N., Trible, B. R., Kerrigan, M. A., Tian, K. & Rowland, R. R. R. ORF5 of porcine reproductive and respiratory syndrome virus (PRRSV) is a target of diversifying selection as infection progresses from acute infection to virus rebound. Infect. Genet. Evol. 40, 167–175 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Carpenter, S. Identification of Genetic Mutations that Confer Escape from Innate or Adaptive Host Immune Responses During PRRSV Infection In Vivo NPB #12-173 (National Pork Board, 2014).Dimitrov, D. S. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol. 2, 109–122 (2004).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Dou, D., Revol, R., Östbye, H., Wang, H. & Daniels, R. Influenza A virus cell entry, replication, virion assembly and movement. Front. Immunol. 9, 1581 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Hamilton, B. S., Whittaker, G. R. & Daniel, S. Influenza virus-mediated membrane fusion: determinants of hemagglutinin fusogenic activity and experimental approaches for assessing virus fusion. Viruses 4, 1144–1168 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li, K. et al. Virus–host interactions in foot-and-mouth disease virus infection. Front. Immunol. 12, 571509 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Millet, J. K., Jaimes, J. A. & Whittaker, G. R. Molecular diversity of coronavirus host cell entry receptors. FEMS Microbiol. Rev. https://doi.org/10.1093/femsre/fuaa057 (2020).Wang, G., Wang, Y., Shang, Y., Zhang, Z. & Liu, X. How foot-and-mouth disease virus receptor mediates foot-and-mouth disease virus infection. Virol. J. 12, 9 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sokol, C. L. & Luster, A. D. The chemokine system in innate immunity. Cold Spring Harb. Perspect. Biol. 7, a016303 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Takeuchi, O. & Akira, S. Innate immunity to virus infection. Immunol. Rev. 227, 75–86 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Theofilopoulos, A., Baccala, R., Beutler, B. & Kono, D. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 23, 307–336 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mueller, S. N. & Rouse, B. T. in Clinical Immunology (eds Rich, R. R. et al.) 421–431 (Elsevier, 2008); https://doi.org/10.1016/B978-0-323-04404-2.10027-2Chen, X. et al. Host immune response to influenza A virus infection. Front. Immunol. 9, 320 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Agrawal, B. Heterologous immunity: role in natural and vaccine-induced resistance to infections. Front. Immunol. 10, 2631 (2019)iCAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sharma, S. & Thomas, P. G. The two faces of heterologous immunity: protection or immunopathology. J. Leukoc. Biol. 95, 405–416 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Spackman, E. & Sitaras, I. Animal Influenza Virus (Springer, 2020).Anderson, C. S., McCall, P. R., Stern, H. A., Yang, H. & Topham, D. J. Antigenic cartography of H1N1 influenza viruses using sequence-based antigenic distance calculation. BMC Bioinformatics 19, 51 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Cai, Z., Zhang, T. & Wan, X.-F. Concepts and applications for influenza antigenic cartography. Influenza Other Respi. Viruses 5, 204–207 (2011).PubMed Central 

    Google Scholar 
    Wang, P. et al. Predicting influenza antigenicity by matrix completion with antigen and antiserum similarity. Front. Microbiol. 9, 2500 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hirst, G. K. Studies of antigenic differences among strains of influenza by means of red cell agglutination. J. Exp. Med. 78, 407–423 (1943).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kendra, J. A., Tohma, K., Ford-Siltz, L. A., Lepore, C. J. & Parra, G. I. Antigenic cartography reveals complexities of genetic determinants that lead to antigenic differences among pandemic GII.4 noroviruses. Proc. Natl Acad. Sci. USA 118, e2015874118 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bell, S. M., Katzelnick, L. & Bedford, T. Dengue genetic divergence generates within-serotype antigenic variation, but serotypes dominate evolutionary dynamics. Elife 8, e42496 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yao, Y. et al. Predicting influenza antigenicity from Hemagglutintin sequence data based on a joint random forest method. Sci. Rep. 7, 1545 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Zeller, M. A. et al. Machine learning prediction and experimental validation of antigenic drift in h3 influenza A viruses in swine. mSphere 6, e00920–e00920 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wikramaratna, P. S. et al. Five challenges in modelling interacting strain dynamics. Epidemics 10, 31–34 (2015).PubMed 
    Article 

    Google Scholar 
    Elliott, P. et al. Exponential growth, high prevalence of SARS-CoV-2, and vaccine effectiveness associated with the Delta variant. Science 374, eabl9551 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bianco, S., Shaw, L. B. & Schwartz, I. B. Epidemics with multistrain interactions: the interplay between cross immunity and antibody-dependent enhancement. Chaos 19, 043123 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nickbakhsh, S. et al. Virus–virus interactions impact the population dynamics of influenza and the common cold. Proc. Natl Acad. Sci. USA 116, 27142–27150 (2019).CAS 
    PubMed Central 
    Article 

    Google Scholar 
    Poon, A. F. Y. et al. Mapping the shapes of phylogenetic trees from human and zoonotic RNA viruses. PLoS ONE 8, e78122 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lemey, P. et al. Unifying viral genetics and human transportation data to predict the global transmission dynamics of human influenza H3N2. PLoS Pathog. 10, e1003932 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Lemey, P., Rambaut, A., Drummond, A. J. & Suchard, M. A. Bayesian phylogeography finds its roots. PLoS Comput. Biol. 5, e1000520 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901–904 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gill, M. S. et al. Improving bayesian population dynamics inference: A coalescent-based model for multiple loci. Mol. Biol. Evol. 30, 713–724 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kingman, J. F. C. On the genealogy of large populations. J. Appl. Probab. 19, 27–43 (1982).Article 

    Google Scholar 
    Griffiths, R. C. & Tavare, S. Ancestral inference in population genetics. Stat. Sci. 9, 307–319 (1994).Article 

    Google Scholar 
    Magee, D., Suchard, M. A. & Scotch, M. Bayesian phylogeography of influenza A/H3N2 for the 2014–15 season in the United States using three frameworks of ancestral state reconstruction. PLoS Comput. Biol. 13, e1005389 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Müller, N. F., Rasmussen, D. & Stadler, T. MASCOT: parameter and state inference under the marginal structured coalescent approximation. Bioinformatics 34, 3843–3848 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Kühnert, D., Stadler, T., Vaughan, T. G. & Drummond, A. J. Phylodynamics with migration: a computational framework to quantify population structure from genomic data. Mol. Biol. Evol. 33, 2102–2116 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Yan, L., Neher, R. A. & Shraiman, B. I. Phylodynamic theory of persistence, extinction and speciation of rapidly adapting pathogens. Elife 8, e44205 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Paploski, I. A. D. et al. Phylogenetic structure and sequential dominance of sub-lineages of PRRSV type-2 lineage 1 in the United States. Vaccines 9, 608 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kistler, K. E. & Bedford, T. Evidence for adaptive evolution in the receptor-binding domain of seasonal coronaviruses OC43 and 229E. Elife 10, e64509 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bedford, T. et al. Integrating influenza antigenic dynamics with molecular evolution. Elife 2014, e01914 (2014).Article 

    Google Scholar 
    de Carvalho Ferreira, H. C. et al. An integrative analysis of foot-and-mouth disease virus carriers in Vietnam achieved through targeted surveillance and molecular epidemiology. Transbound. Emerg. Dis. 64, 547–563 (2017).PubMed 
    Article 
    CAS 

    Google Scholar 
    Huang, J. H. et al. Molecular characterization and phylogenetic analysis of dengue viruses imported into Taiwan during 2008–2010. Am. J. Trop. Med. Hyg. 87, 349–358 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Höckerstedt, L. M., Siren, J. P. & Laine, A.-L. Effect of spatial connectivity on host resistance in a highly fragmented natural pathosystem. J. Evol. Biol. 31, 844–852 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Papaïx, J., Burdon, J. J., Lannou, C. & Thrall, P. H. Evolution of pathogen specialisation in a host metapopulation: joint effects of host and pathogen dispersal. PLoS Comput. Biol. 10, e1003633 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Tack, A. J. M., Hakala, J., Petäjä, T., Kulmala, M. & Laine, A.-L. Genotype and spatial structure shape pathogen dispersal and disease dynamics at small spatial scales. Ecology 95, 703–714 (2014).PubMed 
    Article 

    Google Scholar 
    Smith, D. J. et al. Mapping the antigenic and genetic evolution of influenza virus. Science 305, 371–376 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Korneliussen, T. S., Moltke, I., Albrechtsen, A. & Nielsen, R. Calculation of Tajima’s D and other neutrality test statistics from low depth next-generation sequencing data. BMC Bioinformatics 14, 289 (2013).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Wargo, A. R. & Kurath, G. Viral fitness: definitions, measurement, and current insights. Curr. Opin. Virol. 2, 538–545 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dayarian, A. & Shraiman, B. I. How to infer relative fitness from a sample of genomic sequences. Genetics 197, 913–923 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Neher, R. A., Russell, C. A. & Shraiman, B. I. Predicting evolution from the shape of genealogical trees. Elife 3, e03568 (2014).PubMed Central 
    Article 

    Google Scholar 
    Doumayrou, J., Thébaud, G., Vuillaume, F., Peterschmitt, M. & Urbino, C. Mapping genetic determinants of viral traits with FST and quantitative trait locus (QTL) approaches. Virology 484, 346–353 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nagylaki, T. Fixation indices in subdivided populations. Genetics 148, 1325–1332 (1998).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nei, M. & Chesser, R. K. Estimation of fixation indices and gene diversities. Ann. Hum. Genet. 47, 253–259 (1983).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yang, Z. & Nielsen, R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17, 32–43 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tubiana, L., Božič, A. L., Micheletti, C. & Podgornik, R. Synonymous mutations reduce genome compactness in icosahedral ssRNA viruses. Biophys. J. 108, 194–202 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jordan-Paiz, A., Franco, S. & Martínez, M. A. Impact of synonymous genome recoding on the HIV life cycle. Front. Microbiol. https://doi.org/10.3389/fmicb.2021.606087 (2021).Cuevas, J. M., Domingo-Calap, P. & Sanjuán, R. The fitness effects of synonymous mutations in DNA and RNA viruses. Mol. Biol. Evol. 29, 17–20 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kryazhimskiy, S. & Plotkin, J. B. The population genetics of dN/dS. PLoS Genet. 4, e1000304 (2008).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Kosakovsky Pond, S. L. & Frost, S. D. W. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 22, 1208–1222 (2005).PubMed 
    Article 
    CAS 

    Google Scholar 
    Su, Y. C. F. et al. Phylodynamics of H1N1/2009 influenza reveals the transition from host adaptation to immune-driven selection. Nat. Commun. 6, 7952 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kryazhimskiy, S., Dieckmann, U., Levin, S. A. & Dushoff, J. On state-space reduction in multi-strain pathogen models, with an application to antigenic drift in influenza A. PLoS Comput. Biol. 3, e159 (2007).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Peralta, R., Vargas-De-León, C., Cabrera, A. & Miramontes, P. Dynamics of high-risk nonvaccine human papillomavirus types after actual vaccination scheme. Comput. Math. Methods Med. 2014, 542923 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ranjeva, S. L. et al. Recurring infection with ecologically distinct HPV types can explain high prevalence and diversity. Proc. Natl Acad. Sci. USA 114, 13573–13578 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Aguiar, M., Stollenwerk, N. & Kooi, B. W. The stochastic multi-strain dengue model: analysis of the dynamics. AIP Conf. Proc. 1389, 1224 (2011).Blower, S. M., Aschenbach, A. N., Gershengorn, H. B. & Kahn, J. O. Predicting the unpredictable: transmission of drug-resistant HIV. Nat. Med. 7, 1016–1020 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sharomi, O. & Gumel, A. B. Dynamical analysis of a multi-strain model of HIV in the presence of anti-retroviral drugs. J. Biol. Dyn. 2, 323–345 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Roche, B., Drake, J. M. & Rohani, P. An agent-based model to study the epidemiological and evolutionary dynamics of influenza viruses. BMC Bioinformatics 12, 87 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sofonea, M. T., Alizon, S. & Michalakis, Y. From within-host interactions to epidemiological competition: a general model for multiple infections. Phil. Trans. R. Soc. B 370, 20140303 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    VanderWaal, K. L. & Ezenwa, V. O. Heterogeneity in pathogen transmission: mechanisms and methodology. Funct. Ecol. 30, 1606–1622 (2016).Article 

    Google Scholar 
    Cobey, S. & Pascual, M. Consequences of host heterogeneity, epitope immunodominance, and immune breadth for strain competition. J. Theor. Biol. 270, 80–87 (2011).PubMed 
    Article 

    Google Scholar 
    Aguiar, M., Ballesteros, S., Kooi, B. W. & Stollenwerk, N. The role of seasonality and import in a minimalistic multi-strain dengue model capturing differences between primary and secondary infections: complex dynamics and its implications for data analysis. J. Theor. Biol. 289, 181–196 (2011).PubMed 
    Article 

    Google Scholar 
    Breban, R., Drake, J. M. & Rohani, P. A general multi-strain model with environmental transmission: invasion conditions for the disease-free and endemic states. J. Theor. Biol. 264, 729–736 (2010).PubMed 
    Article 

    Google Scholar 
    Kamo, M. & Sasaki, A. The effect of cross-immunity and seasonal forcing in a multi-strain epidemic model. Physica D 165, 228–241 (2002).Martcheva, M. A non-autonomous multi-strain SIS epidemic model. J. Biol. Dyn. 3, 235–251 (2009).PubMed 
    Article 

    Google Scholar 
    Pugliese, A. On the evolutionary coexistence of parasite strains. Math. Biosci. 177–178, 355–375 (2002).PubMed 
    Article 

    Google Scholar 
    Roche, B. & Rohani, P. Environmental transmission scrambles coexistence patterns of avian influenza viruses. Epidemics 2, 92–98 (2010).PubMed 
    Article 

    Google Scholar 
    Korobeinikov, A. & Dempsey, C. A continuous phenotype space model of RNA virus evolution within a host. Math. Biosci. Eng. 11, 919–927 (2014).Article 

    Google Scholar 
    Castillo-Chavez, C., Hethcote, H. W., Andreasen, V., Levin, S. A. & Liu, W. M. Epidemiological models with age structure, proportionate mixing, and cross-immunity. J. Math. Biol. 27, 233–258 (1989).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gupta, S., Swinton, J. & Anderson, R. M. Theoretical studies of the effects of heterogeneity in the parasite population on the transmission dynamics of malaria. Proc. R. Soc. B 256, 231–238 (1994).CAS 
    PubMed 
    Article 

    Google Scholar 
    Koelle, K., Khatri, P., Kamradt, M. & Kepler, T. B. A two-tiered model for simulating the ecological and evolutionary dynamics of rapidly evolving viruses, with an application to influenza. J. R. Soc. Interface 7, 1257–1274 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lion, S. & Gandon, S. Spatial evolutionary epidemiology of spreading epidemics. Proc. R. Soc. B 283, 20161170 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lange, A. & Ferguson, N. M. Antigenic diversity, transmission mechanisms, and the evolution of pathogens. PLoS Comput. Biol. 5, e1000536 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Pilosof, S. et al. Competition for hosts modulates vast antigenic diversity to generate persistent strain structure in Plasmodium falciparum. PLoS Biol. 17, e3000336 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Lipsitch, M., Colijn, C., Cohen, T., Hanage, W. P. & Fraser, C. No coexistence for free: neutral null models for multistrain pathogens. Epidemics 1, 2–13 (2009).PubMed 
    Article 

    Google Scholar 
    Read, J. M. & Keeling, M. J. Disease evolution on networks: the role of contact structure. Proc. R. Soc. Lond. B 270, 699–708 (2003).Article 

    Google Scholar 
    Eshelman, C. M. et al. Unrestricted migration favours virulent pathogens in experimental metapopulations: evolutionary genetics of a rapacious life history. Phil. Trans. R. Soc. B 365, 2503–2513 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Adam, D. C. et al. Clustering and superspreading potential of SARS-CoV-2 infections in Hong Kong. Nat. Med. 26, 1714–1719 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Makau, D. N. et al. Integrating animal movements with phylogeography to model the spread of PRRS virus in the US. Virus Evol. https://doi.org/10.1093/ve/veab060 (2021).Kistler, K. E., Huddleston, J. & Bedford, T. Rapid and parallel adaptive mutations in spike S1 drive clade success in SARS-CoV-2. Cell Host Microbe 30, 545–555 (2022).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li, H. & Roossinck, M. J. Genetic bottlenecks reduce population variation in an experimental RNA virus population. J. Virol. 78, 10582–10587 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McCrone, J. T. et al. Stochastic processes constrain the within and between host evolution of influenza virus. Elife 7, e35962 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nelson, M. I. et al. Stochastic processes are key determinants of short-term evolution in influenza A virus. PLoS Pathog. 2, e125 (2006).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Deng, X. et al. Genomic surveillance reveals multiple introductions of SARS-CoV-2 into Northern California. Science 369, 582–587 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    da Silva Filipe, A. et al. Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland. Nat. Microbiol. 6, 112–122 (2021).PubMed 
    Article 
    CAS 

    Google Scholar 
    Tayoun, A. A. et al. Multiple early introductions of SARS-CoV-2 into a global travel hub in the Middle East. Sci. Rep. 10, 17720 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Obermeyer, F. et al. Analysis of 2.1 million SARS-CoV-2 genomes identifies mutations associated with transmissibility. Science 376, 1327–1332 (2022).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wikramaratna, P. S., Pybus, O. G. & Gupta, S. Contact between bird species of different lifespans can promote the emergence of highly pathogenic avian influenza strains. Proc. Natl Acad. Sci. USA 111, 10767–10772 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Volz, E. M., Koelle, K. & Bedford, T. Viral phylodynamics. PLoS Comput. Biol. 9, e1002947 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evolut. Biol. 22, 245–259 (2009).CAS 
    Article 

    Google Scholar 
    Clay, P. A. & Rudolf, V. H. W. How parasite interaction strategies alter virulence evolution in multi‐parasite communities. Evolution 73, 2189–2203 (2019).PubMed 
    Article 

    Google Scholar 
    Bishop, S. C., Doeschl-Wilson, A. B. & Woolliams, J. A. Uses and implications of field disease data for livestock genomic and genetics studies. Front. Genet. 3, 114 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    Rodríguez‐Nevado, C., Lam, T. T. Y., Holmes, E. C. & Pagán, I. The impact of host genetic diversity on virus evolution and emergence. Ecol. Lett. 21, 253–263 (2018).PubMed 
    Article 

    Google Scholar 
    Schulte, R. D., Makus, C. & Schulenburg, H. Host–parasite coevolution favours parasite genetic diversity and horizontal gene transfer. J. Evol. Biol. 26, 1836–1840 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Duxbury, E. M. L. et al. Host–pathogen coevolution increases genetic variation in susceptibility to infection. Elife 8, e46440 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chabas, H. et al. Evolutionary emergence of infectious diseases in heterogeneous host populations. PLoS Biol. 16, e2006738 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Ganusov, V. V., Bergstrom, C. T. & Antia, R. Within‐host population dynamics and the evolution of microparasites in a heterogeneous host population. Evolution 56, 213–223 (2002).PubMed 
    Article 

    Google Scholar 
    González, R., Butković, A. & Elena, S. F. Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus†. Virus Evol. 5, vez024 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Regoes, R. R., Nowak, M. A. & Bonhoeffer, S. Evolution of virulence in a heterogeneous host population. Evolution 54, 64–71 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yates, A., Antia, R. & Regoes, R. R. How do pathogen evolution and host heterogeneity interact in disease emergence? Proc. R. Soc. B 273, 3075–3083 (2006).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rochman, N. D. et al. Ongoing global and regional adaptive evolution of SARS-CoV-2. Proc. Natl Acad. Sci. USA 118, e2104241118 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Volz, E. et al. Assessing transmissibility of SARS-CoV-2 lineage B.1.1.7 in England. Nature 593, 266–269 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Choi, B. et al. Persistence and evolution of SARS-CoV-2 in an immunocompromised host. N. Engl. J. Med. 383, 2291–2293 (2020).PubMed 
    Article 

    Google Scholar 
    Gidari, A. et al. Cross-neutralization of SARS-CoV-2 B.1.1.7 and P.1 variants in vaccinated, convalescent and P.1 infected. J. Infect. 83, 467–472 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Changrob, S. et al. Cross-neutralization of emerging SARS-CoV-2 variants of concern by antibodies targeting distinct epitopes on spike. MBio https://doi.org/10.1128/mBio.02975-21 (2021).Vidal, S. J. et al. Correlates of neutralization against SARS-CoV-2 variants of concern by early pandemic sera. J. Virol. 95, e0040421 (2021).PubMed 
    Article 

    Google Scholar 
    Muik, A. et al. Neutralization of SARS-CoV-2 lineage B.1.1.7 pseudovirus by BNT162b2 vaccine-elicited human sera. Science 371, 1152–1153 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bushman, M., Kahn, R., Taylor, B. P., Lipsitch, M. & Hanage, W. P. Population impact of SARS-CoV-2 variants with enhanced transmissibility and/or partial immune escape. Cell 184, 6229–6242 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Koopman, J. S., Simon, C. P., Getz, W. M. & Salter, R. Modeling the population effects of escape mutations in SARS-CoV-2 to guide vaccination strategies. Epidemics 36, 100484 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Correlating gut microbial membership to brown bear health metrics

    Van Valen, L. Morphological variation and width of ecological niche. Am. Nat. 99, 377–390 (1965).Article 

    Google Scholar 
    Bolnick, D. I., Svanbäck, R., Araújo, M. S. & Persson, L. Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. PNAS 104, 10075–10079 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bearhop, S., Adams, C. E., Waldron, S., Fuller, R. A. & Macleod, H. Determining trophic niche width: A novel approach using stable isotope analysis. J. Anim. Ecol. 73, 1007–1012 (2004).Article 

    Google Scholar 
    Hooper, D. U. et al. Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol. Monogr. 75, 3–35 (2005).Article 

    Google Scholar 
    Roederer, J. G. & Malone, T. F. (eds) Resilience of Ecosystems: Local Surprise and Global Change 228–269 (Cambridge University Press, 1985).
    Google Scholar 
    Duffy, J. E. et al. The functional role of biodiversity in ecosystems: Incorporating trophic complexity. Ecol. Lett. 10, 522–538 (2007).PubMed 
    Article 

    Google Scholar 
    Lafferty, D. J. R., Belant, J. L. & Phillips, D. L. Testing the niche variation hypothesis with a measure of body condition. Oikos 124, 732–740 (2015).Article 

    Google Scholar 
    Mangipane, L. S. et al. Dietary plasticity in a nutrient-rich system does not influence brown bear (Ursus arctos) body condition or denning. Polar Biol. 41, 763–772 (2018).Article 

    Google Scholar 
    Mangipane, L. S. et al. Dietary plasticity and the importance of salmon to brown bear (Ursus arctos) body size and condition in a low Arctic ecosystem. Polar Biol. 43, 825–833 (2020).Article 

    Google Scholar 
    Stumpf, R. M. et al. Microbiomes, metagenomics, and primate conservation: New strategies, tools, and applications. Biol. Conserv. 199, 56–66 (2016).Article 

    Google Scholar 
    McKenney, E. A., Koelle, K., Dunn, R. R. & Yoder, A. D. The ecosystem services of animal microbiomes. Mol. Ecol. 27, 2164–2172 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L. & Gordon, J. I. Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Martin, A. M., Sun, E. W., Rogers, G. B. & Keating, D. J. The influence of the gut microbiome on host metabolism through the regulation of gut hormone release. Front. Physiol. 10, 428 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Amato, K. R. et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb. Ecol. 69, 434–443 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006).ADS 
    PubMed 
    Article 

    Google Scholar 
    Cani, P. D. & Delzenne, N. M. Interplay between obesity and associated metabolic disorders: New insights into the gut microbiota. Curr. Opin. Pharmacol. 9, 737–743 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Arinell, K. et al. Brown bears (Ursus arctos) seem resistant to atherosclerosis­despite highly elevated plasma lipids during hibernation and active state. Clin. Transl. Sci. 5, 269–272 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Nelson, R. A. Protein and fat metabolism in hibernating bears. Fed. Proc. 39, 2955–2958 (1980).CAS 
    PubMed 

    Google Scholar 
    Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McKenney, E. A., Maslanka, M., Rodrigo, A. & Yoder, A. D. Bamboo specialists from two mammalian orders (primates, carnivora) share a high number of low-abundance gut microbes. Microb. Ecol. 76, 272–284 (2018).PubMed 
    Article 

    Google Scholar 
    Edwards, M. A., Derocher, A. E., Hobson, K. A., Branigan, M. & Nagy, J. A. Fast carnivores and slow herbivores: Differential foraging strategies among grizzly bears in the Canadian Arctic. Oecologia 165, 877–889 (2011).ADS 
    PubMed 
    Article 

    Google Scholar 
    Levi, T. et al. Community ecology and conservation of bear-salmon ecosystems. Front. Ecol. Evol. 8, 513304 (2020).Article 

    Google Scholar 
    Milakovic, B. & Parker, K. L. Quantifying carnivory by grizzly bears in a multi-ungulate system. J. Wildl. Manage. 77, 39–47 (2013).Article 

    Google Scholar 
    Krajmalnik-Brown, R., Ilhan, Z.-E., Kang, D.-W. & DiBaise, J. K. Effects of gut microbes on nutrient absorption and energy regulation. Nutr. Clin. Pract. 27, 201–214 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Flint, H. J., Scott, K. P., Duncan, S. H., Louis, P. & Forano, E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3, 289–306 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hashimoto, T., Hussien, R. & Brooks, G. A. Colocalization of MCT1, CD147, and LDH in mitochondrial inner membrane of L6 muscle cells: Evidence of a mitochondrial lactate oxidation complex. Am. J. Physiol.-Endocrinol. Metab. 290, E1237–E1244 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Baker, S. & The, H. C. Recent insights into Shigella: A major contributor to the global diarrhoeal disease burden. Curr. Opin. Infect. Dis. 31, 449–454 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lee, K.-E. et al. The extracellular vesicle of gut microbial Paenalcaligenes hominis is a risk factor for vagus nerve-mediated cognitive impairment. Microbiome 8, 107 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Waites, K. B., Schelonka, R. L., Xiao, L., Grigsby, P. L. & Novy, M. J. Congenital and opportunistic infections: Ureaplasma species and Mycoplasma hominis. Semin. Fetal Neonatal. Med. 14, 190–199 (2009).PubMed 
    Article 

    Google Scholar 
    Barboza, P. S., Farley, S. D. & Robbins, C. T. Whole-body urea cycling and protein turnover during hyperphagia and dormancy in growing bears (Ursus americanus and U. arctos). Can. J. Zool. 75, 2129. https://doi.org/10.1139/z97-848 (2011).Article 

    Google Scholar 
    Johanne Hansen, M. et al. Ursidibacter maritimus gen. nov., sp. nov. and Ursidibacter arcticus sp. nov., two new members of the family Pasteurellaceae isolated from the oral cavity of bears. Int. J. Syst. Evol. Microbiol. 65, 3683–3689 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Waldram, A. et al. Top-down systems biology modeling of host metabotype-microbiome associations in obese rodents. J. Proteome Res. 8, 2361–2375 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hardie, J. M. & Whiley, R. A. The genus Streptococcus. In The Genera of Lactic Acid Bacteria (eds Wood, B. J. B. & Holzapfel, W. H.) 55–124 (Springer, 1995).Chapter 

    Google Scholar 
    Li, F., Wang, M., Wang, J., Li, R. & Zhang, Y. Alterations to the gut microbiota and their correlation with inflammatory factors in chronic kidney disease. Front. Cell. Infect. Microbiol. 9, 206 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fox, J. G. & Lee, A. The role of Helicobacter species in newly recognized gastrointestinal tract diseases of animals. Lab. Anim. Sci. 47, 222–255 (1997).CAS 
    PubMed 

    Google Scholar 
    McKenney, E. A., Rodrigo, A. & Yoder, A. D. Patterns of gut bacterial colonization in three primate species. PLoS ONE 10, e0124618 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Stevens, C. E. & Hume, I. D. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol. Rev. 78, 393–427 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hilderbrand, G. V. et al. Plasticity in physiological condition of female brown bears across diverse ecosystems. Polar Biol. 41, 773–780 (2018).Article 

    Google Scholar 
    Ley, R. E. et al. Obesity alters gut microbial ecology. PNAS 102, 11070–11075 (2005).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sommer, F. et al. The gut microbiota modulates energy metabolism in the hibernating brown bear ursus arctos. Cell Rep. 14, 1655–1661 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Magne, F. et al. The firmicutes/bacteroidetes ratio: A relevant marker of gut dysbiosis in obese patients? Nutrients 12, 1474 (2020).CAS 
    PubMed Central 
    Article 

    Google Scholar 
    Paine, R. T. A note on trophic complexity and community stability. Am. Nat. 103, 91–93 (1969).Article 

    Google Scholar 
    Amato, K. R. et al. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576–587 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Trujillo, S. M. et al. Intrinsic and extrinsic factors influence on an omnivore’s gut microbiome. PLoS ONE 17, e0266698 (2022).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hilderbrand, G. V. et al. Body size and lean mass of brown bears across and within four diverse ecosystems. J. Zool. 305, 53–62 (2018).Article 

    Google Scholar 
    Wilson, R. R., Gustine, D. D. & Joly, K. Evaluating potential effects of an industrial road on winter habitat of caribou in North-Central Alaska. Arctic 67, 472–482 (2014).Article 

    Google Scholar 
    Gasaway, W. C. et al. The role of predation in limiting moose at low densities in Alaska and Yukon and implications for conservation. Wildl. Monogr. 12, 3–59 (1992).
    Google Scholar 
    Taylor, W. P., Reynolds, H. V. & Ballard, W. B. Immobilization of grizzly bears with tiletamine hydrochloride and zolazepam hydrochloride. J. Wildl. Manage. 53, 978–981 (1989).Article 

    Google Scholar 
    Farley, S. D. & Robbins, C. T. Development of two methods to estimate body composition of bears. Can. J. Zool. 72, 220–226 (1994).Article 

    Google Scholar 
    Hilderbrand, G. V., Robbins, C. T. & Farley, S. D. Response: Use of stable isotopes to determine diets of living and extinct bears. Can. J. Zool. 76, 2301–2303 (1998).Article 

    Google Scholar 
    McKenney, E. A., Greene, L. K., Drea, C. M. & Yoder, A. D. Down for the count: Cryptosporidium infection depletes the gut microbiome in Coquerel’s sifakas. Microb. Ecol. Health Dis. 28, 1335165 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Willis, A. D. Rarefaction, alpha diversity, and statistics. Front. Microbiol. 10, 2407 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Beule, L. & Karlovsky, P. Improved normalization of species count data in ecology by scaling with ranked subsampling (SRS): Application to microbial communities. PeerJ 8, e9593 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Galand, P. E., Casamayor, E. O., Kirchman, D. L. & Lovejoy, C. Ecology of the rare microbial biosphere of the Arctic Ocean. Proc. Natl. Acad. Sci. U.S.A. 106, 22427–22432 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Liu, L., Yang, J., Yu, Z. & Wilkinson, D. M. The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME J. 9, 2068–2077 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hill, M. O. Diversity and evenness: A unifying notation and its consequences. Ecology 54, 427–432 (1973).Article 

    Google Scholar 
    Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).Article 

    Google Scholar 
    Simpson, E. H. Measurement of diversity. Nature 163, 688–688 (1949).ADS 
    MATH 
    Article 

    Google Scholar 
    Lozupone, C. & Knight, R. UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235 (2006).ADS 
    Article 
    CAS 

    Google Scholar 
    Hamidi, B., Wallace, K., Vasu, C. & Alekseyenko, A. V. Wd∗$Wd*-test: Robust distance-based multivariate analysis of variance. Microbiome 7, 51 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Alekseyenko, A. V. Multivariate Welch t-test on distances. Bioinformatics 32, 3552–3558 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More