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    Free-living and particle-attached bacterial community composition, assembly processes and determinants across spatiotemporal scales in a macrotidal temperate estuary

    Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Martiny, J. B. H. et al. Microbial biogeography: Putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. H. Beyond biogeographic patterns: Processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Grossart, H. P. Ecological consequences of bacterioplankton lifestyles: Changes in concepts are needed. Environ. Microbiol. Rep. 2, 706–714 (2010).PubMed 
    Article 

    Google Scholar 
    Simon, M., Grossart, H. P., Schweitzer, B. & Ploug, H. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28, 175–211 (2002).Article 

    Google Scholar 
    Smith, D. C., Simon, M., Alldredge, A. L. & Azam, F. Intense hydrolytic enzyme activity on marine aggregates and implication for rapid particle dissolution. Nature 359, 139–141 (1992).ADS 
    CAS 
    Article 

    Google Scholar 
    Grossart, H. P., Tang, K. W., Kiørboe, T. & Ploug, H. Comparison of cell-specific activity between free-living and attached bacteria using isolates and natural assemblages. FEMS Microbiol. Lett. 206, 194–200 (2007).Article 
    CAS 

    Google Scholar 
    Rieck, A., Herlemann, D. P. R., Jürgens, K. & Grossart, H. Particle-associated differ from free-living bacteria in surface waters of the Baltic Sea. Front. Microbiol. 6, 1297 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Karner, M. & Herndl, G. J. Extracellular enzymatic activity and secondary production in free-living and marine-snow-associated bacteria. Mar. Biol. 113, 341–347 (1992).CAS 
    Article 

    Google Scholar 
    Lyons, M. M. & Dobbs, F. C. Differential utilization of carbon substrates by aggregate-associated and water-associated heterotrophic bacterial communities. Hydrobiologia 686, 181–193 (2012).CAS 
    Article 

    Google Scholar 
    Simon, H. M., Smith, M. W. & Herfort, L. Metagenomic insights into particles and their associated microbiota in a coastal margin ecosystem. Front. Microbiol. 5, 466 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Smith, M. W., Allen, L. Z., Allen, A. E., Herfort, L. & Simon, H. M. Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem. Front. Microbiol. 4, 120 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Mestre, M. et al. Spatial variability of marine bacterial and archaeal communities along the particulate matter continuum. Mol. Ecol. 26, 6827–6840 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bižic-Ionescu, M. et al. Comparison of bacterial communities on limnic versus coastal marine particles reveals profound differences in colonization. Environ. Microbiol. 17, 3500–3514 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Hollibaugh, J. T., Wong, P. S. & Murrell, M. C. Similarity of particle-associated and free-living bacterial communities in northern San Francisco Bay, California. Aquat. Microb. Ecol. 21, 103–114 (2000).Article 

    Google Scholar 
    Ortega-Retuerta, E., Joux, F., Jeffrey, W. H. & Ghiglione, J. F. Spatial variability of particle-attached and free-living bacterial diversity in surface waters from the Mackenzie River to the Beaufort Sea (Canadian Arctic). Biogeosciences 10, 2747–2759 (2013).ADS 
    Article 

    Google Scholar 
    Noble, P. A., Bidle, K. D. & Fletcher, M. Natural microbial community compositions compared by a back-propagating neural network and cluster analysis of 5S rRNA. Appl. Environ. Microbiol. 63, 1762–1770 (1997).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhou, J. & Ning, D. Stochastic community assembly: Does it matter in microbial ecology?. Microbiol. Mol. Biol. Rev. 81, e00002-17 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jain, A., Balmonte, J. P., Singh, R., Bhaskar, P. V. & Krishnan, K. P. Spatially resolved assembly, connectivity and structure of particle-associated and free-living bacterial communities in a high Arctic fjord. FEMS Microbiol. Ecol. 97, 1–12 (2021).Article 
    CAS 

    Google Scholar 
    Yao, Z. et al. Bacterial community assembly in a typical estuarine marsh. Appl. Environ. Microbiol. 85, e02602-18 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wang, J. et al. Assembly processes and source tracking of planktonic and benthic bacterial communities in the Yellow River estuary. Environ. Microbiol. 23, 2578–2591 (2021).PubMed 
    Article 

    Google Scholar 
    Balmonte, J. P. et al. Sharp contrasts between freshwater and marine microbial enzymatic capabilities, community composition, and DOM pools in a NE Greenland fjord. Limnol. Oceanogr. 65, 77–95 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    Fortunato, C. S., Herfort, L., Zuber, P., Baptista, A. M. & Crump, B. C. Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient. ISME J. 6, 554–563 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yawata, Y., Carrara, F., Menolascina, F. & Stocker, R. Constrained optimal foraging by marine bacterioplankton on particulate organic matter. Proc. Natl. Acad. Sci. USA 117, 25571–25579 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hu, Y. et al. The relationships between the free-living and particle-attached bacterial communities in response to elevated eutrophication. Front. Microbiol. 11, 423 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lima-Mendez, G. et al. Determinants of community structure in the grobal plankton interactome. Science (80-) 348, 1262073-1–10 (2015).Article 
    CAS 

    Google Scholar 
    Milici, M. et al. Co-occurrence analysis of microbial taxa in the Atlantic ocean reveals high connectivity in the free-living bacterioplankton. Front. Microbiol. 7, 649 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Herren, C. M. & McMahon, K. D. Cohesion: A method for quantifying the connectivity of microbial communities. ISME J. 11, 2426–2438 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Friedman, J. & Alm, E. J. Inferring correlation networks from genomic survey data. PLoS Comput. Biol. 8, e1002687 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Deng, Y. et al. Molecular ecological network analyses. BMC Bioinform. 13, 113 (2012).Article 

    Google Scholar 
    Labry, C. et al. High alkaline phosphatase activity in phosphate replete waters: The case of two macrotidal estuaries. Limnol. Oceanogr. 61, 1513–1529 (2016).ADS 
    Article 

    Google Scholar 
    Crump, B. C. et al. Quantity and quality of particulate organic matter controls bacterial production in the Columbia River estuary. Limnol. Oceanogr. 62, 2713–2731 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    Canuel, E. A. & Hardison, A. K. Sources, ages, and alteration of organic matter in Estuaries. Ann. Rev. Mar. Sci. 8, 409–434 (2016).PubMed 
    Article 

    Google Scholar 
    He, W., Chen, M., Schlautman, M. A. & Hur, J. Dynamic exchanges between DOM and POM pools in coastal and inland aquatic ecosystems: A review. Sci. Total Environ. 551–552, 415–428 (2016).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Bianchi, T. S. The role of terrestrially derived organic carbon in the coastal ocean: A changing paradigm and the priming effect. Proc. Natl. Acad. Sci. 108, 19473–19481 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Auffret, G. A. Dynamique sédimentaire de la marge continentale celtique-Evolution Cénozoïque-Spécificité du Pleistocène supérieur et de l’Holocène (Université de Bordeaux I, 1983).
    Google Scholar 
    Delmas, R. & Tréguer, P. Évolution saisonnière des nutriments dans un écosystème eutrophe d’Europe occidentale (la rade de Brest). Interactions marines et terrestres. Oceanol. Acta 6, 345–356 (1983).CAS 

    Google Scholar 
    Bassoullet, P. Etude de la dynamique des sédiments en suspension dans l’estuaire de l’Aulne (rade de Brest) (Université de Bretagne Occidentale, 1979).
    Google Scholar 
    Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bolyen, E. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Olesen, S. W., Duvallet, C. & Alm, E. J. dbOTU3: A new implementation of distribution-based OTU calling. PLoS ONE 12, 1–13 (2017).Article 
    CAS 

    Google Scholar 
    Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, 590–596 (2013).Article 
    CAS 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (2013).Whickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).Book 

    Google Scholar 
    Lê, S., Josse, J. & Husson, F. FactoMineR: An R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).Article 

    Google Scholar 
    Wei, T. & Simko, V. R package ‘corrplot’: Visualization of a Correlation Matrix (2011).McMurdie, P. J. & Holmes, S. Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Oksanen, J. et al. Vegan: Community Ecology Package (2022).Liu, C., Cui, Y., Li, X. & Yao, M. Microeco: An R package for data mining in microbial community ecology. FEMS Microbiol. Ecol. 97, fiaa255 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kandlikar, G. ranacapa: Utility Functions and ‘shiny’ App for Simple Environmental DNA Visualizations and Analyses (2021).Cao, Y. microbiomeMarker: microbiome biomarker analysis toolkit (2021).Tsirogiannis, C. & Brody, S. PhyloMeasures: Fast and Exact Algorithms for Computing Phylogenetic Biodiversity Measures (2017).McKnight, D. T. et al. Methods for normalizing microbiome data: An ecological perspective. Methods Ecol. Evol. 10, 389–400 (2019).Article 

    Google Scholar 
    Paradis, E. & Schliep, K. Ape 50: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics https://doi.org/10.1093/bioinformatics/bty633 (2019).Article 
    PubMed 

    Google Scholar 
    Legendre, P. & Legendre, L. Numerical Ecology (Third English Edition) (Elsevier, 2012).MATH 

    Google Scholar 
    Stegen, J. C., Lin, X., Fredrickson, J. K. & Konopka, A. E. Estimating and mapping ecological processes influencing microbial community assembly. Front. Microbiol. 6, 370 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Stegen, J. C., Lin, X., Konopka, A. E. & Fredrickson, J. K. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J. 6, 1653–1664 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Naimi, B. usdm: Uncertainty Analysis for Species Distribution Models (2017).Wu, W., Xu, Z., Dai, M., Gan, J. & Liu, H. Homogeneous selection shapes free-living and particle-associated bacterial communities in subtropical coastal waters. Divers. Distrib. 00, 1–14 (2020).
    Google Scholar 
    Wang, Y. et al. Patterns and processes of free-living and particle-associated bacterioplankton and archaeaplankton communities in a subtropical river-bay system in South China. Limnol. Oceanogr. 65, 161–179 (2020).
    Google Scholar 
    Zhou, L. et al. Environmental filtering dominates bacterioplankton community assembly in a highly urbanized estuarine ecosystem. Environ. Res. 196, 110934 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Graham, E. B. & Stegen, J. C. Dispersal-based microbial community assembly decreases biogeochemical function. Processes 5, 65 (2017).Article 

    Google Scholar 
    Campbell, B. J. & Kirchman, D. L. Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J. 7, 210–220 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Herlemann, D. P. R. et al. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 5, 1571–1579 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fuhrman, J. A., Cram, J. A. & Needham, D. M. Marine microbial community dynamics and their ecological interpretation. Nat. Rev. Microbiol. 13, 133–146 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science (80-) 348, 1261359 (2015).Article 
    CAS 

    Google Scholar 
    Buchan, A., LeCleir, G. R., Gulvik, C. A. & González, J. M. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat. Rev. Microbiol. 12, 686–698 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Martinez-Garcia, M. et al. Capturing single cell genomes of active polysaccharide degraders: An unexpected contribution of verrucomicrobia. PLoS ONE 7, e35314 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Reintjes, G., Arnosti, C., Fuchs, B. M. & Amann, R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 11, 1640–1650 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gralka, M., Szabo, R., Stocker, R. & Cordero, O. X. Trophic interactions and the drivers of microbial community assembly. Curr. Biol. 30, R1176–R1188 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Liu, J., Meng, Z., Liu, X. & Zhang, X. H. Microbial assembly, interaction, functioning, activity and diversification: a review derived from community compositional data. Mar. Life Sci. Technol. 1, 112–128 (2019).ADS 
    Article 

    Google Scholar 
    Hernandez, D. J., David, A. S., Menges, E. S., Searcy, C. A. & Afkhami, M. E. Environmental stress destabilizes microbial networks. ISME J. 15, 1722–1734 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Herren, C. M. & McMahon, K. D. Keystone taxa predict compositional change in microbial communities. Environ. Microbiol. 20, 2207–2217 (2018).PubMed 
    Article 

    Google Scholar 
    Liénart, C. et al. Dynamics of particulate organic matter composition in coastal systems: A spatio-temporal study at multi-systems scale. Prog. Oceanogr. 156, 221–239 (2017).Article 

    Google Scholar 
    Fraisse, S., Bormans, M. & Lagadeuc, Y. Morphofunctional traits reflect differences in phytoplankton community between rivers of contrasting flow regime. Aquat. Ecol. 47, 315–327 (2013).Article 

    Google Scholar 
    Treguer, P. & Queguiner, B. Seasonal variations in conservative and nonconservative mixing of nitrogen compounds in a West European macrotidal estuary. Oceanol. Acta 12, 371–380 (1989).CAS 

    Google Scholar 
    Grossart, H. P. & Tang, K. W. Communicative & integrative biology. Commun. Integr. Biol. 3, 491–494 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

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    The combination of genomic offset and niche modelling provides insights into climate change-driven vulnerability

    Wiens, J. J. Climate-related local extinctions are already widespread among plant and animal species. PLoS Biol. 14, e2001104 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Scheffers, B. R. et al. The broad footprint of climate change from genes to biomes to people. Science 354, aaf7671 (2016).PubMed 
    Article 
    CAS 

    Google Scholar 
    Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Urban, M. C. Accelerating extinction risk from climate change. Science 348, 571–573 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Wingfield, J. C. et al. Organism-environment interactions in a changing world: a mechanistic approach. J. Ornithol. 152, 279–288 (2011).Article 

    Google Scholar 
    Mendoza-Gonzalez, G., Martinez, M. L., Rojas-Soto, O. R., Vazquez, G. & Gallego-Fernandez, J. B. Ecological niche modeling of coastal dune plants and future potential distribution in response to climate change and sea level rise. Glob. Change Biol. 19, 2524–2535 (2013).ADS 
    Article 

    Google Scholar 
    Saunders, S. P. et al. Community science validates climate suitability projections from ecological niche modeling. Ecol. Appl. 30, 17 (2020).Article 

    Google Scholar 
    Peterson, A. T., Cobos, M. E. & Jimenez-Garcia, D. Major challenges for correlational ecological niche model projections to future climate conditions. Ann. N. Y. Acad. Sci. 1429, 66–77 (2018).ADS 
    PubMed 
    Article 

    Google Scholar 
    Mays, H. L. et al. Genomic analysis of demographic history and Ecological niche modeling in the endangered Sumatran Rhinoceros Dicerorhinus sumatrensis. Curr. Biol. 28, 70–76 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Malcolm, R. J., Liu, C., Neilson, P. R., Hansen, L. & Hannah, L. A. Global warming and extinctions of endemic species from biodiversity hotspots. Conserv. Biol. 20, 538–548 (2005).Article 

    Google Scholar 
    Fitzpatrick, M. C. & Keller, S. R. Ecological genomics meets community-level modelling of biodiversity: mapping the genomic landscape of current and future environmental adaptation. Ecol. Lett. 18, 1–16 (2015).PubMed 
    Article 

    Google Scholar 
    Gotelli, J. N. & Stanton-Geddes, J. Climate change, genetic markers and species distribution modelling. J. Biogeogr. 42, 1577–1585 (2015).Article 

    Google Scholar 
    Ruegg, K. et al. Ecological genomics predicts climate vulnerability in an endangered southwestern songbird. Ecol. Lett. 21, 1085–1096 (2018).PubMed 
    Article 

    Google Scholar 
    Razgour, O. et al. Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections. Proc. Natl Acad. Sci. USA 116, 10418–10423 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Valladares, F. et al. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17, 1351–1364 (2014).PubMed 
    Article 

    Google Scholar 
    Bay, R. A. et al. Genomic signals of selection predict climate-driven population declines in a migratory bird. Science 359, 83–86 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Rhone, B. et al. Pearl millet genomic vulnerability to climate change in West Africa highlights the need for regional collaboration. Nat. Commun. 11, 5274 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rahbek, C. et al. Building mountain biodiversity: geological and evolutionary processes. Science 365, 1114–1119 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Fjeldså, J., Bowie, R. C. K. & Rahbek, C. The role of mountain ranges in the diversification of birds. Annu. Rev. Ecol. Evol. Syst. 43, 249–265 (2012).Article 

    Google Scholar 
    Freeman, B. G., Scholer, M. N., Ruiz-Gutierrez, V. & Fitzpatrick, J. W. Climate change causes upslope shifts and mountaintop extirpations in a tropical bird community. Proc. Natl Acad. Sci. USA 115, 11982–11987 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    He, J. K., Lin, S. L., Li, J. T., Yu, J. H. & Jiang, H. S. Evolutionary history of zoogeographical regions surrounding the Tibetan Plateau. Commun. Biol. 3, 9 (2020).Article 
    CAS 

    Google Scholar 
    Wu, Y. J. et al. Explaining the species richness of birds along a subtropical elevational gradient in the Hengduan Mountains. J. Biogeogr. 40, 2310–2323 (2013).Article 

    Google Scholar 
    del Hoyo, J., Elliott, A., Sargatal, J. & Christie, D. A. Handbook of the Birds of the World (Lynx Edicions, 2013).Qu, Y. et al. Lineage diversification and historical demography of a montane bird Garrulax elliotii – implications for the Pleistocene evolutionary history of the eastern Himalayas. BMC Evolut. Biol. 11, 174 (2011).Article 

    Google Scholar 
    Qu, Y. et al. Long-term isolation and stability explain high genetic diversity in the Eastern Himalaya. Mol. Ecol. 23, 705–720 (2014).PubMed 
    Article 

    Google Scholar 
    Wang, W. J. et al. Glacial expansion and diversification of an East Asian montane bird, the green-backed tit (Parus monticolus). J. Biogeogr. 40, 1156–1169 (2013).Article 

    Google Scholar 
    Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Laine, V. N. et al. Evolutionary signals of selection on cognition from the great tit genome and methylome. Nat. Commun. 7, 9 (2016).Article 
    CAS 

    Google Scholar 
    Ellis, N., Smith, S. J. & Pitcher, C. R. Gradient forests: calculating importance gradients on physical predictors. Ecology 93, 156–168 (2012).PubMed 
    Article 

    Google Scholar 
    Giorgetta, M. A. Climate and carbon cycle changes from 1850 to 2100 in MPI-ESM simulations for the Coupled Model Intercomparison Project phase 5. J. Adv. Model. Earth Syst. 5, 572–597 (2013).ADS 
    Article 

    Google Scholar 
    Gent, P. R. et al. The community climate system model version 4. J. Clim. 24, 4973–4991 (2011).ADS 
    Article 

    Google Scholar 
    Watanabe, M. et al. Improved climate simulation by MIROC5: mean states, variability, and climate sensitivity. J. Clim. 23, 6312–6335 (2010).ADS 
    Article 

    Google Scholar 
    Voldoire, A. et al. The CNRM-CM5.1 global climate model: description and basic evaluation. Clim. Dyn. 40, 2091–2121 (2013).Article 

    Google Scholar 
    Frichot, E., Schoville, S. D., Bouchard, G. & Francois, O. Testing for associations between loci and environmental gradients using latent factor mixed models. Mol. Biol. Evol. 30, 1687–1699 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Forester, B. R., Jones, M. R., Joost, S., Landguth, E. L. & Lasky, J. R. Detecting spatial genetic signatures of local adaptation in heterogeneous landscapes. Mol. Ecololgy 25, 104–120 (2016).CAS 
    Article 

    Google Scholar 
    Forester, B. R., Lasky, J. R., Wagner, H. H. & Urban, D. L. Comparing methods for detecting multilocus adaptation with multivariate genotype-environment associations. Mol. Ecol. 27, 2215–2233 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Li, C. et al. Two Antarctic penguin genomes reveal insights into their evolutionary history and molecular changes related to the Antarctic environment. Gigascience 3, 27 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pirri, F. et al. Selection-driven adaptation to the extreme Antarctic environment in Emperor penguin. Preprint at bioRxiv https://doi.org/10.1101/2021.12.14.471946 (2021).Wang, L. C. et al. Involvement of the Arabidopsis HIT1/AtVPS53 tethering protein homologuein the acclimation of the plasma membrane to heat stess.J. Exp. Bot. 62, 3609–3620 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Piñol, R. A. et al. Preoptic BRS3 neurons increase body temperature and heart rate via multiple pathways. Cell Metab. 33, 1389–1403 (2021).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Guilherme, A. et al. Neuronal modulation of brown adipose activity through perturbation of white adipocyte lipogenesis. Mol. Metab. 16, 116–125 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhang, Y., Guo, W., zhang, Y., Zhang, H. & Wu, C. Insights into hypoxic adaptation in Tibetan chicken embryos from comparative proteomics. Comp. Biochem. Physiol. Part D. 31, 100602 (2019).CAS 

    Google Scholar 
    Pizzagalli, M. D., Bensimon, A. & Superti-Furga, G. A guide to plasma membrane solute carrier proteins. FEBS J. 288, 2784–2835 (2020).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Qu, Y. et al. Rapid phenotypic evolution with shallow genomic differentiation during early stages of high elevation adaptation in Eurasian Tree Sparrows. Natl Sci. Rev. 7, 113–127 (2020).PubMed 
    Article 

    Google Scholar 
    Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ferrier, S., Manion, G., Elith, J. & Richardson, K. Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Diversity Distrib. 13, 252–264 (2007).Article 

    Google Scholar 
    Thuiller, W., Lafourcade, B., Engler, R. & Araújo, M. B. BIOMOD – a platform for ensemble forecasting of species distributions. Ecography 32, 369–373 (2009).Article 

    Google Scholar 
    Chen, Y. et al. Large-scale genome-wide reveals climate adaptive variability in a cosmopolitan pest. Nat. Commun. 12, 7206 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Clarke, R. T., Rothery, P. & Raybould, A. F. Confidence limits for regression relationships between distance matrices: Estimating gene flow with distance. J. Agric. Biol. Environ. Stat. 7, 361–372 (2002).Article 

    Google Scholar 
    Excoffier, L., Dupanloup, I., Huerta-Sanchez, E., Sousa, V. C. & Foll, M. Robust demographic inference from genomic and SNP data. PLoS Genet. 9, e1003905 (2013).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Foden, W. B. et al. Climate change vulnerability assessment of species. WIREs Clim. Change 10, e551 (2019).Article 

    Google Scholar 
    Smith, T. B. et al. Genomic vulnerablity and soci-economic threats under climate change in an African rainforest bird. Evolut. Appl. 14, 1239–1247 (2021).Article 

    Google Scholar 
    Liu, B., Liang, E. Y., Liu, K. & Camarero, J. J. Species- and elevation-dependent growth responses to climate warming of mountain forests in the Qinling Mountains, central China. Forests 9, 11 (2018).
    Google Scholar 
    Dang, H. S., Zhang, Y. J., Zhang, K. R., Jiang, M. X. & Zhang, Q. F. Climate-growth relationships of subalpine fir (Abies fargesii) across the altitudinal range in the Shennongjia Mountains, central China. Clim. Change 117, 903–917 (2013).ADS 
    Article 

    Google Scholar 
    Lingua, E., Cherubini, P., Motta, R. & Nola, P. Spatial structure along an altitudinal gradient in the Italian central Alps suggests competition and facilitation among coniferous species. J. Veg. Sci. 19, 425–436 (2008).Article 

    Google Scholar 
    Zhang, D. C., Zhang, Y. H., Boufford, D. E. & Sun, H. Elevational patterns of species richness and endemism for some important taxa in the Hengduan Mountains, southwestern China. Biodivers. Conserv. 18, 699–716 (2009).Article 

    Google Scholar 
    Zhang, R. Z., Zheng, D., Yang, Q. Y. & Liu, Y. H. Physical Geography of Hengduan Mountains (Science Press, 1997).Liu, Y. et al. Sino-Himalayan mountains act as cradles of diversity and immigration centres in the diversification of parrotbills (Paradoxornithidae). J. Biogeogr. 43, 1488–1501 (2016).Bush, A. et al. Incorporating evolutionary adaptation in species distribution modeling reduces projected vulnerability to climate change. Ecol. Lett. 17, 1468–148 (2016).Article 

    Google Scholar 
    Sparks, M. M., Westley, A. A. H., Falke, J. A. & Quinn, T. P. Thermal adaptation and phenotypic plasticity in a warming world: insights from common garden experiments on Alaskan sockeye salmon. Glob. Change Biol. 23, 5203–5217 (2017).ADS 
    Article 

    Google Scholar 
    Merow, C., Wilson, A. M. & Jetz, W. Integrating occurrence data and expert maps for improved species range predictions. Glob. Ecol. Biogeogr. 26, 243–258 (2017).Article 

    Google Scholar 
    Weisenfeld, N. I., Kumar, V., Shah, P., Church, D. M. & Jaffe, D. B. Direct determination of diploid genome sequences. Genome Res. 27, 757–767 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    She, R., Chu, J. S. C., Wang, K., Pei, J. & Chen, N. GenBlastA: enabling BLAST to identify homologous gene sequences. Genome Res. 19, 143–149 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Birney, E., Clamp, M. & Durbin, R. GeneWise and genomewise. Genome Res. 14, 988–995 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McKenna, A. et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).Article 

    Google Scholar 
    Robinson, J. D., Bunnefeld, L., Hearn, J., Stone, G. N. & Hickerson, M. J. ABC inference of multi-population divergence with admixture from unphased population genomic data. Mol. Ecol. 23, 4458–4471 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nazareno, A. G., Bemmels, J. B., Dick, C. W. & Lohmann, L. G. Minimum sample sizes for population genomics: an empirical study from an Amazonian plant species. Mol. Ecol. Resour. 17, 1136–1147 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Willing, E. M., Dreyer, C. & van Oosterhout, C. Estimates of genetic differentiation measured by FST do not necessary require large sample size when using many SNP markers. PLoS One 7, e2649 (2012).Article 
    CAS 

    Google Scholar 
    Keenan, K., Mcginnity, P., Cross, T. F., Crozier, W. W. & Prodöhl, P. A. diveRsity: an Rpackage for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol. Evol. 4, 782–788 (2013).Article 

    Google Scholar 
    Rellstab, C., Gugerli, F., Eckert, I. A., Hancock, M. A. & Holderegger, R. A practical guide to environmental assocaition analysis in landscape genomics. Mol. Ecol. 24, 4348–4370 (2015).PubMed 
    Article 

    Google Scholar 
    Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80–92 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xie, C. et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39, W316–W322 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Araújo, M. B. & New, M. Ensemble forecasting of species distributions. Trends Ecol. Evol. 22, 42–47 (2007).PubMed 
    Article 

    Google Scholar 
    Araújo, M. B. et al. Standards for distribution models in biodiversity assessments. Sci. Adv. 5, eaat4858 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Boria, R. A., Olson, L. E., Goodman, S. M. & Anderson, R. P. Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol. Model. 275, 73–77 (2014).Article 

    Google Scholar 
    Anderson, R. P. & Raza, A. The effect of the extent of the study region on GISmodels of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela. J. Biogeogr. 37, 1378–1393 (2010).Article 

    Google Scholar 
    Pearson, R. G., Raxworthy, C., Nakamura, M. & Peterson, A. T. Predicting species distributions from small numbers of occurrence records: a test case using crypticgeckos in Madagascar. J. Biogeogr. 34, 102–117 (2007).Article 

    Google Scholar 
    Heming, N. M., Dambros, C. & Gutiérrez, E. E. ENMwizard: advanced techniques for Ecological Niche Modeling made easy. https://github.com/HemingNM/ENMwizard (2018).Naimi, B., Hamm, N. A. S., Groen, T. A., Skidmore, A. K. & Toxopeus, A. G. Where is positional uncertainty a problem for species distribution modelling. Ecography 37, 191–203 (2014).Article 

    Google Scholar 
    Muscarella, R. et al. ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for MAXENT ecological niche models. Methods Ecol. Evol. 5, 1198–1205 (2014).Article 

    Google Scholar 
    Owens, H. L. et al. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol. Model. 263, 10–18 (2013).Article 

    Google Scholar 
    Akaike, H. New look at statistical-model identification. IEEE Trans. Autom. Control AC19, 716–723 (1974).ADS 
    MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Phillips, S. J. et al. Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. Ecol. Appl. 19, 181–197 (2009).PubMed 
    Article 

    Google Scholar 
    Barbet-Massin, M., Jiguet, F., Albert, C. H. & Thuiller, W. Selecting pseudo-absences for species distribution models: how, where and how many? Methods Ecol. Evol. 3, 327–338 (2012).Article 

    Google Scholar 
    Bellard, C. et al. Will climate change promote future invasions? Glob. Change Biol. 19, 3740–3748 (2013).ADS 
    Article 

    Google Scholar 
    Elith, J., Kearney, M. & Phillips, S. The art of modelling range-shifting species. Methods Ecol. Evol. 1, 330–342 (2010).Article 

    Google Scholar 
    Anantharaman, R., Hall, K., Shah, V. B. & Edelman, A. Circuitscape in Julia: high performance connectivity modelling to support conservation decisions. Proc. JuliaCon Conf. 1, 58 (2020).Article 

    Google Scholar 
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

    Google Scholar 
    Anderson, D. R. & Burnham, K. P. Avoiding pitfalls when using information-theoretic methods. J. Wildl. Manag. 66, 912–918 (2002).Article 

    Google Scholar 
    Van Strien, M. J., Keller, D. & Holderegger, R. A new analytical approach to landscape genetic modelling: least-cost transect analysis and linear mixed models. Mol. Ecol. 21, 4010–4023 (2012).Article 

    Google Scholar 
    Bartoń, K. MuMIn: multi-model inference, R package version 1.9.13 (2013).Zhang, G. et al. Comparative genomics reveal insights into avian genome evolution and adaptation. Science 346, 1311–1320 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Roesti, M., Kueng, B., Moser, D. & Berner, D. The genomics of ecological vicariance in threespine stickleback fish. Nat. Commun. 6, 8767 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    Effectiveness of protected areas influenced by socio-economic context

    Tittensor, D. P. et al. A mid-term analysis of progress toward international biodiversity targets. Science 346, 241–243 (2014).CAS 
    Article 

    Google Scholar 
    IPBES Secretariat Summary for Policymakers of the Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science—Policy Platform on Biodiversity and Ecosystem Services (IPBES, 2019).Bruner, A. G., Gullison, R. E., Rice, R. E. & Fonseca, G. A. Bda Effectiveness of parks in protecting tropical biodiversity. Science 291, 125–128 (2001).CAS 
    Article 

    Google Scholar 
    Geldmann, J., Joppa, L. N. & Burgess, N. D. Mapping change in human pressure globally on land and within protected areas. Conserv. Biol. 28, 1604–1616 (2014).Article 

    Google Scholar 
    Laurance, W. F. et al. Averting biodiversity collapse in tropical forest protected areas. Nature 489, 290–293 (2012).CAS 
    Article 

    Google Scholar 
    Conference of the Parties, The Strategic Plan for Biodiversity 2011–2020 and the Aichi Biodiversity Targets, COP-10 Decision X/2 (CBD, 2010).Protected Planet Report 2018 (UNEP-WCMC IUCN & NGS, 2018).Craigie, I. D. et al. Large mammal population declines in Africa’s protected areas. Biol. Conserv. 143, 2221–2228 (2010).Article 

    Google Scholar 
    Joppa, L. N., Bailie, J. E. M. & Robinson, J. G. Protected Areas: Are They Safeguarding Biodiversity?. (Wiley Blackwell, 2016).Book 

    Google Scholar 
    Rada, S. et al. Protected areas do not mitigate biodiversity declines: a case study on butterflies. Divers. Distrib. 25, 217–224 (2019).Article 

    Google Scholar 
    Jetz, W., McPherson, J. M. & Guralnick, R. P. Integrating biodiversity distribution knowledge: toward a global map of life. Trends Ecol. Evol. 27, 151–159 (2012).Article 

    Google Scholar 
    Geldmann, J. et al. Effectiveness of terrestrial protected areas in reducing habitat loss and population declines. Biol. Conserv. 161, 230–238 (2013).Article 

    Google Scholar 
    Kindsvater, H. K. et al. Overcoming the data crisis in biodiversity conservation. Trends Ecol. Evol. 33, 676–688 (2018).Article 

    Google Scholar 
    Sutherland, W. J., Pullin, A. S., Dolman, P. M. & Knight, T. M. The need for evidence-based conservation. Trends Ecol. Evol. 19, 305–308 (2004).Article 

    Google Scholar 
    Ferraro, P. J. & Pattanayak, S. K. Money for nothing? A call for empirical evaluation of biodiversity conservation investments. PLoS Biol. 4, 482–488 (2006).CAS 
    Article 

    Google Scholar 
    Polaina, E., González-Suárez, M. & Revilla, E. Socioeconomic correlates of global mammalian conservation status. Ecosphere 6, 1–34. (2015).Article 

    Google Scholar 
    Ferraro, P. J. & Pressey, R. L. Measuring the difference made by conservation initiatives: protected areas and their environmental and social impacts. Philos. Trans. R. Soc. Lond. Biol. Sci. 370, 20140270 (2015).Article 

    Google Scholar 
    Geldmann, J., Manica, A., Burgess, N. D., Coad, L. & Balmford, A. A global-level assessment of the effectiveness of protected areas at resisting anthropogenic pressures. Proc. Natl Acad. Sci. U.S.A. 116, 23209–23215 (2019).CAS 
    Article 

    Google Scholar 
    McGinnis, M. D. & Ostrom, E. Social-ecological system framework: initial changes and continuing challenges. Ecol. Soc. 19, 30 (2014).Article 

    Google Scholar 
    Barnes, M. D. et al. Wildlife population trends in protected areas predicted by national socio-economic metrics and body size. Nat. Commun. 7, 12747 (2016).CAS 
    Article 

    Google Scholar 
    Palomo, I. et al. Incorporating the social-ecological approach in protected areas in the anthropocene. BioScience 64, 181–191 (2014).Article 

    Google Scholar 
    Poteete, A. R., Janssen, M. A., & Ostrom, E. Working Together: Collective Action, the Commons, and Multiple Methods in Practice (Princeton Univ. Press, 2010).Wilson, D. S., Ostrom, E. & Cox, M. E. Generalizing the core design principles for the efficacy of groups. J. Econ. Behav. Organ. 90, S21–S32 (2013).Article 

    Google Scholar 
    Tebet, G., Trimble, M. & Pereira Medeiros, R. Using Ostrom’s principles to assess institutional dynamics of conservation: lessons from a marine protected area in Brazil. Mar. Policy 88, 174–181 (2018).Article 

    Google Scholar 
    Ban, N. C. et al. Social and ecological effectiveness of large marine protected areas. Glob. Environ. Change 43, 82–91 (2017).Article 

    Google Scholar 
    Fleischman, F. D. et al. Governing large-scale social-ecological systems: lessons from five cases. Int. J. Commons 8, 428–456 (2014).Article 

    Google Scholar 
    Faff, R., Ho, Y. K., Lin, W. & Yap, C. M. Diminishing marginal returns from R&D investment: evidence from manufacturing firms. Appl. Econ. 45, 611–622 (2013).Article 

    Google Scholar 
    Gill, D. A. et al. Capacity shortfalls hinder the performance of marine protected areas globally. Nature 543, 665–669 (2017).CAS 
    Article 

    Google Scholar 
    Bowles, S. & Polanía-Reyes, S. Economic incentives and social preferences: substitutes or complements? J. Econ. Lit. 50, 368–425 (2012).Article 

    Google Scholar 
    Irwin, K., Mulder, L. & Simpson, B. The detrimental effects of sanctions on intragroup trust: comparing punishments and rewards. Soc. Psychol. Q. 77, 253–272 (2014).Article 

    Google Scholar 
    Pacifici, M. et al. Assessing species vulnerability to climate change. Nat. Clim. Change 5, 215–225. (2015).Article 

    Google Scholar 
    Urban, M. Accelerating extinction risk from climate change. Science 348, 571–573 (2015).CAS 
    Article 

    Google Scholar 
    Lovett, G. M. et al. Effects of air pollution on ecosystems and biological diversity in the eastern United States. Ann. N. Y. Acad. Sci. 1162, 99–135 (2009).CAS 
    Article 

    Google Scholar 
    Backhaus, T., Snape, J. & Lazorchak, J. The impact of chemical pollution on biodiversity and ecosystem services: the need for an improved understanding. Integr. Environ. Assess. Manag. 8, 575–576 (2012).CAS 
    Article 

    Google Scholar 
    Benítez-López, A. et al. The impact of hunting on tropical mammal and bird populations. Science 356, 180–183 (2017).Article 
    CAS 

    Google Scholar 
    Calabrese, A. et al. Conservation status of Asian elephants: the influence of habitat and governance. Biodivers. Conserv. 26, 2067–2081 (2017).Article 

    Google Scholar 
    Shaffer, L. J., Khadka, K. K., Van Den Hoek, J. & Naithani, K. J. Human–elephant conflict: a review of current management strategies and future directions. Front. Ecol. Evol. 6, 235 (2019).Article 

    Google Scholar 
    Klaassen, R. H. G. et al. When and where does mortality occur in migratory birds? Direct evidence from long-term satellite tracking of raptors. J. Anim. Ecol. 83, 176–184 (2014).Article 

    Google Scholar 
    Güneralp, P. & Seto, K. C. Futures of global urban expansion: uncertainties and implications for biodiversity conservation. Environ. Res. Lett. 8, 014025 (2013).Article 

    Google Scholar 
    Sherry, T.W., Johnson, M.D. & Strong, A. in Birds of Two Worlds. The Ecology and Evolution of Migration (eds Greenberg, R. & Marra, P. P.) 414–425 (The John Hopkins Univ. Press, 2005).Sanderson, F. J., Donald, P. F., Pain, D. J., Burfield, I. J. & Van Bommel, F. P. Long-term population declines in Afro-Palearctic migrant birds. Biol. Conserv. 131, 93–105 (2006).Article 

    Google Scholar 
    Runge, C. A. et al. Protected areas and global conservation of migratory birds. Science 350, 1255–1258 (2015).CAS 
    Article 

    Google Scholar 
    Balme, G. A., Slotow, R. & Hunter, L. T. B. Edge effects and the impact of non-protected areas in carnivore conservation: leopards in the Phinda-Mkhuze Complex, South Africa. Anim. Conserv. 13, 315–323 (2010).Article 

    Google Scholar 
    Chase, J. M., Blowes, S. A., Knight, T. M., Gerstner, K. & May, F. Ecosystem decay exacerbates biodiversity loss with habitat loss. Nature 584, 238–243 (2020).CAS 
    Article 

    Google Scholar 
    Ostrom, E. Governing the Commons: The Evolution of Institutions for Collective Action (Cambridge Univ. Press, 1990).Lacroix, K. & Richards, G. An alternative policy evaluation of the British Columbia carbon tax: broadening the application of Elinor Ostrom’s design principles for managing common-pool resources. Ecol. Soc. 20, 38 (2015).Article 

    Google Scholar 
    Bennett, N. J. et al. Mainstreaming the social sciences in conservation. Conserv. Biol. 31, 56–66 (2017).Article 

    Google Scholar 
    Dasgupta, P. The Economics of Biodiversity: The Dasgupta Review (HM Treasury, 2021).Resasco, J. Meta-analysis on a decade of testing corridor efficacy: what new have we learned? Curr. Landsc. Ecol. Rep. 4, 61–69 (2019).Article 

    Google Scholar 
    Andrade, G. S. M. & Rhodes, J. R. Protected areas and local communities: an inevitable partnership toward successful conservation strategies? Ecol. Soc. https://doi.org/10.5751/ES-05216-170414 (2012).Morell, V. Massive wolf kill disrupts long-running Yellowstone Park study. Science 375, 482–482 (2022).CAS 
    Article 

    Google Scholar 
    Post, G. & Geldmann, J. Exceptional responders in conservation. Conserv. Biol. 32, 576–583 (2018).Article 

    Google Scholar 
    Wauchope, H. S. et al. Protected areas have a mixed impact on waterbirds, but management helps. Nature 605, 103–107 (2022).CAS 
    Article 

    Google Scholar 
    Ostrom, E. A general framework for analyzing sustainability of social–ecological systems. Science 325, 419–422 (2009).CAS 
    Article 

    Google Scholar 
    Kline, M. A., Waring, T. M. & Salerno, J. D. Designing cultural multilevel selection research for sustainability science. Sustainability Sci. 13, 9–19 (2017).Article 

    Google Scholar 
    Lindsey, P. A. et al. The performance of African protected areas for lions and their prey. Biol. Conserv. 209, 137–149 (2017).Article 

    Google Scholar 
    The World Database on Protected Areas (WDPA) (IUCN & UNEP‐WCMC, 2018); https://www.protectedplanet.net/en/search-areas?geo_type=country&filters%5Bdb_type%5D%5B%5D=wdpaCoad, L. et al. Measuring impact of protected area management interventions: current and future use of the global database of protected area management effectiveness. Phil. Trans. R. Soc. B 370, 20140281 (2015).Article 

    Google Scholar 
    Geldmann, J. et al. A global analysis of management capacity and ecological outcomes in terrestrial protected areas. Conserv. Lett. 11, e12434 (2018).Article 

    Google Scholar 
    Living Planet Database (LPD) (Zoological Society of London, 2018); http://www.livingplanetindex.orgKühl, H., Williamson, L., Sanz, C. M., Morgan, D. & Boesch, C. Launch of A.P.E.S. database. Gorilla Journal 34, 20–21 (2007).
    Google Scholar 
    Koerner, S. E., Poulsen, J. R., Blanchard, E. J., Okouyi, J. & Clark, C. J. Vertebrate community composition and diversity declines along a defaunation gradient radiating from rural villages in Gabon. J. Appl. Ecol. 54, 805–814 (2017).Article 

    Google Scholar 
    Bauer, H. et al. Lion (Panthera leo) populations are declining rapidly across Africa, except in intensively managed areas. Proc. Natl Acad. Sci. U.S.A. 112, 14894–14899 (2015).CAS 
    Article 

    Google Scholar 
    Barr, D., Levy, R., Scheepers, C. & Tily, H. J. Random effects structure for confirmatory hypothesis testing: keep it maximal. J. Mem. Lang. 68, 1–43 (2014).
    Google Scholar 
    Schielzeth, H. & Forstmeier, W. Conclusions beyond support: overconfident estimates in mixed models. Behav. Ecol. 20, 416–420 (2009).Article 

    Google Scholar 
    McElreath, R. in Statistical Rethinking: A Bayesian Course with Examples in R and Stan (CRC Press, 2016).Bürkner, P. C. (2017). brms: an R package for Bayesian multilevel models using Stan. J. Stat. Software https://doi.org/10.18637/jss.v080.i01 (2017).Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010).Article 

    Google Scholar 
    R Core Team R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2019).Gelman, A., Carlin, J. B. B., Stern, H. S. S. & Rubin, D. B. B. Bayesian Data Analysis (CRC Press, 2014).Protected Planet: The World Database on Protected Areas (WDPA) (UNEP-WCMC & IUCN, 2019); www.protectedplanet.netChamberlain, S. rphylopic: Get ‘Silhouettes’ of ‘Organisms’ from ‘Phylopic’. R version 0.3.3.91 https://github.com/sckott/rphylopic (2022). More

  • in

    Expression plasticity regulates intraspecific variation in the acclimatization potential of a reef-building coral

    Gregg T. M., Mead L., Burns J. H., Takabayashi M. Puka mai he ko ‘a: the significance of corals in Hawaiian culture. In: Ethnobiology of Corals and Coral Reefs). (Springer, 2015).Chevin, L.-M., Lande, R. & Mace, G. M. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8, e1000357 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Hochachka P. W., Somero G. N. Biochemical adaptation: mechanism and process in physiological evolution. (Oxford university press, 2002).Munday, P. L., Warner, R. R., Monro, K., Pandolfi, J. M. & Marshall, D. J. Predicting evolutionary responses to climate change in the sea. Ecol. Lett. 16, 1488–1500 (2013).PubMed 
    Article 

    Google Scholar 
    Seebacher, F., White, C. R. & Franklin, C. E. Physiological plasticity increases resilience of ectothermic animals to climate change. Nat. Clim. Change 5, 61–66 (2015).ADS 
    Article 

    Google Scholar 
    Coles, S. L., Jokiel, P. L. & Lewis, C. R. Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac. Sci. 30, 159–166 (1976).
    Google Scholar 
    Pandolfi, J. M. et al. Global trajectories of the long-term decline of coral reef ecosystems. Science 301, 955–958 (2003).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    LaJeunesse, T. C. et al. Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. Curr. Biol. 28, 2570–2580 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Glynn, P. W. Coral reef bleaching: ecological perspectives. Coral Reefs 12, 1–17 (1993).ADS 
    Article 

    Google Scholar 
    Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Van Hooidonk, R. et al. Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci. Rep. 6, 1–8 (2016).Article 
    CAS 

    Google Scholar 
    Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895–898 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Silverstein, R. N., Cunning, R. & Baker, A. C. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob. Change Biol. 21, 236–249 (2015).ADS 
    Article 

    Google Scholar 
    Ziegler, M. et al. Coral bacterial community structure responds to environmental change in a host-specific manner. Nat. Commun. 10, 1–11 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Rivera, H. E. et al. A framework for understanding gene expression plasticity and its influence on stress tolerance. Mol. Ecol. 30, 1381–1397 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Drury C. & Lirman D. Genotype by environment interactions in coral bleaching. Proceedings of the Royal Society B: Biological Sciences 288, 20210177 (2021).Drury, C., Manzello, D. & Lirman, D. Genotype and local environment dynamically influence growth, disturbance response and survivorship in the threatened coral, Acropora cervicornis. PLoS ONE 12, e0174000 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Todd, P. A. Morphological plasticity in scleractinian corals. Biol. Rev. 83, 315–337 (2008).PubMed 
    Article 

    Google Scholar 
    Eirin-Lopez J. M. & Putnam H. M. Marine environmental epigenetics. Annual review of marine science 11, 335–368 (2019).Putnam, H. M., Davidson, J. M. & Gates, R. D. Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evolut. Appl. 9, 1165–1178 (2016).CAS 
    Article 

    Google Scholar 
    Dixon, G., Liao, Y., Bay, L. K. & Matz, M. V. Role of gene body methylation in acclimatization and adaptation in a basal metazoan. Proc. Natl Acad. Sci. 115, 13342–13346 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rodriguez‐Casariego, J. A., Cunning, R., Baker, A. C. & Eirin‐Lopez, J. M. Symbiont shuffling induces differential DNA methylation responses to thermal stress in the coral Montastraea cavernosa. Mol. Ecol. 31, 588–602 (2022).PubMed 
    Article 
    CAS 

    Google Scholar 
    Meyer, E., Aglyamova, G. & Matz, M. Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA‐Seq procedure. Mol. Ecol. 20, 3599–3616 (2011).CAS 
    PubMed 

    Google Scholar 
    Barshis, D. J. et al. Genomic basis for coral resilience to climate change. Proc. Natl Acad. Sci. 110, 1387–1392 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460–1462 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Dixon, G., Abbott, E. & Matz, M. Meta‐analysis of the coral environmental stress response: Acropora corals show opposing responses depending on stress intensity. Mol. Ecol. 29, 2855–2870 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Traylor-Knowles, N., Rose, N. H., Sheets, E. A. & Palumbi, S. R. Early transcriptional responses during heat stress in the coral Acropora hyacinthus. Biol. Bull. 232, 91–100 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Majerová, E., Carey, F. C., Drury, C. & Gates, R. D. Preconditioning improves bleaching tolerance in the reef‐building coral Pocillopora acuta through modulations in the programmed cell death pathways. Mol. Ecol. 30, 3560–3574 (2021).PubMed 
    Article 
    CAS 

    Google Scholar 
    Vidal-Dupiol, J. et al. Thermal stress triggers broad Pocillopora damicornis transcriptomic remodeling, while Vibrio coralliilyticus infection induces a more targeted immuno-suppression response. PLoS ONE 9, e107672 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Middlebrook, R., Hoegh-Guldberg, O. & Leggat, W. The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J. Exp. Biol. 211, 1050–1056 (2008).PubMed 
    Article 

    Google Scholar 
    Bellantuono, A. J., Granados-Cifuentes, C., Miller, D. J., Hoegh-Guldberg, O. & Rodriguez-Lanetty, M. Coral thermal tolerance: tuning gene expression to resist thermal stress. PLoS ONE 7, e50685 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bay, R. A. & Palumbi, S. R. Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biol. Evol. 7, 1602–1612 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ainsworth, T. D. et al. Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352, 338–342 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    van Oppen, M. J., Oliver, J. K., Putnam, H. M. & Gates, R. D. Building coral reef resilience through assisted evolution. Proc. Natl Acad. Sci. 112, 2307–2313 (2015).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    National Academies of Sciences E, and Medicine. A Research Review of Interventions to Increase the Persistence and Resilience of Coral Reefs. (The National Academies Press, 2019).Kellett M., Hoffmann A. A., Mckechnie S. W. Hardening capacity in the Drosophila melanogaster species group is constrained by basal thermotolerance. Funct. Ecol. 19, 853–858 (2005).Gerken, A. R., Eller, O. C., Hahn, D. A. & Morgan, T. J. Constraints, independence, and evolution of thermal plasticity: probing genetic architecture of long-and short-term thermal acclimation. Proc. Natl Acad. Sci. 112, 4399–4404 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Calosi, P., Bilton, D. T. & Spicer, J. I. Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biol. Lett. 4, 99–102 (2008).PubMed 
    Article 

    Google Scholar 
    Nyamukondiwa, C., Terblanche, J. S., Marshall, K. & Sinclair, B. Basal cold but not heat tolerance constrains plasticity among Drosophila species (Diptera: Drosophilidae). J. Evolut. Biol. 24, 1927–1938 (2011).CAS 
    Article 

    Google Scholar 
    Bellantuono, A. J., Hoegh-Guldberg, O. & Rodriguez-Lanetty, M. Resistance to thermal stress in corals without changes in symbiont composition. Proc. R. Soc. Lond. B: Biol. Sci. 279, 1100–1107 (2011).
    Google Scholar 
    DeMerlis, A. et al. Pre-exposure to a variable temperature treatment improves the response of Acropora cervicornis to acute thermal stress. Coral Reefs, 41, 1–11 (2022).Oliver, T. & Palumbi, S. Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30, 429–440 (2011).ADS 
    Article 

    Google Scholar 
    Klepac, C. & Barshis, D. Reduced thermal tolerance of massive coral species in a highly variable environment. Proc. R. Soc. B 287, 20201379 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bahr, K. D., Jokiel, P. L. & Rodgers, K. S. The 2014 coral bleaching and freshwater flood events in Kāneʻohe Bay, Hawaiʻi. PeerJ 3, e1136 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cunning, R., Ritson-Williams, R. & Gates, R. D. Patterns of bleaching and recovery of Montipora capitata in Kāne’ohe Bay, Hawai’i, USA. Mar. Ecol. Prog. Ser. 551, 131–139 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    Innis, T., Cunning, R., Ritson-Williams, R., Wall, C. & Gates, R. Coral color and depth drive symbiosis ecology of Montipora capitata in Kāne’ohe Bay, O’ahu, Hawai’i. Coral Reefs 37, 423–430 (2018).ADS 
    Article 

    Google Scholar 
    Wall C. B., Ritson-Williams R., Popp B. N., Gates R. D. Spatial variation in the biochemical and isotopic composition of corals during bleaching and recovery. Limnol. Oceanogr. 64, 2011–2028 (2019).Ritson-Williams, R. & Gates, R. D. Coral community resilience to successive years of bleaching in Kane ‘ohe Bay, Hawai ‘i. Coral Reefs 10, 757–769 (2020).Article 

    Google Scholar 
    Drury, C. et al. Intrapopulation adaptive variance supports thermal tolerance in a reef-building coral. Commun. Biol. 5, 1–10 (2022).Article 
    CAS 

    Google Scholar 
    Dilworth J., Caruso C., Kahkejian V. A., Baker A. C., Drury C. Host genotype and stable differences in algal symbiont communities explain patterns of thermal stress response of Montipora capitata following thermal pre-exposure and across multiple bleaching events. Coral Reefs 40, 151–163 (2020).Pinzón, J. H. et al. Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. R. Soc. Open Sci. 2, 140214 (2015).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Thomas, L. & Palumbi, S. R. The genomics of recovery from coral bleaching. Proc. R. Soc. Lond. B: Biol. Sci. 284, 20171790 (2017).
    Google Scholar 
    Bertucci, A., Foret, S., Ball, E. & Miller, D. J. Transcriptomic differences between day and night in Acropora millepora provide new insights into metabolite exchange and light‐enhanced calcification in corals. Mol. Ecol. 24, 4489–4504 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Drury, C. Resilience in reef-building corals: the ecological and evolutionary importance of the host response to thermal stress. Mol. Ecol. 00, 1–18 (2019).CAS 

    Google Scholar 
    Whitehead, A. & Crawford, D. L. Neutral and adaptive variation in gene expression. Proc. Natl Acad. Sci. 103, 5425–5430 (2006).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kenkel, C. D. & Matz, M. V. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol. 1, 1–6 (2016).
    Google Scholar 
    Cunning, R. & Baker, A. C. Thermotolerant coral symbionts modulate heat stress‐responsive genes in their hosts. Mol. Ecol. 29, 2940–2950 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    van Heerwaarden, B. & Kellermann, V. Does plasticity trade off with basal heat tolerance? Trends Ecol. Evol. 35, 874–885 (2020).PubMed 
    Article 

    Google Scholar 
    Sasaki, M. C. & Dam, H. G. Negative relationship between thermal tolerance and plasticity in tolerance emerges during experimental evolution in a widespread marine invertebrate. Evolut. Appl. 14, 2114–2123 (2021).Article 

    Google Scholar 
    Roach T.N., Dilworth J., Jones A.D., Quinn R.A., Drury C. Metabolomic signatures of coral bleaching history. Nat. Ecol. Evol. 5, 1–9 (2021).Snider, J., Thibault, G. & Houry, W. A. The AAA+ superfamily of functionally diverse proteins. Genome Biol. 9, 1–8 (2008).Article 
    CAS 

    Google Scholar 
    Moon, S. Y. & Zheng, Y. Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13, 13–22 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hobbs, G. A., Zhou, B., Cox, A. D. & Campbell, S. L. Rho GTPases, oxidation, and cell redox control. Small GTPases 5, e28579 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Majerová E., Drury C. A BI-1 mediated cascade improves redox homeostasis during thermal stress and prevents oxidative damage in a preconditioned reef-building coral. bioRxiv, (2021).Coleman, M. & Olson, M. Rho GTPase signalling pathways in the morphological changes associated with apoptosis. Cell Death Differ. 9, 493–504 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Opalińska, M. & Jańska, H. AAA proteases: guardians of mitochondrial function and homeostasis. Cells 7, 163 (2018).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Matsuda, S. et al. Coral bleaching susceptibility is predictive of subsequent mortality within but not between coral species. Front. Ecol. Evol. 8, 1–14 (2020).Barott, K. L. et al. Coral bleaching response is unaltered following acclimatization to reefs with distinct environmental conditions. Proc. Natl Acad. Sci. 118, 1–8 (2021).Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011).Article 

    Google Scholar 
    Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Williams, A. et al. Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata. PeerJ 9, e12335 (2021).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Shumaker, A. et al. Genome analysis of the rice coral Montipora capitata. Sci. Rep. 9, 2571 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kriventseva, E. V. et al. OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 47, D807–D811 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hunter, S. et al. InterPro: the integrative protein signature database. Nucleic Acids Res. 37, D211–D215 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bateman, A. et al. The Pfam protein families database. Nucleic Acids Res. 32, D138–D141 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Leggat, W., Heron, S. F., Fordyce, A., Suggett, D. J. & Ainsworth, T. D. Experiment Degree Heating Week (eDHW) as a novel metric to reconcile and validate past and future global coral bleaching studies. J. Environ. Manag. 301, 113919 (2022).Article 

    Google Scholar 
    Ritz, C., Baty, F., Streibig, J. C. & Gerhard, D. Dose-response analysis using R. PloS ONE 10, e0146021 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 1–21 (2014).Article 
    CAS 

    Google Scholar 
    Philip, D. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14, 927–930 (2003).Wright, R. M. et al. Positive genetic associations among fitness traits support evolvability of a reef-building coral under multiple stressors. Glob. Change Biol. 25, 3294–3304 (2019).ADS 
    Article 

    Google Scholar 
    Drury C., Dilworth J., Majerová E., Caruso C., Greer J. B. Expression plasticity regulates intraspecific variation in the acclimatization potential of a reef-building coral [dataset]. Zenodo https://doi.org/10.5281/zenodo.6877825 (2022). More

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    The microbiome of a bacterivorous marine choanoflagellate contains a resource-demanding obligate bacterial associate

    Worden, A. Z. et al. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347, 1257594 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Bjorbækmo, M. F. M., Evenstad, A., Røsæg, L. L., Krabberød, A. K. & Logares, R. The planktonic protist interactome: where do we stand after a century of research? ISME J. 14, 544–559 (2020).PubMed 
    Article 

    Google Scholar 
    Pandolfi, J. M., Staples, T. L. & Kiessling, W. Increased extinction in the emergence of novel ecological communities. Science 370, 220–222 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jürgens, K. & Massana, R. in Microbial Ecology of the Oceans (ed. Kirchman, D. L.) 383–441 (John Wiley & Sons, 2008).Archibald, J. M. Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 25, R911–R921 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    McCutcheon, J. P. & Moran, N. A. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10, 13–26 (2011).PubMed 
    Article 
    CAS 

    Google Scholar 
    Drew, G. C., Stevens, E. J. & King, K. C. Microbial evolution and transitions along the parasite–mutualist continuum. Nat. Rev. Microbiol. 19, 623–638 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Buck, K. R., Chavez, F. P. & Thomsen, H. A. Choanoflagellates of the central California waters: abundance and distribution. Ophelia 33, 179–186 (1991).Article 

    Google Scholar 
    Leadbeater, B. S. C. The Choanoflagellates: Evolution, Biology and Ecology (Cambridge Univ. Press, 2015).de Vargas, C. et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Alegado, R. A. et al. A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1, e00013 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Woznica, A. et al. Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. Proc. Natl Acad. Sci. USA 113, 7894–7899 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Woznica, A., Gerdt, J. P., Hulett, R. E., Clardy, J. & King, N. Mating in the closest living relatives of animals is induced by a bacterial chondroitinase. Cell 170, 1175–1183.e11 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Needham, D. M. et al. A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. Proc. Natl Acad. Sci. USA 116, 20574–20583 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Needham, D. M. et al. Targeted metagenomic recovery of four divergent viruses reveals shared and distinctive characteristics of giant viruses of marine eukaryotes. Phil. Trans. R. Soc. Lond. B 374, 20190086 (2019).CAS 
    Article 

    Google Scholar 
    Frank, N., Helge Abuldhauge, T. & Daniel, J. R. Bridging the gap between morphological species and molecular barcodes – exemplified by loricate choanoflagellates. Eur. J. Protistol. 57, 26–37 (2017).Article 

    Google Scholar 
    Logares, R. et al. Disentangling the mechanisms shaping the surface ocean microbiota. Microbiome 8, 55 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Eldin, C. et al. From Q fever to Coxiella burnetii infection: a paradigm change. Clin. Microbiol. Rev. 30, 115–190 (2017).PubMed 
    Article 

    Google Scholar 
    Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lenski, R. E. in Advances in Microbial Ecology (ed. Marshall, K. C.) 1–44 (Springer, 1988).Zimmerman, A. E. et al. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat. Rev. Microbiol. 18, 21–34 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Vincent, F., Sheyn, U., Porat, Z., Schatz, D. & Vardi, A. Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise. Proc. Natl Acad. Sci. USA 118, e2021586118 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mruwat, N. et al. A single-cell polony method reveals low levels of infected Prochlorococcus in oligotrophic waters despite high cyanophage abundances. ISME J 15, 41–54 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Canbäck, B., Tamas, I. & Andersson, S. G. E. A phylogenomic study of endosymbiotic bacteria. Mol. Biol. Evol. 21, 1110–1122 (2004).PubMed 
    Article 
    CAS 

    Google Scholar 
    Giovannoni, S. J. SAR11 bacteria: the most abundant plankton in the oceans. Annu. Rev. Mar. Sci. 9, 231–255 (2017).Article 

    Google Scholar 
    Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pachiadaki, M. G. et al. Charting the complexity of the marine microbiome through single-cell genomics. Cell 179, 1623–1635.e11 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cordero, O. X. & Polz, M. F. Explaining microbial genomic diversity in light of evolutionary ecology. Nat. Rev. Microbiol. 12, 263–273 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Delmont, T. O. et al. Single-amino acid variants reveal evolutionary processes that shape the biogeography of a global SAR11 subclade. eLife 8, e46497 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kashtan, N. et al. Single-cell genomics reveals hundreds of coexisting subpopulations in wild. Prochlorococcus. Science 344, 416–420 (2014).CAS 
    PubMed 

    Google Scholar 
    Toft, C. & Andersson, S. G. E. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat. Rev. Genet. 11, 465–475 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Qiu, J. & Luo, Z.-Q. Legionella and Coxiella effectors: strength in diversity and activity. Nat. Rev. Microbiol. 15, 591–605 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Husnik, F. et al. Bacterial and archaeal symbioses with protists. Curr. Biol. 31, R862–R877 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boamah, D. K., Zhou, G., Ensminger, A. W. & O’Connor, T. J. From many hosts, one accidental pathogen: the diverse protozoan hosts of Legionella. Front. Cell. Infect. Microbiol. 7, 477 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Graf, J. S. et al. Anaerobic endosymbiont generates energy for ciliate host by denitrification. Nature 591, 445–450 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pinhassi, J., DeLong, E. F., Béjà, O., González, J. M. & Pedrós-Alió, C. Marine bacterial and archaeal ion-pumping rhodopsins: genetic diversity, physiology, and ecology. Microbiol. Mol. Biol. Rev. 80, 929–954 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Brunet, T. et al. Light-regulated collective contractility in a multicellular choanoflagellate. Science 366, 326–334 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Schmitz-Esser, S. et al. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J. Bacteriol. 186, 683–691 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    George, E. E. et al. Highly reduced genomes of protist endosymbionts show evolutionary convergence. Curr. Biol. 30, 925–933.e3 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Deeg, C. M. et al. Chromulinavorax destructans, a pathogen of microzooplankton that provides a window into the enigmatic candidate phylum Dependentiae. PLoS Pathog. 15, e1007801–e1007801 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Major, P., Embley, T. M. & Williams, T. A. Phylogenetic diversity of NTT nucleotide transport proteins in free-living and parasitic bacteria and eukaryotes. Genome Biol. Evol. 9, 480–487 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Trentmann, O., Decker, C., Winkler, H. H. & Neuhaus, H. E. Charged amino-acid residues in transmembrane domains of the plastidic ATP/ADP transporter from Arabidopsis are important for transport efficiency, substrate specificity, and counter exchange properties. Eur. J. Biochem. 267, 4098–4105 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang, G., Meredith, T. C. & Kahne, D. On the essentiality of lipopolysaccharide to Gram-negative bacteria. Curr. Opin. Microbiol. 16, 779–785 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bertani, B. & Ruiz, N. Function and biogenesis of lipopolysaccharides. EcoSal Plus 8, ESP-0001–2018 (2018).Article 

    Google Scholar 
    Russell, D. G., Vanderven, B. C., Glennie, S., Mwandumba, H. & Heyderman, R. S. The macrophage marches on its phagosome: dynamic assays of phagosome function. Nat. Rev. Immunol. 9, 594–600 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sañudo-Wilhelmy, S. A., Gómez-Consarnau, L., Suffridge, C. & Webb, E. A. The role of B vitamins in marine biogeochemistry. Annu. Rev. Mar. Sci. 6, 339–367 (2014).Article 

    Google Scholar 
    Omsland, A. & Heinzen, R. A. Life on the outside: the rescue of Coxiella burnetii from its host cell. Annu. Rev. Microbiol. 65, 111–128 (2011).CAS 
    PubMed 
    Article 

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

    Google Scholar 
    Oliver, K. M., Campos, J., Moran, N. A. & Hunter, M. S. Population dynamics of defensive symbionts in aphids. Proc. Biol. Sci. 275, 293–299 (2008).PubMed 

    Google Scholar 
    Schulz, F. & Horn, M. Intranuclear bacteria: inside the cellular control center of eukaryotes. Trends Cell Biol. 25, 339–346 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hamann, E. et al. Environmental Breviatea harbour mutualistic Arcobacter epibionts. Nature 534, 254–258 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seah, B. K. B. et al. Sulfur-oxidizing symbionts without canonical genes for autotrophic CO2 fixation. mBio 10, e01112-19 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Salonen, I. S., Chronopoulou, P.-M., Bird, C., Reichart, G.-J. & Koho, K. A. Enrichment of intracellular sulphur cycle-associated bacteria in intertidal benthic foraminifera revealed by 16S and aprA gene analysis. Sci. Rep. 9, 11692 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vallesi, A. et al. A new species of the γ-Proteobacterium Francisella, F. adeliensis sp. nov., endocytobiont in an Antarctic marine ciliate and potential evolutionary forerunner of pathogenic species. Microb. Ecol. 77, 587–596 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tashyreva, D. et al. Life cycle, ultrastructure, and phylogeny of new diplonemids and their endosymbiotic bacteria. mBio 9, e02447-17 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Foster, R. A. & Zehr, J. P. Diversity, genomics, and distribution of phytoplankton-cyanobacterium single-cell symbiotic associations. Annu. Rev. Microbiol. 73, 435–456 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lin, Y.-C. et al. Distribution patterns and phylogeny of marine stramenopiles in the North Pacific Ocean. Appl. Environ. Microbiol. 78, 3387–3399 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kim, E. et al. Newly identified and diverse plastid-bearing branch on the eukaryotic tree of life. Proc. Natl Acad. Sci. USA 108, 1496–1500 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wylezich, C., Karpov, S. A., Mylnikov, A. P., Anderson, R. & Jürgens, K. Ecologically relevant choanoflagellates collected from hypoxic water masses of the Baltic Sea have untypical mitochondrial cristae. BMC Microbiol. 12, 271 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wilson, A. C. C. & Duncan, R. P. Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses. Proc. Natl Acad. Sci. USA 112, 10255–10261 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Douglas, A. E. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60, 17–34 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Newton, H. J. et al. Sel1 repeat protein LpnE is a Legionella pneumophila virulence determinant that influences vacuolar trafficking. Infect. Immun. 75, 5575–5585 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Boch, J., Bonas, U. & Lahaye, T. TAL effectors–pathogen strategies and plant resistance engineering. New Phytol. 204, 823–832 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Schmitz-Esser, S. et al. The genome of the amoeba symbiont ‘Candidatus Amoebophilus asiaticus’ reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J. Bacteriol. 192, 1045–1057 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Abby, S. S. et al. Identification of protein secretion systems in bacterial genomes. Sci. Rep. 6, 23080 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bratanis, E., Andersson, T., Lood, R. & Bukowska-Faniband, E. Biotechnological potential of Bdellovibrio and like organisms and their secreted enzymes. Front. Microbiol. https://doi.org/10.3389/fmicb.2020.00662 (2020).Rose, J., Caron, D., Sieracki, M. & Poulton, N. Counting heterotrophic nanoplanktonic protists in cultures and aquatic communities by flow cytometry. Aquat. Microb. Ecol. 34, 263–277 (2004).Article 

    Google Scholar 
    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108, 4516–4522 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Stoeck, T. et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19, 21–31 (2010).CAS 
    PubMed 
    Article 

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

    Google Scholar 
    Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17, 10–12 (2011).Article 

    Google Scholar 
    Callahan, B. J. et al. DADA2 : high resolution sample inference from amplicon data. Nat. Methods 13, 581–583 (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 
    Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nelson, M. C., Morrison, H. G., Benjamino, J., Grim, S. L. & Graf, J. Analysis, optimization and verification of illumina-generated 16S rRNA gene amplicon surveys. PLoS ONE 9, e94249 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Eren, A. M. et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3, e1319 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jain, C., Rodriguez-R, L. M., Phillippy, A. M., Konstantinidis, K. T. & Aluru, S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9, 5114 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Darling, A. E., Mau, B. & Perna, N. T. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5, e11147 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    Gao, F. & Zhang, C.-T. Ori-Finder: a web-based system for finding oriCs in unannotated bacterial genomes. BMC Bioinformatics 9, 79 (2008).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Delcher, A. L., Phillippy, A., Carlton, J. & Salzberg, S. L. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 30, 2478–2483 (2002).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Laslett, D. & Canback, B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 32, 11–16 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Huerta-Cepas, J. et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Mol. Biol. Evol. 34, 2115–2122 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Huerta-Cepas, J. et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, D309–D314 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Eddy, S. R. Profile hidden Markov models. Bioinformatics 14, 755–763 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Finn, R. D. et al. Pfam: the protein families database. Nucleic Acids Res. 42, D222–D230 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Arkin, A. P. et al. KBase: The United States Department of Energy Systems Biology Knowledgebase. Nat. Biotechnol. 36, 566 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Aziz, R. K. et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9, 75 (2008).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Karp, P. D. et al. Pathway Tools version 19.0 update: software for pathway/genome informatics and systems biology. Brief. Bioinform. 17, 877–890 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Käll, L., Krogh, A. & Sonnhammer, E. L. L. Advantages of combined transmembrane topology and signal peptide prediction–the Phobius web server. Nucleic Acids Res. 35, W429–W432 (2007).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Elbourne, L. D. H., Tetu, S. G., Hassan, K. A. & Paulsen, I. T. TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life. Nucleic Acids Res. 45, D320–D324 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sandoz, K. M. et al. Transcriptional profiling of Coxiella burnetii reveals extensive cell wall remodeling in the small cell variant developmental form. PLoS ONE 11, e0149957 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Rekha, S. et al. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc. Natl Acad. Sci. USA 100, 5455–5460 (2003).Article 
    CAS 

    Google Scholar 
    Bushnell, B. BBMap Short Read Aligner (Univ. California, Berkeley, 2016); http://sourceforge.net/projects/bbmapAnders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chen, I.-M. A. et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res. 47, D666–D677 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Delmont, T. O. et al. Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes. Nat. Microbiol. 3, 804–813 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Aylward, F. O. & Santoro, A. E. Heterotrophic Thaumarchaea with small genomes are widespread in the dark ocean. mSystems 5, e00415–20 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rodriguez-R, L. M. & Konstantinidis, K. T. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. Preprint at PeerJ https://doi.org/10.7287/peerj.preprints.1900v1 (2016).Konstantinidis, K. T. & Tiedje, J. M. Towards a genome-based taxonomy for prokaryotes. J. Bacteriol. 187, 6258–6264 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yoon, S.-H., Ha, S.-M., Lim, J., Kwon, S. & Chun, J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110, 1281–1286 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lee, I., Ouk Kim, Y., Park, S.-C. & Chun, J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol. 66, 1100–1103 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lee, M. D. GToTree: a user-friendly workflow for phylogenomics. Bioinformatics 35, 4162–4164 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Katoh, K. & Standley, D. M. MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Seemann, T. barrnap 0.9: Rapid Ribosomal RNA Prediction (2018); https://github.com/tseemann/barrnapFu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Warren, D. L., Geneva, A. J. & Lanfear, R. RWTY (R We There Yet): an R package for examining convergence of Bayesian phylogenetic analyses. Mol. Biol. Evol. 34, 1016–1020 (2017).CAS 
    PubMed 

    Google Scholar 
    Bi, D. et al. SecReT4: a web-based bacterial type IV secretion system resource. Nucleic Acids Res. 41, D660–D665 (2013).CAS 
    PubMed 
    Article 

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

    Google Scholar 
    Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Tully, B. J., Graham, E. D. & Heidelberg, J. F. The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Sci. Data 5, 170203 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Olson, D. K., Yoshizawa, S., Boeuf, D., Iwasaki, W. & DeLong, E. F. Proteorhodopsin variability and distribution in the North Pacific Subtropical Gyre. ISME J. 12, 1047–1060 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Philosof, A. & Béjà, O. Bacterial, archaeal and viral-like rhodopsins from the Red Sea. Environ. Microbiol. Rep. 5, 475–482 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boeuf, D., Audic, S., Brillet-Guéguen, L., Caron, C. & Jeanthon, C. MicRhoDE: a curated database for the analysis of microbial rhodopsin diversity and evolution. Database 2015, bav080 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Robert, X. & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320–W324 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Demir-Hilton, E. et al. Global distribution patterns of distinct clades of the photosynthetic picoeukaryote Ostreococcus. ISME J. 5, 1095–1107 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    Barbera, P. et al. EPA-ng: massively parallel evolutionary placement of genetic sequences. Syst. Biol. 68, 365–369 (2019).PubMed 
    Article 

    Google Scholar 
    Amaral-Zettler, L. A., McCliment, E. A., Ducklow, H. W. & Huse, S. M. A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE 4, e6372 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Needham, D. M. & Fuhrman, J. A. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat. Microbiol. 1, 16005 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Xia, L. C. et al. Extended local similarity analysis (eLSA) of microbial community and other time series data with replicates. BMC. Syst. Biol. 5, S15 (2011).
    Google Scholar 
    Choi, H. M. T. et al. Third-generation in situ hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust. Development 145, dev165753 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Schramm, A., Fuchs, B. M., Nielsen, J. L., Tonolla, M. & Stahl, D. A. Fluorescence in situ hybridization of 16S rRNA gene clones (Clone-FISH) for probe validation and screening of clone libraries. Environ. Microbiol. 4, 713–720 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Weiss, S. et al. Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J. 10, 1669–1681 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gloor, G. B., Macklaim, J. M., Pawlowsky-Glahn, V. & Egozcue, J. J. Microbiome datasets are compositional: and this is not optional. Front. Microbiol. 8, 2224 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Darling, A. C. E., Mau, B., Blattner, F. R. & Perna, N. T. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394–1403 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

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    The abundance and persistence of Caprinae populations

    Given Caprinae life history and plausible combinations of mean recruitment and adult female survivorship, we evaluated population persistence and estimated population MVP. The values describing adult female survivorship and recruitment, plus the variability we employed match values found in other populations of Caprinae. We do not pool data across different Caprinae populations or species. Our approach and results directly inform the conservation and management of many Caprinae, especially those for which the acquisition of demographic data remains beyond reach.Our work embodies the characteristics of a high-quality PVA: clear objectives, appropriate demographic data, model structure matching species life histories, stochasticity, examination of extinction probability, appropriate time interval, use of mean values and associated variability6. As with most ecological models, the quest for more data remains problematic, not debilitating, and is addressed by creatively and aptly using existing information to generate meaningful results3.Wildlife agencies generate lamb:adult female ratios from Caprinae surveys, recognizing that yearlings can be mistaken for adult females, causing miscounts. Excluding yearlings from the ratio’s denominator assumes that no miscounts are occurring, yet an unknown and inconsistent number of yearlings remain in the adult female category across survey events. For these reasons, surveyors of other species, like Dall’s sheep and caribou, pool counts of yearlings and adult females, generating lamb:“adult female-like” ratios instead15,23,24,25.Managers of Caprinae populations can follow these precedents and produce lamb:(adult female + yearling) ratios. Consistency would help standardize methods for building comparisons and meta-analyses across populations of Caprinae, while reducing variability across surveys due to differing techniques.Typically, metrics like elasticity (proportional) and sensitivity (additive) describe the influences of demographic parameters on population growth13,14,22,26. For Caprinae, when adult female survivorship is 0.90 and recruitment 0.30, the elasticity in survivorship and recruitment are 0.61 (90% CIs 0.40–0.75) and 0.24 (90% CIs 0.13–0.40) respectively (elasticity in young adult survivorship is 0.16 (90% CIs 0.12–0.21). For ungulates in general, the elasticity values for survival tend to be higher than those for recruitment27. Our results match this pattern, as the elasticity results indicate that a change in adult survival has a 2.5 times greater effect on λ than an equivalent change in recruitment. Relatedly, other theoretical work reports that demographic parameters with more temporal variability have lower elasticities, indicating less impact on population fitness (e.g.28,29).Our work centers on applications. Since most management actions affect these demographic parameters simultaneously, at issue is the practicality (e.g. feasibility and affordability) of management to increase these parameters, and understanding how such changes could impact λ. For example, imagine a population with mean recruitment of 0.30 and adult survival 0.85, with a biologist interested in increasing recruitment or adult female survival to acquire λ ≥ 1. The answer is to increase either value by 0.02 (Fig. 1, Supplementary Data S1). Similarly, one can set a λ target and determine the amount of recruitment and adult female survival necessary for acquiring it (Fig. 1, Supplementary Data S1).Minimum abundance targetA minimum population of 50 adult females meets the persistence criteria, given intermediate levels of recruitment and survival producing λ ~ 1 (Table 2). The risk of population collapse wanes as populations increase above the minimum threshold (Table 2; Fig. 1). For example, a population of ~ 100 adult females always meets persistence criteria (Table 2). Populations of adult females should be somewhat larger than 50 when modest declines (λ ~ 0.97) are suspected, providing a cushion to address the causes of decline, and mitigate further reductions.Translocation of 5 adult females during each of 5 years, or 10 in each of 3 years, requires a starting abundance of 70 adult females for the population to maintain the persistence criteria, never reach a lower confidence interval of 0, and for the population to return to the starting population size within 30 years. If managers mistakenly target a population having  More

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    Even a small nuclear war threatens food security

    Nuclear weapons obliterate targets. The soot ejected into the stratosphere spreads, changing global weather patterns. When weapons are especially high yielding, the resultant soot could trigger global famine.About 66 million years ago, roughly three-quarters of all species on Earth died when a 10–15-km-diameter asteroid travelling at 72,000 km h−1 struck at Chicxulub, Mexico1. Sulfates and soot lofted high in the atmosphere, cutting off sunlight. The Earth cooled, weather changed and primary productivity crashed. While the best-known victims of the asteroid impact were dinosaurs, the resultant food scarcity impacted the entire Earth; those not affected immediately by the impact eventually died from starvation. Any mechanism that can loft massive quantities of aerosols high into the atmosphere, such as massive volcanic explosions2 or nuclear wars3, can interfere with the weather globally and change world food security. More

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    Prevalent emergence of reciprocity among cross-feeding bacteria

    Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci. 2015;112:6449–54.CAS 
    Article 

    Google Scholar 
    D’Souza G, Shitut S, Preussger D, Yousif G, Waschina S, Kost C. Ecology and evolution of metabolic cross-feeding interactions in bacteria. Natural Product Reports. 2018;35:455–88.Article 

    Google Scholar 
    Garcia SL, Buck M, McMahon KD, Grossart H-P, Eiler A, Warnecke F. Auxotrophy and intrapopulation complementary in the ‘interactome’ of a cultivated freshwater model community. Mol Ecology. 2015;24:4449–59.CAS 
    Article 

    Google Scholar 
    Johnson WM, Alexander H, Bier RL, Miller DR, Muscarella ME, Pitz KJ, et al. Auxotrophic interactions: A stabilizing attribute of aquatic microbial communities? FEMS Microbiol Ecology. 2020;96:1–14.D’Souza G, Waschina S, Pande S, Bohl K, Kaleta C, Kost C. Less is more: Selective advantages can explain the prevalent loss of biosynthetic genes in bacteria. Evolution. 2014;68:2559–70.Article 

    Google Scholar 
    Oliveira NM, Niehus R, Foster KR. Evolutionary limits to cooperation in microbial communities. Proc Natl Acad Sci. 2014;111:17941–6.CAS 
    Article 

    Google Scholar 
    Pande S, Kost C. Bacterial unculturability and the formation of intercellular metabolic networks. Trends Microbiol. 2017;25:349–61.CAS 
    Article 

    Google Scholar 
    Douglas AE. The microbial exometabolome: ecological resource and architect of microbial communities. Philos Trans R Soc B: Biological Sci. 2020;375:20190250.CAS 
    Article 

    Google Scholar 
    Paczia N, Nilgen A, Lehmann T, Gätgens J, Wiechert W, Noack S. Extensive exometabolome analysis reveals extended overflow metabolism in various microorganisms. Microbial Cell Factories. 2012;11:122.CAS 
    Article 

    Google Scholar 
    Sokolovskaya OM, Shelton AN, Taga ME. Sharing vitamins: Cobamides unveil microbial interactions. Science. 2020;369:eaba0165.CAS 
    Article 

    Google Scholar 
    Zomorrodi AR, Segrè D. Genome-driven evolutionary game theory helps understand the rise of metabolic interdependencies in microbial communities. Nat Commun. 2017;8:1563.Article 

    Google Scholar 
    D’Souza G, Kost C. Experimental evolution of metabolic dependency in bacteria. PLoS Genetics. 2016;12:e1006364.Article 

    Google Scholar 
    Giri S, Oña L, Waschina S, Shitut S, Yousif G, Kaleta C, et al. Metabolic dissimilarity determines the establishment of cross-feeding interactions in bacteria. Curr Biology. 2021;31:5547–57.CAS 
    Article 

    Google Scholar 
    Jiang X, Zerfaß C, Feng S, Eichmann R, Asally M, Schäfer P, et al. Impact of spatial organization on a novel auxotrophic interaction among soil microbes. ISME J. 2018;12:1443–56.CAS 
    Article 

    Google Scholar 
    Konstantinidis D, Pereira F, Geissen E-M, Grkovska K, Kafkia E, Jouhten P, et al. Adaptive laboratory evolution of microbial co-cultures for improved metabolite secretion. Mol Syst Biology. 2021;17:e10189.CAS 
    Article 

    Google Scholar 
    Harcombe WR, Chacón JM, Adamowicz EM, Chubiz LM, Marx CJ. Evolution of bidirectional costly mutualism from byproduct consumption. Proc Natl Acad Sci. 2018;115:12000–4.CAS 
    Article 

    Google Scholar 
    Giri S, Waschina S, Kaleta C, Kost C. Defining division of labor in microbial communities. J Mol Biol. 2019;431:4712–31.CAS 
    Article 

    Google Scholar 
    Sanchez A, Gore J. Feedback between population and evolutionary dynamics determines the fate of social microbial populations. PLOS Biology. 2013;11:e1001547.CAS 
    Article 

    Google Scholar 
    Preussger D, Giri S, Muhsal LK, Oña L, Kost C. Reciprocal fitness feedbacks promote the evolution of mutualistic cooperation. Curr Biology. 2020;30:3580–3590.e7.CAS 
    Article 

    Google Scholar 
    McNally CP, Borenstein E. Metabolic model-based analysis of the emergence of bacterial cross-feeding via extensive gene loss. BMC Syst Biology. 2018;12:69.Article 

    Google Scholar 
    Estrela S, Morris JJ, Kerr B. Private benefits and metabolic conflicts shape the emergence of microbial interdependencies. Environ Microbiol. 2016;18:1415–27.Article 

    Google Scholar 
    Libby E, Hébert-Dufresne L, Hosseini S-R, Wagner A. Syntrophy emerges spontaneously in complex metabolic systems. PLOS Comput Biology. 2019;15:e1007169.Article 

    Google Scholar 
    Rabbers I, Gottstein W, Feist A, Teusink B, Bruggeman FJ, Bachmann H Selection for cell yield does not reduce overflow metabolism in E. coli. bioRxiv. 2021:2021.05.24.445453.Pacheco AR, Moel M, Segrè D. Costless metabolic secretions as drivers of interspecies interactions in microbial ecosystems. Nat Commun. 2019;10:103.Article 

    Google Scholar 
    Gude S, Pherribo GJ, Taga ME. Emergence of metabolite provisioning as a by-product of evolved biological functions. mSystems. 2020;5:e00259–20.CAS 
    Article 

    Google Scholar 
    Campbell K, Herrera-Dominguez L, Correia-Melo C, Zelezniak A, Ralser M. Biochemical principles enabling metabolic cooperativity and phenotypic heterogeneity at the single cell level. Current Opinion in. Syst Biology. 2018;8:97–108.
    Google Scholar 
    Morris JJ. Black Queen evolution: the role of leakiness in structuring microbial communities. Trends Genetics. 2015;31:475–82.CAS 
    Article 

    Google Scholar 
    van Tatenhove-Pel RJ, Rijavec T, Lapanje A, van Swam I, Zwering E, Hernandez-Valdes JA, et al. Microbial competition reduces metabolic interaction distances to the low µm-range. ISME J. 2021;15:688–701.Article 

    Google Scholar 
    Shitut S, Ahsendorf T, Pande S, Egbert M, Kost C. Nanotube-mediated cross-feeding couples the metabolism of interacting bacterial cells. Environ Microbiol. 2019;21:1306–20.CAS 
    Article 

    Google Scholar 
    Klee SM, Sinn JP, Finley M, Allman EL, Smith PB, Aimufua O, et al. Erwinia amylovora auxotrophic mutant exometabolomics and virulence on apples. Appl Environ Microbiol. 2019;85:e00935–19.CAS 
    Article 

    Google Scholar 
    Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8:15–25.CAS 
    Article 

    Google Scholar 
    Wienhausen G, Noriega-Ortega BE, Niggemann J, Dittmar T, Simon M The exometabolome of two model strains of the Roseobacter group: A marketplace of microbial metabolites. Front Microbiol. 2017;8.Pinu FR, Granucci N, Daniell J, Han T-L, Carneiro S, Rocha I, et al. Metabolite secretion in microorganisms: the theory of metabolic overflow put to the test. Metabolomics. 2018;14:43.Article 

    Google Scholar 
    Shiio I, Ôtsuka S-I, Takahashi M. Effect of biotin on the bacterial formation of glutamic acid: I. Glutamate formation and cellular permeability of amino acids. J Biochem. 1962;51:56–62.CAS 
    Article 

    Google Scholar 
    Konings WN, Poolman B, Driessen AJM. Can the excretion of metabolites by bacteria be manipulated? FEMS Microbiol Rev. 1992;8:93–108.CAS 
    Article 

    Google Scholar 
    Zampieri M, Hörl M, Hotz F, Müller NF, Sauer U. Regulatory mechanisms underlying coordination of amino acid and glucose catabolism in Escherichia coli. Nat Commun. 2019;10:3354.Article 

    Google Scholar 
    Kochanowski K, Okano H, Patsalo V, Williamson J, Sauer U, Hwa T. Global coordination of metabolic pathways in Escherichia coli by active and passive regulation. Mol Syst Biology. 2021;17:e10064.CAS 
    Article 

    Google Scholar 
    Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 1999;27:29–34.CAS 
    Article 

    Google Scholar 
    Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biology. 2006;2:2006.0008.Article 

    Google Scholar 
    Thomason LC, Costantino N, Court DL E. coli genome manipulation by P1 transduction. Curr Protocols Mol Biology. 2007;79:1.17.1-1.8.Pande S, Shitut S, Freund L, Westermann M, Bertels F, Colesie C, et al. Metabolic cross-feeding via intercellular nanotubes among bacteria. Nat Commun. 2015;6:6238.CAS 
    Article 

    Google Scholar 
    Oña L, Giri S, Avermann N, Kreienbaum M, Thormann KM, Kost C. Obligate cross-feeding expands the metabolic niche of bacteria. Nat Ecology Evolut. 2021;5:1224–32.Article 

    Google Scholar 
    Choi K-H, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, et al. A Tn7-based broad-range bacterial cloning and expression system. Nat Methods. 2005;2:443–8.CAS 
    Article 

    Google Scholar 
    Vanstockem M, Michiels K, Vanderleyden J, Van Gool AP. Transposon Mutagenesis of Azospirillum brasilense and Azospirillum lipoferum: Physical analysis of Tn5 and Tn5-Mob insertion mutants. Appl Environ Microbiology. 1987;53:410–5.CAS 
    Article 

    Google Scholar  More