More stories

  • in

    Microbial diversity in extreme environments

    1.Rothschild, L. J. & Mancinelli, R. L. Life in extreme environments. Nature 409, 1092–1101 (2001).CAS 
    PubMed 

    Google Scholar 
    2.Schmid, A. K., Allers, T. & DiRuggiero, J. Snapshot: microbial extremophiles. Cell 180, 818–818.e1 (2020).CAS 
    PubMed 

    Google Scholar 
    3.Denef, V. J., Mueller, R. S. & Banfield, J. F. AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J. 4, 599–610 (2010).PubMed 

    Google Scholar 
    4.Inskeep, W. P. et al. The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front. Microbiol. 4, 67 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    5.Oren, A. Halophilic microbial communities and their environments. Curr. Opin. Microbiol. 33, 119–124 (2015).CAS 

    Google Scholar 
    6.Reysenbach, A. L., Wickham, G. S. & Pace, N. R. Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park. Appl. Environ. Microbiol. 60, 2113–2119 (1994).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    7.Bond, P. L., Smriga, S. P. & Banfield, J. F. Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl. Environ. Microbiol. 66, 3842–3849 (2000).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    8.Huber, J. A. et al. Microbial population structures in the deep marine biosphere. Science 318, 97–100 (2007).CAS 
    PubMed 

    Google Scholar 
    9.Kuang, J. L. et al. Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J. 7, 1038–1050 (2013).CAS 
    PubMed 

    Google Scholar 
    10.Power, J. F. et al. Microbial biogeography of 925 geothermal springs in New Zealand. Nat. Commun. 9, 2876 (2018). Extensive sampling and high-throughput 16S rRNA gene sequencing have provided deeper insights into the patterns and ecological drivers of microbial communities inhabiting geothermal springs.PubMed 
    PubMed Central 

    Google Scholar 
    11.Podell, S. et al. Seasonal fluctuations in ionic concentrations drive microbial succession in a hypersaline lake community. ISME J. 8, 979–990 (2014).CAS 
    PubMed 

    Google Scholar 
    12.Chen, L. X. et al. Comparative metagenomic and metatranscriptomic analyses of microbial communities in acid mine drainage. ISME J. 9, 1579–1592 (2015).PubMed 

    Google Scholar 
    13.Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).CAS 
    PubMed 

    Google Scholar 
    14.Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523, 208–211 (2015).CAS 
    PubMed 

    Google Scholar 
    15.Castelle, C. J. et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 25, 690–701 (2015). The cultivation-independent reconstruction of the first complete genomes for members of the DPANN archaea allowed confident prediction of incomplete or absent pathways for these enigmatic organisms.CAS 
    PubMed 

    Google Scholar 
    16.Sharp, C. E. et al. Humboldt’s spa: microbial diversity is controlled by temperature in geothermal environments. ISME J. 8, 1166–1174 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    17.Hedlund, B. P. et al. Uncultivated thermophiles: current status and spotlight on ‘Aigarchaeota’. Curr. Opin. Microbiol. 25, 136–145 (2015).CAS 
    PubMed 

    Google Scholar 
    18.Hua, Z. S. et al. Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics. ISME J. 9, 1280–1294 (2015).CAS 
    PubMed 

    Google Scholar 
    19.Tyson, G. W. et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43 (2004). This is the first shotgun metagenomic sequencing study that enabled reconstruction of near-complete microbial genomes directly (without cultivation) from a natural community.CAS 
    PubMed 

    Google Scholar 
    20.Castelle, C. J. & Banfield, J. F. Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell 172, 1181–1197 (2018).CAS 
    PubMed 

    Google Scholar 
    21.Chen, L. X. et al. Metabolic versatility of small archaea Micrarchaeota and Parvarchaeota. ISME J. 12, 756–775 (2018).CAS 
    PubMed 

    Google Scholar 
    22.Baker, B. J. et al. Enigmatic, ultrasmall, uncultivated Archaea. Proc. Natl Acad. Sci. USA 107, 8806–8811 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    23.Narasingarao, P. et al. De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J. 6, 81–93 (2012).CAS 
    PubMed 

    Google Scholar 
    24.Brock, T. D. Life at high temperatures. Science 158, 1012–1019 (1967).CAS 
    PubMed 

    Google Scholar 
    25.Cole, J. K. et al. Sediment microbial communities in Great Boiling Spring are controlled by temperature and distinct from water communities. ISME J. 7, 718–729 (2013).CAS 
    PubMed 

    Google Scholar 
    26.Colman, D. R. et al. Ecological differentiation in planktonic and sediment-associated chemotrophic microbial populations in Yellowstone hot springs. FEMS Microbiol. Ecol. 92, fiw137 (2016).PubMed 

    Google Scholar 
    27.Ward, D. M. et al. 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345, 63–65 (1990).CAS 
    PubMed 

    Google Scholar 
    28.Miller, S. R. et al. Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Appl. Environ. Microbiol. 75, 4565–4572 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    29.Ward, L. et al. Microbial community dynamics in Inferno Crater Lake, a thermally fluctuating geothermal spring. ISME J. 11, 1158–1167 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    30.Barns, S. M., Fundyga, R. E., Jeffries, M. W. & Pace, N. R. Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc. Natl Acad. Sci. USA 91, 1609–1613 (1994).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Takai, K. & Yoshihiko, S. A molecular view of archaeal diversity in marine and terrestrial hot water environments. FEMS Microbiol. Ecol. 28, 177–188 (1999).CAS 

    Google Scholar 
    32.Elkins, J. G. et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl Acad. Sci. USA 105, 8102–8107 (2008).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    33.Dombrowski, N., Teske, A. P. & Baker, B. J. Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nat. Commun. 9, 4999 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    34.Nunoura, T. et al. Genetic and functional properties of uncultivated thermophilic crenarchaeotes from a subsurface gold mine as revealed by analysis of genome fragments. Environ. Microbiol. 7, 1967–1984 (2005).CAS 
    PubMed 

    Google Scholar 
    35.Nunoura, T. et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39, 3204–3223 (2011).CAS 
    PubMed 

    Google Scholar 
    36.Beam, J. P. et al. Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community. ISME J. 10, 210–224 (2016).CAS 
    PubMed 

    Google Scholar 
    37.Hua, Z. S. et al. Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota. Nat. Commun. 9, 2832 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    38.Takami, H. et al. A deeply branching thermophilic bacterium with an ancient acetyl-CoA pathway dominates a subsurface ecosystem. PLoS ONE 7, e30559 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Colman, D. R. et al. Novel, deep-branching heterotrophic bacterial populations recovered from thermal spring metagenomes. Front. Microbiol. 7, 304 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    40.Nobu, M. et al. Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics. ISME J. 10, 273–286 (2016).CAS 
    PubMed 

    Google Scholar 
    41.Hugenholtz, P., Pitulle, C., Hershberger, K. L. & Pace, N. R. Novel division level bacterial diversity in a Yellowstone hot spring. J. Bacteriol. 180, 366–376 (1998).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Orcutt, B. N., Sylvan, J. B., Knab, N. J. & Edwards, K. J. Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol. Mol. Biol. Rev. 75, 361–422 (2011).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    43.Eloe-Fadrosh, E. A. et al. Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs. Nat. Commun. 7, 10476 (2016). This is a good example of how analysis of the increasing wealth of metagenomic data collected from diverse environments may lead to the discovery of novel major lineages.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Kelley, D. S., Baross, J. A. & Delaney, J. R. Volcanoes, fluids, and life at Mid-Ocean Ridge spreading centers. Annu. Rev. Earth Planet. Sci. 30, 385–491 (2002).CAS 

    Google Scholar 
    45.Perner, M. et al. In situ chemistry and microbial community compositions in five deep-sea hydrothermal fluid samples from Irina II in the Logatchev field. Environ. Microbiol. 15, 1551–1560 (2013).CAS 
    PubMed 

    Google Scholar 
    46.Flores, G. E. et al. Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. Environ. Microbiol. 13, 2158–2171 (2011).CAS 
    PubMed 

    Google Scholar 
    47.Dick, G. J. et al. The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat. Rev. Microbiol. 17, 271–283 (2019).CAS 
    PubMed 

    Google Scholar 
    48.Campbell, B. J., Summers Engel, A., Porter, M. L. & Takai, K. The versatile ε-proteobacteria: key players in sulphidic habitats. Nat. Rev. Microbiol. 4, 458–468 (2006).CAS 
    PubMed 

    Google Scholar 
    49.Reysenbach, A. L., Longnecker, K. & Kirshtein, J. Novel bacterial and archaeal lineages from an in situ growth chamber deployed at a Mid-Atlantic Ridge hydrothermal vent. Appl. Environ. Microbiol. 66, 3798–3806 (2000).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    50.Takai, K., Komatsu, T., Inagaki, F. & Horikoshi, K. Distribution of archaea in a black smoker chimney structure. Appl. Environ. Microbiol. 67, 3618–3629 (2001).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    51.Schrenk, M. O., Kelley, D. S., Bolton, S. A. & Baross, J. A. Low archaeal diversity linked to subseafloor geochemical processes at the Lost City Hydrothermal Field, Mid-Atlantic Ridge. Environ. Microbiol. 6, 1086–1095 (2004).CAS 
    PubMed 

    Google Scholar 
    52.Brazelton, W. J., Schrenk, M. O., Kelley, D. S. & Baross, J. A. Methane- and sulfur-metabolizing microbial communities dominate the Lost City Hydrothermal Field ecosystem. Appl. Environ. Microbiol. 72, 6257–6270 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    53.Reveillaud, J. et al. Subseafloor microbial communities in hydrogen-rich vent fluids from hydrothermal systems along the Mid-Cayman Rise. Environ. Microbiol. 18, 1970–1987 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    54.Brazelton, W. J. et al. Archaea and bacteria with surprising micro-diversity show shifts in dominance over 1000-year time scales in hydrothermal chimneys. Proc. Natl Acad. Sci. USA 107, 1612–1617 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    55.Huber, H. et al. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63–67 (2002).CAS 
    PubMed 

    Google Scholar 
    56.Waters, E. et al. The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc. Natl Acad. Sci. USA 100, 12984–12988 (2003).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    57.Casanueva, A. et al. Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments. Extremophiles 12, 651–656 (2008).CAS 
    PubMed 

    Google Scholar 
    58.Wurch, L. et al. Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment. Nat. Commun. 7, 12115 (2016). This is an interesting study demonstrating that insights from genomic studies may help develop effective cultivation strategies for the isolation of novel microbial species.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    59.Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015). The discovery and genomic characterization of Lokiarchaeota have unveiled insights into eukaryogenesis.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    60.Seitz, K. W., Lazar, C. S., Hinrichs, K. U., Teske, A. P. & Baker, B. J. Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J. 10, 1696–1705 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    61.Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).CAS 
    PubMed 

    Google Scholar 
    62.Imachi, H. et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 577, 519–525 (2020). This study reports the isolation of the first member of the superphylum Asgard, confirming the existence of these archaea and their close phylogenetic relatedness to eukaryotes.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    63.Margesin, R. & Collins, T. Microbial ecology of the cryosphere (glacial and permafrost habitats): current knowledge. Appl. Microbiol. Biotechnol. 103, 2537–2549 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    64.Boetius, A., Anesio, A. M., Deming, J. W., Mikucki, J. A. & Rapp, J. Z. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat. Rev. Microbiol. 13, 677–690 (2015).CAS 
    PubMed 

    Google Scholar 
    65.Hoham, R. W. & Duval, B. in Snow Ecology (eds Jones, H. et al.) 168–228 (Cambridge Univ. Press, 2001).66.Edwards, A. et al. Coupled cryoconite ecosystem structure-function relationships are revealed by comparing bacterial communities in alpine and Arctic glaciers. FEMS Microbiol. Ecol. 89, 222–237 (2014).CAS 
    PubMed 

    Google Scholar 
    67.Jungblut, A. D., Lovejoy, C. & Vincent, W. F. Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J. 4, 191–202 (2010).CAS 
    PubMed 

    Google Scholar 
    68.Franzetti, A. et al. Temporal variability of bacterial communities in cryoconite on an alpine glacier. Environ. Microbiol. Rep. 9, 71–78 (2017).CAS 
    PubMed 

    Google Scholar 
    69.Anesio, A. M., Hodson, A. J., Fritz, A., Psenner, R. & Sattler, B. High microbial activity on glaciers: importance to the global carbon cycle. Glob. Chang. Biol. 15, 955–960 (2009).
    Google Scholar 
    70.Christner, B. C. et al. A microbial ecosystem beneath the West Antarctic ice sheet. Nature 512, 310–313 (2014).CAS 
    PubMed 

    Google Scholar 
    71.Hultman, J. et al. Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521, 208–212 (2015).CAS 
    PubMed 

    Google Scholar 
    72.Mackelprang, R. et al. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480, 368–371 (2011).CAS 
    PubMed 

    Google Scholar 
    73.Frey, B. et al. Microbial diversity in European alpine permafrost and active layers. FEMS Microbiol. Ecol. 92, fiw018 (2016).PubMed 

    Google Scholar 
    74.Fernández, A. B. et al. Prokaryotic taxonomic and metabolic diversity of an intermediate salinity hypersaline habitat assessed by metagenomics. FEMS Microbiol. Ecol. 88, 623–635 (2014).PubMed 

    Google Scholar 
    75.Ventosa, A. et al. Microbial diversity of hypersaline environments: a metagenomic approach. Curr. Opin. Microbiol. 25, 80–87 (2015).CAS 
    PubMed 

    Google Scholar 
    76.Emerson, J. B. et al. Virus-host and CRISPR dynamics in Archaea-dominated hypersaline Lake Tyrrell, Victoria, Australia. Archaea 2013, 370871 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    77.Ley, R. E. et al. Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl. Environ. Microbiol. 72, 3685–3695 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    78.Harris, J. K. et al. Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat. ISME J. 7, 50–60 (2013). This study retrieves an unprecedented number of nearly full length 16S rRNA gene sequences from the microbial mats of the Guerrero Negro hypersaline environment, Mexico, demonstrating them to be among the most diverse, complex and novel microbial ecosystems known.PubMed 

    Google Scholar 
    79.Vavourakis, C. D. et al. Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Front. Microbiol. 7, 211 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    80.Hamm, J. N. et al. Unexpected host dependency of Antarctic Nanohaloarchaeota. Proc. Natl Acad. Sci. USA. 116, 14661–14670 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    81.Nigro, L. M., Hyde, A. S., MacGregor, B. J. & Teske, A. Phylogeography, salinity adaptations and metabolic potential of the candidate division KB1 bacteria based on a partial single cell genome. Front. Microbiol. 7, 1266 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    82.Vavourakis, C. D. et al. A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments. Microbiome 6, 168 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    83.Edwards, K. J., Becker, K. & Colwell, F. The deep, dark energy biosphere: intraterrestrial life on Earth. Annu. Rev. Earth Planet. Sci. 40, 551–568 (2012).CAS 

    Google Scholar 
    84.Parkes, R. J. et al. A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere: geosphere interactions. Mar. Geol. 352, 409–425 (2014).CAS 

    Google Scholar 
    85.Starnawski, P. et al. Microbial community assembly and evolution in subseafloor sediment. Proc. Natl Acad. Sci. USA 114, 2940–2945 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    86.Ciobanu, M. C. et al. Microorganisms persist at record depths in the subseafloor of the Canterbury Basin. ISME J. 8, 1370–1380 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    87.Inagaki, F. et al. Exploring deep microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor. Science 349, 420–424 (2015).CAS 
    PubMed 

    Google Scholar 
    88.D’Hondt, S., Pockalny, R., Fulfer, V. M. & Spivack, A. J. Subseafloor life and its biogeochemical impacts. Nat. Commun. 10, 3519 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    89.Petro, C., Starnawski, P., Schramm, A. & Kjeldsen, K. U. Microbial community assembly in marine sediments. Aquat. Microb. Ecol. 79, 177–195 (2017).
    Google Scholar 
    90.Teske, A. & Sørensen, K. B. Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J. 2, 3–18 (2008).CAS 
    PubMed 

    Google Scholar 
    91.Orsi, W. D. Ecology and evolution of seafloor and subseafloor microbial communities. Nat. Rev. Microbiol. 16, 671–683 (2018).CAS 
    PubMed 

    Google Scholar 
    92.Sørensen, K. B. & Teske, A. Stratified communities of active Archaea in deep marine subsurface sediments. Appl. Environ. Microbiol. 72, 4596–4603 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    93.Walsh, E. A. et al. Relationship of bacterial richness to organic degradation rate and sediment age in subseafloor sediment. Appl. Environ. Microbiol. 82, 4994–4999 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    94.Petro, C. et al. Marine deep biosphere microbial communities assemble in near-surface sediments in Aarhus Bay. Front. Microbiol. 10, 758 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    95.Jorgensen, S. L. et al. Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge. Proc. Natl Acad. Sci. USA 109, E2846–E2855 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    96.Edwards, K. J., Wheat, C. G. & Sylvan, J. B. Under the sea: microbial life in volcanic oceanic crust. Nat. Rev. Microbiol. 9, 703–712 (2011).CAS 
    PubMed 

    Google Scholar 
    97.Li, J. et al. Recycling and metabolic flexibility dictate life in the lower oceanic crust. Nature 579, 250–255 (2020). This is a multiple-approach exploration to provide the first insights into the ultralow-biomass microbial assemblages inhabiting the lithified lower oceanic crust.CAS 
    PubMed 

    Google Scholar 
    98.Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    99.Nyyssönen, M. et al. Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield. ISME J. 8, 126–138 (2014).PubMed 

    Google Scholar 
    100.Lin, X., Kennedy, D., Fredrickson, J., Bjornstad, B. & Konopka, A. Vertical stratification of subsurface microbial community composition across geological formations at the Hanford Site. Environ. Microbiol. 14, 414–425 (2012).CAS 
    PubMed 

    Google Scholar 
    101.Osburn, M. R. et al. Chemolithotrophy in the continental deep subsurface: Sanford Underground Research Facility (SURF), USA. Front. Microbiol. 5, 610 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    102.Magnabosco, C. et al. The biomass and biodiversity of the continental subsurface. Nat. Geosci. 11, 707–717 (2018).CAS 

    Google Scholar 
    103.Navarro-Noya, Y. E. et al. Pyrosequencing analysis of the bacterial community in drinking water wells. Microb. Ecol. 66, 19–29 (2013).PubMed 

    Google Scholar 
    104.Wrighton, K. C. et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661–1665 (2012).CAS 
    PubMed 

    Google Scholar 
    105.Bagnoud, A. et al. Reconstructing a hydrogen driven microbial metabolic network in Opalinus Clay rock. Nat. Commun. 7, 12770 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    106.Magnabosco, C. et al. A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust. ISME J. 10, 730–741 (2016).CAS 
    PubMed 

    Google Scholar 
    107.Hernsdorf, A. W. et al. Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments. ISME J. 11, 1915–1929 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    108.Anantharaman, K. et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat. Commun. 7, 13219 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    109.Kantor, R. S. et al. Small genomes and sparse metabolisms of sediment-associated bacteria from four candidate phyla. mBio 4, e00708–e00713 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    110.Wrighton, K. C. et al. Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer. ISME J. 8, 1452–1463 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    111.Hallberg, K. B., Coupland, K., Kimura, S. & Johnson, D. B. Macroscopic streamer growths in acidic, metal-rich mine waters in north Wales consist of novel and remarkably simple bacterial communities. Appl. Environ. Microbiol. 72, 2022–2030 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    112.Belnap, C. P. et al. Quantitative proteomic analyses of the response of acidophilic microbial communities to different pH conditions. ISME J. 5, 1152–1161 (2011).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    113.Edwards, K. J. et al. Seasonal variations in microbial populations and environmental conditions in an extreme acid mine drainage environment. Appl. Environ. Microbiol. 65, 3627–3632 (1999).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    114.Liu, J. et al. Correlating microbial diversity patterns with geochemistry in an extreme and heterogeneous environment of mine tailings. Appl. Environ. Microbiol. 80, 3677–3686 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    115.Golyshina, O. V. et al. ‘ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ. Nat. Commun. 8, 60 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    116.Antony, C. P. et al. Microbiology of Lonar Lake and other soda lakes. ISME J. 7, 468–476 (2013).PubMed 

    Google Scholar 
    117.Sorokin, D. Y. et al. Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18, 791–809 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    118.Reynolds, J. F. et al. Global desertification: building a science for dryland development. Science 316, 847–851 (2007).CAS 
    PubMed 

    Google Scholar 
    119.Maestre, F. T. et al. Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc. Natl Acad. Sci. USA. 112, 15684–15689 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    120.Makhalanyane, T. P. et al. Microbial ecology of hot desert edaphic systems. FEMS Microbiol. Rev. 39, 203–221 (2015).CAS 
    PubMed 

    Google Scholar 
    121.Reinthaler, T. et al. Prokaryotic respiration and production in the meso- and bathypelagic realm of the eastern and western North Atlantic basin. Limnol. Oceanogr. 51, 1262–1273 (2006).CAS 

    Google Scholar 
    122.Hewson, I., Steele, J. A., Capone, D. G. & Fuhrman, J. A. Remarkable heterogeneity in meso- and bathypelagic bacterioplankton assemblage composition. Limnol. Oceanogr. 51, 1274–1283 (2006).
    Google Scholar 
    123.DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311, 496–503 (2006).CAS 
    PubMed 

    Google Scholar 
    124.Pham, V. D., Konstantinidis, K. T., Palden, T. & DeLong, E. F. Phylogenetic analyses of ribosomal DNA-containing bacterioplankton genome fragments from a 4000 m vertical profile in the North Pacific Subtropical Gyre. Environ. Microbiol. 10, 2313–2330 (2008).CAS 
    PubMed 

    Google Scholar 
    125.Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001).CAS 
    PubMed 

    Google Scholar 
    126.Ziegler, S. et al. Oxygen-dependent niche formation of a pyrite-dependent acidophilic consortium built by archaea and bacteria. ISME J. 7, 1725–1737 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    127.Méndez-García, C. et al. Microbial stratification in low pH oxic and suboxic macroscopic growths along an acid mine drainage. ISME J. 8, 1259–1274 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    128.Klatt, C. G. et al. Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting a microbial mat in a geothermal spring. ISME J. 7, 1775–1789 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    129.Klatt, C. G. et al. Community structure and function of high-temperature chlorophototrophic microbial mats inhabiting diverse geothermal environments. Front. Microbiol. 4, 106 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    130.Inskeep, W. P. et al. Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PLoS ONE 5, e9773 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    131.Swingley, W. D. et al. Coordinating environmental genomics and geochemistry reveals metabolic transitions in a hot spring ecosystem. PLoS ONE 7, e38108 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    132.Liu, Z. et al. Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat. ISME J. 5, 1279–1290 (2011).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    133.Woodcroft, B. J. et al. Genome-centric view of carbon processing in thawing permafrost. Nature 560, 49–54 (2018).CAS 
    PubMed 

    Google Scholar 
    134.Ghai, R. et al. New abundant microbial groups in aquatic hypersaline environments. Sci. Rep. 1, 135 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    135.Uritskiy, G. et al. Halophilic microbial community compositional shift after a rare rainfall in the Atacama Desert. ISME J. 13, 2737–2749 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    136.Uritskiy, G. et al. Cellular life from the three domains and viruses are transcriptionally active in a hypersaline desert community. Environ. Microbiol. 23, 3401–3417 (2021).CAS 
    PubMed 

    Google Scholar 
    137.Herrmann, M. et al. Large fractions of CO2-fixing microorganisms in pristine limestone aquifers appear to be involved in the oxidation of reduced sulfur and nitrogen compounds. Appl. Environ. Microbiol. 81, 2384–2394 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    138.Probst, A. J. et al. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat. Microbiol. 3, 328–336 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    139.Mueller, R. S. et al. Ecological distribution and population physiology defined by proteomics in a natural microbial community. Mol. Syst. Biol. 6, 374 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    140.Chen, L. X. et al. Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ. Microbiol. 15, 2431–2444 (2013).CAS 
    PubMed 

    Google Scholar 
    141.Mueller, R. S. et al. Proteome changes in the initial bacterial colonist during ecological succession in an acid mine drainage biofilm community. Environ. Microbiol. 13, 2279–2292 (2011).CAS 
    PubMed 

    Google Scholar 
    142.Mosier, A. C. et al. Elevated temperature alters proteomic responses of individual organisms within a biofilm community. ISME J. 9, 180–194 (2015).CAS 
    PubMed 

    Google Scholar 
    143.Papke, R. T., Koenig, J. E., Rodriguez-Valera, F. & Doolittle, W. F. Frequent recombination in a saltern population of Halorubrum. Science 306, 1928–1929 (2004).CAS 
    PubMed 

    Google Scholar 
    144.Whitaker, R. J., Grogan, D. W. & Taylor, J. W. Recombination shapes the natural population structure of the hyperthermophilic archaeon Sulfolobus islandicus. Mol. Biol. Evol. 22, 2354–2361 (2005).CAS 
    PubMed 

    Google Scholar 
    145.Naor, A., Lapierre, P., Mevarech, M., Papke, R. T. & Gophna, U. Low species barriers in halophilic archaea and the formation of recombinant hybrids. Curr. Biol. 22, 1444–1448 (2012).CAS 
    PubMed 

    Google Scholar 
    146.Reno, M. L., Held, N. L., Fields, C. J., Burke, P. V. & Whitaker, R. J. Biogeography of the Sulfolobus islandicus pan-genome. Proc. Natl Acad. Sci. USA 106, 8605–8610 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    147.Mongodin, E. F. et al. The genome of Salinibacter Ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc. Natl Acad. Sci. USA 102, 18147–18152 (2005).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    148.Nelson-Sathi, S. et al. Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc. Natl Acad. Sci. USA 109, 20537–20542 (2012). Comparative genomics provides evidence that massive amounts of gene influx from bacterial sources may have led to the drastic change in lifestyle in the extremely salt tolerant Haloarchaea.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    149.Wolf, Y. I., Makarova, K. S., Yutin, N. & Koonin, E. V. Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol. Direct 7, 46 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    150.Nelson-Sathi, S. et al. Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 517, 77–80 (2015).CAS 
    PubMed 

    Google Scholar 
    151.Simmons, S. L. et al. Population genomic analysis of strain variation in Leptospirillum group II bacteria involved in acid mine drainage formation. PLoS Biol. 6, e177 (2008).PubMed 
    PubMed Central 

    Google Scholar 
    152.Lo, I. et al. Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446, 537–541 (2007).CAS 
    PubMed 

    Google Scholar 
    153.Denef, V. J. et al. Proteomics-inferred genome typing (PIGT) demonstrates inter-population recombination as a strategy for environmental adaptation. Environ. Microbiol. 11, 313–325 (2009).CAS 
    PubMed 

    Google Scholar 
    154.Denef, V. J. et al. Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc. Natl Acad. Sci. USA 107, 2383–2390 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    155.Denef, V. J. & Banfield, J. F. In situ evolutionary rate measurements show ecological success of recently emerged bacterial hybrids. Science 336, 462–466 (2012). This study provides a time-series population metagenomic analysis of microorganisms in exceptionally low diversity AMD biofilms, allowing for the first time measurement of evolutionary rates for wild populations.CAS 
    PubMed 

    Google Scholar 
    156.Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245–252 (2008).CAS 
    PubMed 

    Google Scholar 
    157.Kelly, S., Wickstead, B. & Gull, K. Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. Proc. Biol. Sci. 278, 1009–1018 (2011).CAS 
    PubMed 

    Google Scholar 
    158.Sorokin, D. Y. et al. Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis. Nat. Microbiol. 2, 17081 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    159.Baker, B. J. et al. Diversity, ecology and evolution of archaea. Nat. Microbiol. 5, 887–900 (2020).CAS 
    PubMed 

    Google Scholar 
    160.Paul, B. G. et al. Targeted diversity generation by intraterrestrial archaea and archaeal viruses. Nat. Commun. 6, 6585 (2015).CAS 
    PubMed 

    Google Scholar 
    161.Paul, B. G. et al. Retroelement-guided protein diversification abounds in vast lineages of Bacteria and Archaea. Nat. Microbiol. 2, 17045 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    162.Burstein, D. et al. New CRISPR-Cas systems from uncultivated microbes. Nature 542, 237–241 (2017).CAS 
    PubMed 

    Google Scholar 
    163.Anderson, R. E. et al. Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents. Nat. Commun. 8, 1114 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    164.Brazelton, W. J. & Baross, J. A. Abundant transposases encoded by the metagenome of a hydrothermal chimney biofilm. ISME J. 3, 1420–1424 (2009).CAS 
    PubMed 

    Google Scholar 
    165.Jansson, J. K. & Taş, N. The microbial ecology of permafrost. Nat. Rev. Microbiol. 12, 414–425 (2014).CAS 
    PubMed 

    Google Scholar 
    166.Kuang, J. et al. Predicting taxonomic and functional structure of microbial communities in acid mine drainage. ISME J. 10, 1527–1539 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    167.Clark, D. R. et al. Biogeography at the limits of life: do extremophilic microbial communities show biogeographical regionalization? Glob. Ecol. Biogeogr. 26, 1435–1446 (2017).
    Google Scholar 
    168.Atanasova, N. S., Roine, E., Oren, A., Bamford, D. H. & Oksanen, H. M. Global network of specific virus-host interactions in hypersaline environments. Environ. Microbiol. 14, 426–440 (2012).CAS 
    PubMed 

    Google Scholar 
    169.Wilkins, D. et al. Key microbial drivers in Antarctic aquatic environments. FEMS Microbiol. Rev. 37, 303–335 (2013).CAS 
    PubMed 

    Google Scholar 
    170.Cavicchioli, R. Microbial ecology of Antarctic aquatic systems. Nat. Rev. Microbiol. 13, 691–706 (2015).CAS 
    PubMed 

    Google Scholar 
    171.López-Bueno, A. et al. High diversity of the viral community from an Antarctic lake. Science 326, 858–861 (2009).PubMed 

    Google Scholar 
    172.Aguirre de Cárcer, D., López-Bueno, A., Pearce, D. A. & Alcamí, A. Biodiversity and distribution of polar freshwater DNA viruses. Sci. Adv. 1, e1400127 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    173.Yau, S. et al. Virophage control of Antarctic algal host–virus dynamics. Proc. Natl Acad. Sci. USA 108, 6163–6168 (2011). This is the first study to reveal the important ecological roles of virophages and their regulation of host–virus interactions.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    174.Al-Shayeb, B. et al. Clades of huge phages from across Earth’s ecosystems. Nature 578, 425–431 (2020). Analysis of massive metagenomic datasets revealed clades of huge phages from diverse habitats, including extreme environments.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    175.Tschitschko, B. et al. Antarctic archaea-virus interactions: metaproteome-led analysis of invasion, evasion and adaptation. ISME J. 9, 2094–2107 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    176.Mosier, A. C. et al. Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage. Front. Microbiol. 7, 238 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    177.Quemener, M. et al. Meta-omics highlights the diversity, activity and adaptations of fungi in deep oceanic crust. Environ. Microbiol. 22, 3950–3967 (2020).CAS 
    PubMed 

    Google Scholar 
    178.Fredrickson, J. K. Ecological communities by design. Science 348, 1425–1427 (2015).CAS 
    PubMed 

    Google Scholar 
    179.Fuhrman, J. A. et al. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc. Natl Acad. Sci. USA 103, 13104–13109 (2006).CAS 
    PubMed 
    PubMed Central 

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

    Google Scholar 
    181.Lozupone, C. A. & Knight, R. Global patterns in bacterial diversity. Proc. Natl Acad. Sci. USA 104, 11436–11440 (2007).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    182.Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl Acad. Sci. USA 103, 626–631 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    183.López-Pérez, M., Haro-Moreno, J. M., Coutinho, F. H., Martinez-Garcia, M. & Rodriguez-Valera, F. The evolutionary success of the marine bacterium SAR11 analyzed through a metagenomic perspective. mSystems 5, e00605-20 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    184.Altshuler, I., Goordial, J. & Whyte, L. G. in Psychrophiles: From Biodiversity to Biotechnology (ed. Margesin, R.) 153–180 (Springer International Publishing, 2017).185.Huang, L. N., Kuang, J. L. & Shu, W. S. Microbial ecology and evolution in the acid mine drainage model system. Trends Microbiol. 24, 581–593 (2016).CAS 
    PubMed 

    Google Scholar 
    186.Klatt, C. G. et al. Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential. ISME J. 5, 1262–1278 (2011).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    187.Menzel, P. et al. Comparative metagenomics of eight geographically remote terrestrial hot springs. Microb. Ecol. 70, 411–424 (2015).PubMed 

    Google Scholar 
    188.Stokke, R. et al. Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm. Environ. Microbiol. 17, 4063–4077 (2015).CAS 
    PubMed 

    Google Scholar 
    189.Zeng, Y. et al. Potential rhodopsin- and bacteriochlorophyll-based dual phototrophy in a High Arctic glacier. mBio 11, e02641–20 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    190.Simon, C., Wiezer, A., Strittmatter, A. W. & Daniel, R. Phylogenetic diversity and metabolic potential revealed in a glacier ice metagenome. Appl. Environ. Microbiol. 75, 7519–7526 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    191.Lipson, D. A. et al. Metagenomic insights into anaerobic metabolism along an Arctic peat soil profile. PLoS ONE 8, e64659 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    192.Podell, S. et al. Assembly-driven community genomics of a hypersaline microbial ecosystem. PLoS ONE 8, e61692 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    193.DeMaere, M. Z. et al. High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake. Proc. Natl Acad. Sci. USA. 110, 16939–16944 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    194.Smith, A. R. et al. Carbon fixation and energy metabolisms of a subseafloor olivine biofilm. ISME J. 13, 1737–1749 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    195.Zhao, R. et al. Geochemical transition zone powering microbial growth in subsurface sediments. Proc. Natl Acad. Sci. USA. 117, 32617–32626 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    196.Luo, Z. H. et al. Diversity and genomic characterization of a novel Parvarchaeota family in acid mine drainage sediments. Front. Microbiol. 11, 612257 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    197.Lewin, A., Wentzel, A. & Valla, S. Metagenomics of microbial life in extreme temperature environments. Curr. Opin. Biotechnol. 24, 516–525 (2013).CAS 
    PubMed 

    Google Scholar 
    198.Schlesinger, M. J. Heat-shock proteins. J. Biol. Chem. 265, 12111–12114 (1990).CAS 
    PubMed 

    Google Scholar 
    199.D’Amico, S., Collins, T., Marx, J.-C., Feller, G. & Gerday, C. Psychrophilic microorganisms: challenges for life. EMBO Rep. 7, 385–389 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    200.Bakermans, C., Bergholz, P. W., Ayala-del-Río, H. & Tiedje, J. in Permafrost Soils (ed. Margesin, R.) 159–168 (Springer, 2009).201.Gunde-Cimerman, N., Plemenitaš, A. & Oren, A. Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiol. Rev. 42, 353–375 (2018).CAS 
    PubMed 

    Google Scholar 
    202.Baker-Austin, C. & Dopson, M. Life in acid: pH homeostasis in acidophiles. Trends Microbiol. 15, 165–171 (2007).CAS 
    PubMed 

    Google Scholar 
    203.Dopson, M., Baker-Austin, C., Koppineedi, P. R. & Bond, P. L. Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic micro-organisms. Microbiology 149, 1959–1970 (2003).CAS 
    PubMed 

    Google Scholar 
    204.Dopson, M., Ossandon, F. J., Lövgren, L. & Holmes, D. S. Metal resistance or tolerance? Acidophiles confront high metal loads via both abiotic and biotic mechanisms. Front. Microbiol. 5, 157 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    205.Allen, E. E. & Banfield, J. F. Community genomics in microbial ecology and evolution. Nat. Rev. Microbiol. 3, 489–498 (2005).CAS 
    PubMed 

    Google Scholar 
    206.Sakowski, E. et al. Current state of and future opportunities for prediction in microbiome research: report from the Mid-Atlantic Microbiome Meet-up in Baltimore on 9 January 2019. mSystems 4, e00392–19 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    207.Lima-Mendez, G. et al. Determinants of community structure in the global plankton interactome. Science 348, 1262073 (2015).PubMed 

    Google Scholar  More

  • in

    Water column structure influences long-distance latitudinal migration patterns and habitat use of bumphead sunfish Mola alexandrini in the Pacific Ocean

    1.Sims, D. W., Queiroz, N., Doyle, T. K., Houghton, J. D. R. & Hays, G. C. Satellite tracking of the world’s largest bony fish, the ocean sunfish (Mola mola L.) in the North East Atlantic. J. Exp. Mar. Biol. Ecol. 370, 127–133 (2009a)2.Sims, D. W., Queiroz, N., Humphries, N. E., Lima, F. P. & Hays, G. C. Long-term GPS tracking of ocean sunfish Mola mola offers a new direction in fish monitoring. PLoS ONE 4, e7351 (2009b).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    3.Dewar, H. et al. Satellite tracking the world’s largest jelly predator, the ocean sunfish, Mola mola, in the Western Pacific. J. Exp. Mar. Biol. Ecol. 393, 32–42 (2010).Article 

    Google Scholar 
    4.Thys, T. M. et al. Ecology of the ocean sunfish, Mola mola, in the southern California current system. J. Exp. Mar. Biol. Ecol. 471, 64–76 (2015).Article 

    Google Scholar 
    5.Sousa, L. L., Queiroz, N., Mucientes, G., Humphries, N. E. & Sims, D. W. Environmental influence on the seasonal movements of satellite-tracked ocean sunfish Mola mola in the north-east Atlantic. Anim. Biotelemetry 4, 7 (2016a).Article 

    Google Scholar 
    6.Sousa, L. L. et al. Integrated monitoring of Mola mola behaviour in space and time. PLoS ONE 11, e0160404 (2016b).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    7.Chang, C. T. et al. Horizontal and vertical movement patterns of sunfish off eastern Taiwan. Deep-Sea Res. Part II Top. Stud. Oceanogr. 175, 104683 (2020).8.Sawai, E., Yamanoue, Y., Yoshita, Y., Sakai, Y. & Hashimoto, H. Seasonal occurrence patterns of Mola sunfishes (Mola spp. A and B; Molidae) in waters off the Sanriku region, eastern Japan. Japan. J. Ichthyol. 58, 181–187 (2011).
    Google Scholar 
    9.Thys, T. M., Ryan, J. P., Weng, K. C., Erdmann, M. & Tresnati, J. Tracking a marine ecotourism star: Movements of the short ocean sunfish Mola ramsayi in Nusa Penida, Bali, Indonesia. J. Mar. Biol. 2016, 8750193 (2016).Article 

    Google Scholar 
    10.Thys, T. M., Hearn, A. R., Weng, K. C., Ryan, J. P. & Peñaherrera-Palma, C. Satellite tracking and site fidelity of short ocean sunfish, Mola ramsayi, in the Galapagos Islands. J. Mar. Biol. 2017, 7097965 (2017).Article 

    Google Scholar 
    11.Aspillaga, E. et al. Thermal stratification drives movement of a coastal apex predator. Sci. Rep. 7, 526 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    12.Gaube, P. et al. Mesoscale eddies influence the movements of mature female white sharks in the Gulf Stream and Sargasso Sea. Sci. Rep. 8, 7363 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    13.Nakamura, I., Goto, Y. & Sato, K. Ocean sunfish rewarm at the surface at the surface after deep excursion to forage for siphonophores. J. Anim. Ecol. 84, 590–603 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Tolotti, M. et al. Fine-scale vertical movements of oceanic whitetip sharks (Carcharhinus longimanus). Fish. Bull. 115, 380–395 (2017).Article 

    Google Scholar 
    15.Musyl, M. K. et al. Postrelease survival, vertical and horizontal movements, and thermal habitats of five species of pelagic sharks in the central Pacific Ocean. Fish. Bull. 109, 341–368 (2011).
    Google Scholar 
    16.Furukawa, S. et al. Vertical movements of Pacific bluefin tuna (Thunnus orientalis) and dolphinfish (Coryphaena hippurus) relative to the thermocline in the northern East China Sea. Fish. Res. 149, 86–91 (2014).Article 

    Google Scholar 
    17.Gaube, P. et al. The use of mesoscale eddies by juvenile loggerhead sea turtles (Caretta caretta) in the southwestern Atlantic. PloS ONE 12, e0172839 (2017).18.Braun, C. D., Gaube, P., Sinclair-Taylor, T. H., Skomal, G. B. & Thorrold, S. R. Mesoscale eddies release pelagic sharks from thermal constraints to foraging in the ocean twilight zone. PNAS 116, 17187–17192 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Sawai, E., Yamanoue, Y., Nyegaard, M. & Sakai, Y. Redescription of the bump-head sunfish Mola alexandrini (Ranzani 1839), senior synonym of Mola ramsayi (Giglioli 1883), with designation of a neotype for Mola mola (Linnaeus 1758) (Tetraodontiformes: Molidae). Ichthyol. Res. 65, 142–160 (2018).Article 

    Google Scholar 
    20.Sawai, E. & Yamada, M. Bump-head sunfish Mola alexandrini photographed in the north-west Pacific Ocean mesopelagic zone. J. Fish Biol. 96, 278–280 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Kiyofuji, H. et al. Northward migration dynamics of skipjack tuna (Katsuwonus pelamis) associated with the lower thermal limit in the western Pacific Ocean. Progr. Oceanogr. 175, 55–67 (2019).ADS 
    Article 

    Google Scholar 
    22.Fujioka, K. et al. Spatial and temporal variability in the trans-Pacific migration of Pacific bluefin tuna (Thunnus orientalis) revealed by archival tags. Progr. Oceanogr. 162, 52–65 (2018).23.Kobari, T. et al. Variability in taxonomic composition, standing stock, and productivity of the plankton community in the Kuroshio and its neighboring waters in Kuroshio Current: Physical, Biogeochemical, and Ecosystem Dynamics (ed. Nagai, T., Saito, H., Suzuki, K., Takahashi, M.) 223–243 (Hoboken, 2019).24.Queiroz, N., Humphries, N. E., Noble, L. R., Santos, A. M. & Sims, D. W. Short-term movements and diving behaviour of satellite-tracked blue sharks Prionace glauca in the northeastern Atlantic Ocean. Mar. Ecol. Progress Ser. 406, 265–279 (2010).ADS 
    Article 

    Google Scholar 
    25.McMahon, C. R. & Hays, G. C. Thermal niche, large-scale movements and implications of climate change for a critically endangered marine vertebrate. Glob. Change Biol. 12, 1330–1338 (2006).ADS 
    Article 

    Google Scholar 
    26.Nakatsubo, T., Kawachi, M., Mano, N. & Hirose, H. Spawning period of ocean sunfish Mola mola in waters of the eastern Kanto region, Japan. Aquacult. Sci. 55, 613–618 (2007).
    Google Scholar 
    27.Ashida, H., Suzuki, N., Tanabe, T., Suzuki, N. & Aonuma, Y. Reproductive condition, batch fecundity, and spawning fraction of large Pacific bluefin tuna Thunnus orientalis landed at Ishigaki Island, Okinawa, Japan. Environ. Biol. Fish. 98, 1173–1183 (2015).Article 

    Google Scholar 
    28.Watai, M. et al. Comparative analysis of the early growth history of Pacific bluefin tuna Thunnus orientalis from different spawning grounds. Mar. Ecol. Progress Ser. 607, 207–220 (2018).ADS 
    Article 

    Google Scholar 
    29.Stevens, J. D., Bradford, R. W. & West, G. J. Satellite tagging of blue sharks (Prionace glauca) and other pelagic sharks off eastern Australia: Depth behaviour, temperature experience and movements. Mar. Biol. 157, 575–591 (2010).Article 

    Google Scholar 
    30.Musyl, M. K. et al. Vertical movements of bigeye tuna (Thunnus obesus) associated with islands, buoys, and seamounts near the main Hawaiian Islands from archival tagging data. Fish. Oceanogr. 12, 152–169 (2003).Article 

    Google Scholar 
    31.Lin, S. J. et al. Vertical and horizontal movements of bigeye tuna (Thunnus obesus) in southeastern Taiwan. Mar. Freshw. Behav. Physiol. 54, 1–21 (2021).Article 

    Google Scholar 
    32.Yasuda, I. & Kitagawa, D. Locations of early fishing grounds of saury in the northwestern Pacific. Fish. Oceanogr. 5, 63–69 (1996).Article 

    Google Scholar 
    33.Godø, O. R. et al. Mesoscale eddies are oases for higher trophic marine life. PloS ONE 7, e30161 (2012). 34.Polovina, J. J. et al. Forage and migration habitat of loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea) sea turtles in the central North Pacific Ocean. Fish. Oceanogr. 13, 36–51 (2004).Article 

    Google Scholar 
    35.Sbragaglia, V. et al. Annual rhythms of temporal niche partitioning in the Sparidae family are correlated to different environmental variables. Sci. Rep. 9, 1708 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    36.Nakamura, I., Mastumoto, R. & Sato, K. Body temperature stability in the whale shark, the world’s largest fish. J. Exp. Biol. 223, jeb210286 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Brill, R. W., Bigelow, K. A., Musyl, M. K., Fritsches, K. A. & Warrant, E. J. Bigeye tuna (Thunnus obesus) behavior and physiology and their relevance to stock assessments and fishery biology. Col. Vol. Sci. Pap. ICCAT 57, 142–161 (2005).
    Google Scholar 
    38.Stramma, L. et al. Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nat. Clim. Change 2, 33–37 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    39.Brill, R. W. A review of temperature and oxygen tolerance studies of tunas pertinent to fisheries oceanography, movement models and stock assessments. Fish. Oceanogr. 3, 204–216 (1994).Article 

    Google Scholar 
    40.Lam, C. H., Kiefer, D. A. & Domeier, M. L. Habitat characterization for striped marlin in the Pacific Ocean. Fish. Res. 166, 80–91 (2015).Article 

    Google Scholar 
    41.Carlisle, A. B. et al. Influence of temperature and oxygen on the distribution of blue marlin (Makaira nigricans) in the Central Pacific. Fish. Oceanogr. 26, 34–48 (2017).Article 

    Google Scholar 
    42.Madigan D. J. et al. Water column structure defines vertical habitat of twelve pelagic predators in the South Atlantic. ICES J. Mar. Sci. 78, 867–883 (2021).Article 

    Google Scholar 
    43.Schlitzer, R. Export production in the equatorial and North Pacific derived from dissolved oxygen, nutrient and carbon data. J. Oceanogr. 60, 53–62 (2004).CAS 
    Article 

    Google Scholar 
    44.Thomsen, S. et al. The formation of a subsurface anticyclonic eddy in the Peru-Chile Undercurrent and its impact on the near-coastal salinity, oxygen, and nutrient distributions. J. Geophys. Res. 121, 476–501 (2016).ADS 
    Article 

    Google Scholar 
    45.Nakamura, I. & Sato, K. Ontogenetic shift in foraging habit of ocean sunfish Mola mola from dietary and behavioral studies. Mar. Biol. 161, 1263–1273 (2014).Article 

    Google Scholar 
    46.QGIS Development Team. Quantum GIS geographic information system. Open Source Geospatial Foundation Project. http://www.qgis.org/en/site/ (2016).47.Chelton, D. B., Gaube, P., Schlax, M. G., Early, J. J. & Samelson, R. M. The influence of nonlinear mesoscale eddies on near-surface oceanic chlorophyll. Science 334, 328–332 (2011).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Fiedler, P. C. Comparison of objective descriptions of the thermocline. Limnol. Oceanogr. Methods 8, 313–325 (2010).Article 

    Google Scholar 
    49.Zar, J. H. Biostatistical Analysis 4th edn. (Prentice Hall, 1999).
    Google Scholar 
    50.Clarke, K. R., & Gorley, R. N. PRIMER v6: User manual/tutorial. PRIMER-E, Plymouth.51.Wood, S. N. On p-values for smooth components of an extended generalized additive model. Biometrika 100, 221–228 (2013).MathSciNet 
    MATH 
    Article 

    Google Scholar  More

  • in

    Pheromones that correlate with reproductive success in competitive conditions

    Reproductive successThe production of urinary pheromones correlated with male but not female reproductive success (RS; defined in “Materials and methods” section). The most important predictors of male RS were total urinary protein concentration (75%) and social status (69%; Table 1; based on conditional model average sum of weights). The relative importance of age, creatinine, and mass ranged from 23 to 39%; PC ratio (protein:creatinine concentration) was excluded from the model due to collinearity (VIF = 6.97). Total urinary protein concentration during the enclosure phase was positively correlated with RS for males (Spearman R = 0.52, p = 0.01; Fig. 1a), but not females (Fig. 1b). This correlation is explained by the low protein concentration in the urine of non-reproductive males, as it is no longer significant after removing these males from the analysis (R = 0.12, p = 0.62; Supplementary Fig. S2). The median total urinary protein concentration was 5512 µg mL−1 and 5028 µg mL−1 for reproductive and non-reproductive males, respectively (Wilcoxon rank sum test W = 5, p  More

  • in

    Turn taking is not restricted by task specialisation but does not facilitate equality in offspring provisioning

    1.Trivers, R. L. Parental investment and sexual selection. in Sexual Selection and the Descent of Man 1871–1971 136–207 (Aldine, 1972). doi:https://doi.org/10.1002/ajpa.13304002262.Stearns, S. Trade-offs in life-history evolution. Funct. Ecol. 3, 259–268 (1989).Article 

    Google Scholar 
    3.McNamara, J. M., Gasson, C. E. & Houston, A. I. Incorporating rules for responding into evolutionary games. Nature 401, 368–371 (1999).ADS 
    CAS 
    PubMed 

    Google Scholar 
    4.Houston, A. I. & Davies, N. B. The evolution of cooperation and life-history in the dunnock. Behav. Ecol. 1, 471–487 (1985).
    Google Scholar 
    5.McNamara, J. M., Houston, A. I., Barta, Z. & Osorno, J. L. Should young ever be better off with one parent than with two?. Behav. Ecol. 14, 301–310 (2003).Article 

    Google Scholar 
    6.Lessells, C. M. & McNamara, J. M. Sexual conflict over parental investment in repeated bouts: negotiation reduces overall care. Proc. R. Soc. B Biol. Sci. 279, 1506–1514 (2012).CAS 
    Article 

    Google Scholar 
    7.Harrison, F., Barta, Z. & Székely, T. How is sexual conflict over parental care resolved? A meta-analysis.. J. Evol. Biol. 22, 1800–1812 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Johnstone, R. A. & Hinde, C. A. Negotiation over offspring care – how should parents respond to each other’s efforts?. Behav. Ecol. 17, 818–827 (2006).Article 

    Google Scholar 
    9.Johnstone, R. A. et al. Reciprocity and conditional cooperation between great tit parents. Behav. Ecol. 25, 216–222 (2014).Article 

    Google Scholar 
    10.Gächter, S. Conditional cooperation: behavioral regularities from the lab and the field and their policy implications. In Psychology and economics: a promising new cross-disciplinary field (eds Frey, B. S. & Stutzer, A.) 19–50 (MIT Press, 2007).
    Google Scholar 
    11.Hinde, C. A. Negotiation over offspring care? – A positive response to partner-provisioning rate in great tits. Behav. Ecol. 17, 6–12 (2006).Article 

    Google Scholar 
    12.Meade, J., Nam, K.-B., Lee, J.-W. & Hatchwell, B. J. An experimental test of the information model for negotiation of biparental care. PLoS ONE 6, e19684 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    13.Savage, J. L., Browning, L. E., Manica, A., Russell, A. F. & Johnstone, R. A. Turn-taking in cooperative offspring provisioning: by-product of individual provisioning behaviour or active response rule?. Behav. Ecol. Sociobiol. 71, 162 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Santema, P., Schlicht, E. & Kempenaers, B. Testing the conditional cooperation model: What can we learn from parents taking turns when feeding offspring?. Front. Ecol. Evol. 7, 1–6 (2019).Article 

    Google Scholar 
    15.Baldan, D., Curk, T., Hinde, C. A. & Lessells, C. M. Alternation of nest visits varies with experimentally manipulated workload in brood-provisioning great tits. Anim. Behav. 156, 139–146 (2019).Article 

    Google Scholar 
    16.Baldan, D., Hinde, C. A. & Lessells, C. M. Turn-Taking Between Provisioning Parents: Partitioning Alternation. Front. Ecol. Evol. 7, 1 (2019).Article 

    Google Scholar 
    17.Iserbyt, A., Fresneau, N., Kortenhoff, T., Eens, M. & Müller, W. Decreasing parental task specialization promotes conditional cooperation. Sci. Rep. 7, 6565 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    18.Lessells, C. M. Sexual selection. in The evolution of parental care (eds. Royle, N. J., Smiseth, P. T. & Kolliker, M.) 150–170 (Oxford university press, 2012).19.Barta, Z., Székely, T., Liker, A. & Harrison, F. Social role specialization promotes cooperation between parents. Am. Nat. 183, 747–761 (2014).PubMed 
    Article 

    Google Scholar 
    20.Andreasson, F., Nord, A. & Nilsson, J. -Å. Brood size constrains the development of endothermy in blue tits. J. Exp. Biol. 219, 2212–2219 (2016).PubMed 
    Article 

    Google Scholar 
    21.Perrins, C. M. British tits. (Collins, 1979).22.Banbura, J. et al. Sex differences in parental care in a Corsican Blue Tit Parus caeruleus population. Ardea 89, 517–526 (2001).
    Google Scholar 
    23.García-Navas, V., Ferrer, E. S. & Sanz, J. J. Plumage yellowness predicts foraging ability in the blue tit Cyanistes caeruleus. Biol. J. Linn. Soc. 106, 418–429 (2012).Article 

    Google Scholar 
    24.Mainwaring, M. C. et al. Latitudinal variation in blue tit and great tit nest characteristics indicates environmental adjustment. J. Biogeogr. 39, 1669–1677 (2012).Article 

    Google Scholar 
    25.Pagani-Núñez, E. & Senar, J. C. One hour of sampling is enough: Great tit Parus major parents feed their nestlings consistently across time. Acta Ornithol. 48, 194–200 (2013).Article 

    Google Scholar 
    26.Griffioen, M., Müller, W. & Iserbyt, A. A fixed agreement—consequences of brood size manipulation on alternation in blue tits. PeerJ 7, e6826 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Ihle, M., Pick, J. L., Winney, I. S., Nakagawa, S. & Burke, T. Measuring up to reality: Null models and analysis simulations to study parental coordination over provisioning offspring. Front. Ecol. Evol. 7, 142 (2019).Article 

    Google Scholar 
    28.Schlicht, E., Santema, P., Schlicht, R. & Kempenaers, B. Evidence for cooperation in biparental care systems? A comment on Johnstone et al.. Behav. Ecol. 27, 1 (2016).Article 

    Google Scholar 
    29.Griffioen, M., Iserbyt, A. & Müller, W. Handicapping males does not affect their rate of parental provisioning, but impinges on their partners’ turn taking behavior. Front. Ecol. Evol. 7, 1–7 (2019).Article 

    Google Scholar 
    30.Andreasson, F., Nord, A. & Nilsson, J.-Å. Experimentally increased nest temperature affects body temperature, growth and apparent survival in blue tit nestlings. J. Avian Biol. Biol. e01620, (2018).31.Iserbyt, A., Griffioen, M., Eens, M. & Müller, W. Enduring rules of care within pairs – how blue tit parents resume provisioning behaviour after experimental disturbance. Sci. Rep. 9, 2776 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    32.Lucass, C., Fresneau, N., Eens, M. & Müller, W. Sex roles in nest keeping – how information asymmetry contributes to parent-offspring co-adaptation. Ecol. Evol. 6, 1825–1833 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Yoon, J., Sofaer, H. R., Sillett, T. S., Morrison, S. A. & Ghalambor, C. K. The relationship between female brooding and male nestling provisioning: Does climate underlie geographic variation in sex roles ?. J. Avian Biol. 47, 1–9 (2016).Article 

    Google Scholar 
    34.Amininasab, S. M., Kingma, S. A., Birker, M., Hildenbrandt, H. & Komdeur, J. The effect of ambient temperature, habitat quality and individual age on incubation behaviour and incubation feeding in a socially monogamous songbird. Behav. Ecol. Sociobiol. https://doi.org/10.1007/s00265-016-2167-2 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Bryan, S. M. & Bryant, D. M. Heating nest-boxes reveals an energetic constraint on incubation behaviour in great tits, Parus major. Proc. R. Soc. B 266, 157 (1999).PubMed Central 
    Article 

    Google Scholar 
    36.Sanz, J. J. & Moreno, J. Mass loss in brooding female pied flycatchers ficedula hypoleuca: No evidence for reproductive stress. J. Avian Biol. 26, 313 (1995).Article 

    Google Scholar 
    37.Chastel, O. & Kersten, M. Brood size and body condition in the House Sparrow Passer domesticus: The influence of brooding behaviour. Ibis (Lond. 1859). 144, 284–292 (2002).38.Stearns, S. The evolution of life histories. (Oxford University Press (OUP), 1992). https://doi.org/10.5962/bhl.title.166231.39.Ardia, D. R., Perez, J. H. & Clotfelter, E. D. Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows. Proc. R. Soc. B – Biol. Sci. 277, 1881–1888 (2010).40.Perez, J. H., Ardia, D. R., Chad, E. K. & Clotfelter, E. D. Experimental heating reveals nest temperature affects nestling condition in tree swallows ( Tachycineta bicolor ). Biol. Lett. 4, 468–471 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Nour, N., Currie, D., Matthysen, E., Van Damme, R. & Dhondt, A. A. Effects of habitat fragmentation on provisioning rates, diet and breeding success in two species of tit (great tit and blue tit). Oecologia 114, 522–530 (1998).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Grieco, F. Time constraint on food choice in provisioning blue tits, Parus caeruleus: The relationship between feeding rate and prey size. Anim. Behav. 64, 517–526 (2002).Article 

    Google Scholar 
    43.Jenkins, J. B., Mueller, A. J., Thompson, C. F., Sakaluk, S. K. & Bowers, E. K. Female birds monitor the activity of their mates while brooding nest-bound young. Anim. Cogn. https://doi.org/10.1007/s10071-020-01453-5 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Johnstone, R. A. & Savage, J. L. Conditional cooperation and turn-taking in parental care. Front. Ecol. Evol. 7, 1 (2019).Article 

    Google Scholar 
    45.Santema, P., Schlicht, E., Schlicht, L. & Kempenaers, B. Blue tits do not return faster to the nest in response to either short- or long-term begging playbacks. Anim. Behav. 123, 117–127 (2017).Article 

    Google Scholar 
    46.Székely, T. Sexual Conflict Between Parents: Offspring Desertion and Asymmetrical Parental Care. Cold Spring Harb. Perspect. Biol. 6, 1–20 (2014).Article 

    Google Scholar 
    47.Griffith, S. C. Cooperation and Coordination in Socially Monogamous Birds: Moving Away From a Focus on Sexual Conflict. Front. Ecol. Evol. 7, 1–15 (2019).Article 

    Google Scholar 
    48.Patrick, S. C., Corbeau, A., Réale, D. & Weimerskirch, H. Coordination in parental effort decreases with age in a long-lived seabird. Oikos 129, 1763–1772 (2020).Article 

    Google Scholar 
    49.Lejeune, L. et al. Environmental effects on parental care visitation patterns in blue tits Cyanistes caeruleus. Front. Ecol. Evol. 7, 1–15 (2019).Article 

    Google Scholar 
    50.Baldan, D. & Ouyang, J. Q. Urban resources limit pair coordination over offspring provisioning. Sci. Rep. 1, 1–11. https://doi.org/10.1038/s41598-020-72951-2 (2020).CAS 
    Article 

    Google Scholar 
    51.Bebbington, K. & Hatchwell, B. J. Coordinated parental provisioning is related to feeding rate and reproductive success in a songbird. Behav. Ecol. 27, 652–659 (2016).Article 

    Google Scholar 
    52.Koenig, W. D. & Walters, E. L. Provisioning patterns in the cooperatively breeding acorn woodpecker: does feeding behaviour serve as a signal?. Anim. Behav. 119, 125–134 (2016).Article 

    Google Scholar 
    53.Leniowski, K. & Węgrzyn, E. Synchronisation of parental behaviours reduces the risk of nest predation in a socially monogamous passerine bird. Sci. Rep. 8, 7385 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Tyson, C. et al. Coordinated provisioning in a dual foraging pelagic seabird. Anim. Behav. 132, 73–79 (2017).Article 

    Google Scholar 
    55.Wojczulanis-Jakubas, K., Araya-Salas, M. & Jakubas, D. Seabird parents provision their chick in a coordinated manner. PLoS ONE 13, 1–13 (2018).Article 
    CAS 

    Google Scholar  More

  • in

    Morphological and spectroscopic analysis of snow and glacier algae and their parasitic fungi on different glaciers of Svalbard

    1.Perini, L., Gostinčar, C. & Gunde-Cimerman, N. Fungal and bacterial diversity of Svalbard subglacial ice. Diversity and hidden host specificity of chytrids infecting colonial volvocacean algae. Sci. Rep. 27, 20230. https://doi.org/10.1038/s41598-019-56290-5 (2019).CAS 
    Article 

    Google Scholar 
    2.Margesin, R., Schinner, F. Cold-adapted organisms. In Ecology, Physiology, Enzymology and Molecular Biology (eds. Margesin, R. & Schinner, F) (Springer, 1999).3.Mueller, D. R. & Pollard, W. H. Gradient analysis of cryoconite ecosystems from two polar glaciers. Polar Biol. 27, 66–74 (2004).Article 

    Google Scholar 
    4.Hodson, A. et al. Glacial ecosystems. Ecol. Monogr. 78, 41–67 (2008).Article 

    Google Scholar 
    5.Hoham, R. W. & Remias, D. Snow and glacial algae: A review. J. Phycol. 56, 264–282. https://doi.org/10.1111/jpy.12952 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    6.Kol, E. & Eurola, S. Red snow algae from Spitsbergen. Astarte. J. Arct. Biol. 7, 61–66 (1974).
    Google Scholar 
    7.Stibal, M., Elster, J., Sabacká, M. & Kastovská, K. Seasonal and diel changes in photosynthetic activity of the snow alga Chlamydomonas nivalis (Chlorophyceae) from Svalbard determined by pulse amplitude modulation fluorometry. FEMS Microbiol. Ecol. 59, 265–273 (2007).CAS 
    Article 

    Google Scholar 
    8.Kviderová, J. Research on cryosestic communities in Svalbard: the snow algae of temporary snowfields in Petuniabukta, Central Svalbard. Czech Polar Rep. 2, 8–19 (2012).Article 

    Google Scholar 
    9.Remias, D., Lütz-Meindl, U. & Lütz, C. Photosynthesis, pigments, and ultrastructure of the alpine snow alga Chlamydomonas nivalis. Eur. J. Phycol. 40, 259–268 (2005).CAS 
    Article 

    Google Scholar 
    10.Takeuchi, N. et al. Variations in phototroph communities on the ablating bare-ice surface of glaciers on Brøggerhalvøya, Svalbard. Front. Earth Sci. https://doi.org/10.3389/feart.2019.00004 (2019).Article 

    Google Scholar 
    11.Leya, T., Müller, T., Ling, H. U., Fuhr, G. Snow algae from north-western Spitsbergen (Svalbard). In The Coastal Ecosystem of Kongsfjorden, Svalbard. Synopsis of Biological Research Performed at the Koldewey Station in the Years 1991–2003. Ber. (ed. Wiencke, C.) 46–54 (Polarforsch. Meeresforsch, 2004).12.Remias, D., Holzinger, A., Aigner, S. & Lütz, C. Ecophysiology and ultrastructure of Ancylonema nordenskioeldii (Zygnematales, Streptophyta), causing brown ice on glaciers in Svalbard (high Arctic). Polar Biol. 35, 899–908 (2011).Article 

    Google Scholar 
    13.Uetake, J., Naganuma, T., Hebsgaard, M. B., Kanda, H. & Kohshima, S. Communities of algae and cyanobacteria on glaciers in west Greenland. Polar Sci. 4, 71–80 (2010).ADS 
    Article 

    Google Scholar 
    14.Takeuchi, N. The altitudinal distribution of snow algae on an Alaska glacier (Gulkana Glacier in the Alaska Range). Hydrol. Process. 15, 3447–3459 (2001).ADS 
    Article 

    Google Scholar 
    15.Takeuchi, N. & Kohshima, S. A snow algal community on Tyndall Glacier in the Southern Patagonia Icefield, Chile. Arct. Antarct. Alp. Res. 36, 92–99 (2004).Article 

    Google Scholar 
    16.Yoshimura, Y., Kohshima, S. & Ohtani, S. A community of snow algae on a Himalayan glacier: Change of algal biomass and community structure with altitude. Arct. Antarct. Alp. Res. 29, 126–137 (1997).Article 

    Google Scholar 
    17.Komárek, O. & Komárek, J. Contribution to the taxonomy and ecology of cryosestic algae in the summer season 1995–96 at King George Island, S. Shetland Islands. Nova Hedwig. Beih. 123, 121–140 (2001).
    Google Scholar 
    18.Kagami, M., de Bruin, A., Ibelings, B. W. & Van Donk, E. Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578, 113–129 (2007).Article 

    Google Scholar 
    19.Gromov, B. V., Pljusch, A. V. & Mamkaeva, K. A. Morphology and possible host range of Rhyizophydium algavorum sp. nov. (Chytridiales) – An obligate parasite of algae. Protistology 1, 62–65 (1999).
    Google Scholar 
    20.Hassett, B. T. & Gradinger, R. Chytrids dominate arctic marine fungal communities. Environ. Microbiol. 18, 2001–2009 (2016).CAS 
    Article 

    Google Scholar 
    21.Hassett, B. T. et al. Arctic marine fungi: Biomass, functional genes, and putative ecological roles. ISME J. 13, 1484–1496 (2019).CAS 
    Article 

    Google Scholar 
    22.Rämä, T. et al. Fungi sailing the Arctic Ocean: Speciose communities in North Atlantic driftwood as revealed by high-throughput amplicon sequencing. Microb. Ecol. 72, 295–304 (2016).Article 

    Google Scholar 
    23.Rämä, T., Hassett, B. T. & Bubnova, E. Arctic marine fungi: From filaments and flagella to operational taxonomic units and beyond. Bot. Mar. 60, 433–452 (2017).Article 

    Google Scholar 
    24.Zhang, T., Wang, N. F., Zhang, Y. Q., Liu, H. Y. & Yu, L. Y. Diversity and distribution of fungal communities in the marine sediments of Kongsfjorden, Svalbard (High Arctic). Sci. Rep. 5, 14524. https://doi.org/10.1038/srep14524 (2015).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Zhang, T., Wang, N. F., Zhang, Y. Q., Liu, H. Y. & Yu, L. Y. Diversity, and distribution of aquatic fungal communities in the Ny-Ålesund region, Svalbard (High Arctic): aquatic fungi in the Arctic. Microb. Ecol. 71, 543–554 (2016).Article 

    Google Scholar 
    26.Remy, W., Taylor, T. N. & Hass, H. Early Devonian fungi: A Blastocladalean fungus with sexual reproduction. Am. J. Bot. 81, 690–702 (1994).Article 

    Google Scholar 
    27.Senanayake, I. C. et al. Morphological approaches in studying fungi: Collection, examination, isolation, sporulation and preservation. Mycosphere 11, 2678–2754 (2020).Article 

    Google Scholar 
    28.Fiołka, M. J., Takeuchi, N., Sofińska-Chmiel, W., Mieszawska, S. & Treska, I. Morphological and physicochemical diversity of snow algae from Alaska. Sci. Rep. 10, 19167. https://doi.org/10.1038/s41598-020-76215-x (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    29.Monheit, J. E., Cowan, D. F. & Moore, D. G. Rapid detection of fungi in tissues using calcofluor white and fluorescence microscopy. Arch. Pathol. Lab. Med. 108, 616–618 (1984).CAS 
    PubMed 

    Google Scholar 
    30.Semedo, M. C., Karmali, A. & Fonseca, L. A high throughput colorimetric assay of β-1,3-d-glucans by Congo red dye. J. Microbiol. Methods. 10, 140–148 (2015).Article 

    Google Scholar 
    31.Herburger, K. & Holzinger, A. Aniline blue and Calcofluor white staining of callose and cellulose in the streptophyte green algae Zygnema and Klebsormidium. Bio Protoc. 6, 1969. https://doi.org/10.21769/BioProtoc.1969 (2016).Article 

    Google Scholar 
    32.Müller, U. & Sengbusch, P. Visualization of aquatic fungi (Chytridiales) parasitizing on algae by means of induced fluorescence. Arch. Hydrobiol. 97, 471–485 (1983).
    Google Scholar 
    33.Yang, Y., Xiang, Y. & Xu, M. From red to green: The propidium iodide-permeable membrane of Shewanella decolorationis S12 is repairable. Sci. Rep. 5, 18583. https://doi.org/10.1038/srep18583 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    34.Luo, Z. et al. Preparation and properties of enzyme-modified cassava starch−zinc complexes. Agric. Food Chem. 61, 4631–4638 (2013).CAS 
    Article 

    Google Scholar 
    35.Beamson, G., Briggs, D. High Resolution XPS of Organic Polymers—The Scienta ESCA300 Database (Wiley Interscience, 1992).36.Miller, D. J., Biesinger, M. C. & McIntyre, N. S. Interactions of CO2 and CO at fractional atmosphere pressures with iron and iron oxide surfaces: One possible mechanism for surface contamination?. Surf. Interface Anal. 33, 299–305 (2002).CAS 
    Article 

    Google Scholar 
    37.Payne, B. P., Biesinger, M. C. & McIntyre, N. S. The study of polycrystalline nickel metal oxidation by water vapour. J. Electron Spectros. Relat. Phenom. 184, 29–37 (2011).CAS 
    Article 

    Google Scholar 
    38.Oh, Y. J. et al. Oxygen functional groups and electrochemical capacitive behavior of incompletely reduced graphene oxides as a thin-film electrode of supercapacitor. Electrachem. Acta. 116, 118–128 (2014).CAS 
    Article 

    Google Scholar 
    39.Procházková, L., Leya, T., Křížková, H. & Nedbalová, L. Sanguina nivaloides and Sanguina aurantia gen. et spp. nov. (Chlorophyta): The taxonomy, phylogeny, biogeography and ecology of two newly recognised algae causing red and orange snow. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiz064 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    40.Procházková, L., Řezanka, T., Nedbalová, L. & Remias, D. Unicellular versus filamentous: The glacial alga Ancylonema alaskana comb. et stat. nov. and its ecophysiological relatedness to Ancylonema nordenskioeldii (Zygnematophyceae, Streptophyta). Microorganisms. https://doi.org/10.3390/microorganisms9051103 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    41.Müller, T., Bleiss, W., Martin, C. D., Rogaschewski, S. & Fuhr, G. Snow algae from northwest Svalbard: Their identification, distribution, pigment and nutrient content. Polar Biol. 20, 14–32 (1998).Article 

    Google Scholar 
    42.Domozych, D. et al. The cell walls of green algae: A journey through evolution and diversity. Front. Plant. Sci. https://doi.org/10.3389/fpls.2012.00082 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    43.Holzinger, A. & Lütz, C. Algae and UV irradiation: Effects on ultrastructure and related metabolic functions. Micron 37, 190–207 (2006).Article 

    Google Scholar 
    44.Rad-Menéndez, C. et al. Rediscovering Zygorhizidium affluenscanter: molecular taxonomy, infectious cycle, and cryopreservation of a chytrid infecting the bloom-forming diatom Asterionella formosa. Appl. Environ. Microbiol. 84, e01826-e1918. https://doi.org/10.1128/AEM.01826-18 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Canter-Lund, H., Lund, J.G. Freshwater Algae: Their Microscopic World Explored. (ed. Canter-Lund, H.). 21–93. (Biopress, 1995).46.Kol, E. Kryobiologie. Biologie und Limnologie des Schneesund Eises. I. Kryovegetation. Die Binnengewa¨sser, Band XXIV. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart (1968).47.Stein, J. R. & Amundsen, C. C. Studies on snow algae and fungi from the front range of Colorado. Can. J. Bot. 45, 2033–2045 (1967).Article 

    Google Scholar 
    48.Hoham, R. W., Laursen, A. E., Clive, S. O., Duval, B. Snow algae and other microbes in several alpine areas in New England. in Proceedings of the 61st Annual Western Snow Conference, Quebec City, Canada. 165–173 (1993).49.Brown, P. S., Olson, B. J. S. C. & Jumpponen, A. Fungi and algae co-occur in snow: an issue of shared habitat or algal facilitation of heterotrophs?. Arct. Antarct. Alp. Res. 47, 729–749 (2015).Article 

    Google Scholar 
    50.Jumpponen, A., Egerton-Warburton, L. Mycorrhizal fungi in successional environments—A community assembly model incorporating host plant, environmental and biotic filters. In Dighton (ed. White, J. & Oudemans, P.) 139–180 (CRC Press, 2005).51.Freeman, K. R. et al. Evidence that chytrids dominate fungal communities in high elevation soils. PNAS 106, 18315–18320 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    52.Sime-Ngando, T. Phytoplankton chytridiomycosis: Fungal parasites of phytoplankton and their imprints on the food web dynamics. Front. Microbiol. https://doi.org/10.3389/fmicb.2012.00361 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    53.Powell, M. J. Looking at mycology with a Janus face. A glimpse at Chytridiomycetes active in the environment. Mycologia 85, 1–20 (1993).Article 

    Google Scholar 
    54.Ibelings, B. W. et al. Host parasite interactions between freshwater phytoplankton and chytrid fungi (Chytridiomycota). J. Phycol. 40, 437–453 (2004).Article 

    Google Scholar 
    55.Scholz, B., Küpper, F. C., Vyverman, W., Ólafsson, H. G. & Karsten, U. Chytridiomycosis of marine diatoms—The role of stress physiology and resistance in parasite-host recognition and accumulation of defense molecules. Mar. Drugs. 15, 26. https://doi.org/10.3390/md15020026 (2017).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    56.Müehlstein, L. K., Amon, J. P. & Leffler, D. L. Chemotaxis in the marine fungus Rhizophydium littoreum. Appl. Environ. Microbiol. 54, 1668–1672 (1988).ADS 
    Article 

    Google Scholar 
    57.Moss, A. S., Reddy, N. S., Dortaj, I. M. & San Francisco, M. J. Chemotaxis of the amphibian pathogen Batrachochytrium dendrobatidis and its response to a variety of attractants. Mycologia 100, 1–5 (2008).CAS 
    Article 

    Google Scholar 
    58.Powell, M. J. Production, and modifications of extracellular structures during development of Chytridiomycetes. Protoplasma 181, 123–141 (1994).Article 

    Google Scholar 
    59.Konishi, H., Hio, M., Kobayashi, M., Takase, R. & Hashimoto, W. Bacterial chemotaxis towards polysaccharide pectin by pectin-binding protein. Sci. Rep. 10, 3977. https://doi.org/10.1038/s41598-020-60274-1 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    60.Bruning, K. Effects of temperature and light on the population-dynamics of the Asterionella-Rhizophydium association. J. Plankton Res. 13, 707–719 (1991).Article 

    Google Scholar  More

  • in

    Genetic diversity in North American Cercis Canadensis reveals an ancient population bottleneck that originated after the last glacial maximum

    1.Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913. https://doi.org/10.1038/35016000 (2000).ADS 
    Article 
    PubMed 
    CAS 

    Google Scholar 
    2.Hewitt, G. Genetic consequences of climatic oscillations in the Quaternary. Philos. Trans. R. Soc. Lond. 359, 183–195. https://doi.org/10.1098/rstb.2003.1388 (2004).Article 
    CAS 

    Google Scholar 
    3.Ehlers, J. & Gibbard, P. Quaternary Glaciations-Extent and Chronology: Part I: Europe Vol. 2 (Elsevier, New York, 2004).
    Google Scholar 
    4.Call, A. et al. Genetic structure and post-glacial expansion of Cornus florida L. (Cornaceae): Integrative evidence from phylogeography, population demographic history, and species distribution modeling. J. Syst. Evol. 54, 136–151. https://doi.org/10.1111/jse.12171 (2016).Article 

    Google Scholar 
    5.Jackson, S. et al. Vegetation and environment in eastern North America during the Last Glacial Maximum. Quatern. Sci. Rev. 19, 489–508. https://doi.org/10.1016/S0277-3791(99)00093-1 (2000).ADS 
    Article 

    Google Scholar 
    6.Nadeau, S. et al. Contrasting patterns of genetic diversity across the ranges of Pinus monticola and P. strobus: A comparison between eastern and western North American postglacial colonization histories. Am. J. Bot. 102, 1342–1355. https://doi.org/10.3732/ajb.1500160 (2015).Article 
    PubMed 
    CAS 

    Google Scholar 
    7.Beaulieu, J. & Simon, J. Genetic structure and variability in Pinus strobus in Quebec. Can. J. For. Res. 24, 1726–1733. https://doi.org/10.1139/x94-223 (1994).Article 

    Google Scholar 
    8.Provan, J. & Bennett, K. Phylogeographic insights into cryptic glacial refugia. Trends Ecol. Evol. 23, 564–571. https://doi.org/10.1016/j.tree.2008.06.010 (2008).Article 
    PubMed 

    Google Scholar 
    9.Soltis, D., Morris, A., McLachlan, J., Manos, P. & Soltis, P. Comparative phylogeography of unglaciated eastern North America. Mol. Ecol. 15, 4261–4293. https://doi.org/10.1111/j.1365-294X.2006.03061.x (2006).Article 
    PubMed 

    Google Scholar 
    10.Mee, J. & Moore, J. The ecological and evolutionary implications of microrefugia. J. Biogeogr. 41, 837–841. https://doi.org/10.1111/jbi.12254 (2014).Article 

    Google Scholar 
    11.Hoban, S. et al. Range-wide distribution of genetic diversity in the North American tree Juglans cinerea: A product of range shifts, not ecological marginality or recent population decline. Mol. Ecol. 19, 4876–4891. https://doi.org/10.1111/j.1365-294X.2010.04834.x (2010).Article 
    PubMed 

    Google Scholar 
    12.Hampe, A. & Petit, R. Conserving biodiversity under climate change: The rear edge matters. Ecol. Lett. 8, 461–467. https://doi.org/10.1111/j.1461-0248.2005.00739.x (2005).Article 
    PubMed 

    Google Scholar 
    13.Excoffier, L., Foll, M. & Petit, R. Genetic consequences of range expansions. Annu. Rev. Ecol. Evol. Syst. 40, 481–501. https://doi.org/10.1146/annurev.ecolsys.39.110707.173414 (2009).Article 

    Google Scholar 
    14.McLachlan, J., Clark, J. & Manos, P. Molecular indicators of tree migration capacity under rapid climate change. Ecology 86, 2088–2098. https://doi.org/10.1890/04-1036 (2005).Article 

    Google Scholar 
    15.Bemmels, J. & Dick, C. Genomic evidence of a widespread southern distribution during the Last Glacial Maximum for two eastern North American hickory species. J. Biogeogr. 45, 1739–1750. https://doi.org/10.1111/jbi.13358 (2018).Article 

    Google Scholar 
    16.Jaramillo-Correa, J., Beaulieu, J., Khasa, D. & Bousquet, J. Inferring the past from the present phylogeographic structure of North American forest trees: Seeing the forest for the genes. Can. J. For. Res. 39, 286–307. https://doi.org/10.1139/X08-181 (2009).Article 

    Google Scholar 
    17.Eckert, C., Samis, K. & Lougheed, S. Genetic variation across species’ geographical ranges: The central–marginal hypothesis and beyond. Mol. Ecol. 17, 1170–1188. https://doi.org/10.1111/j.1365-294X.2007.03659.x (2008).Article 
    PubMed 
    CAS 

    Google Scholar 
    18.Foll, M. & Gaggiotti, O. Identifying the environmental factors that determine the genetic structure of populations. Genetics 174, 875–891. https://doi.org/10.1534/genetics.106.059451 (2006).Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 
    19.Loveless, M. & Hamrick, J. Ecological determinants of genetic structure in plant populations. Ann. Rev. Ecol. Syst. 15, 65–95. https://doi.org/10.1146/annurev.es.15.110184.000433 (1984).Article 

    Google Scholar 
    20.Roberts, D., Werner, D., Wadl, P. & Trigiano, R. Inheritance and allelism of morphological traits in eastern redbud (Cercis canadensis L.). Hortic. Res. 2, 1–11 (2015).Article 

    Google Scholar 
    21.Couvillon, G. Cercis canadensis L. seed size influences germination rate, seedling dry matter, and seedling leaf area. HortScience 37, 206–207 (2002).Article 

    Google Scholar 
    22.Li, S. et al. Methods for breaking the dormancy of eastern redbud (Cercis canadensis) seeds. Seed Sci. Technol. 41, 27–35 (2013).Article 

    Google Scholar 
    23.Cheong, E. & Pooler, M. Micropropagation of Chinese redbud (Cercis yunnanensis) through axillary bud breaking and induction of adventitious shoots from leaf pieces. In Vitro Cell. Dev. Biol. Plant 39, 455–458 (2003).Article 

    Google Scholar 
    24.Pooler, M., Jacobs, K. & Kramer, M. Differential resistance to Botryosphaeria ribis among Cercis taxa. Plant Dis. 86, 880–882. https://doi.org/10.1094/PDIS.2002.86.8.880 (2002).Article 
    PubMed 
    CAS 

    Google Scholar 
    25.Trigiano, R., Beaty, R. & Graham, E. Somatic embryogenesis from immature embryos of redbud (Cercis canadensis). Plant Cell Rep. 7, 148–150. https://doi.org/10.1007/BF00270127 (1988).Article 
    PubMed 
    CAS 

    Google Scholar 
    26.Wadl, P., Trigiano, R., Werner, D., Pooler, M. & Rinehart, T. Simple sequence repeat markers from Cercis canadensis show wide cross-species transfer and use in genetic studies. J. Am. Soc. Hortic. Sci. 137, 189–201. https://doi.org/10.21273/JASHS.137.3.189 (2012).Article 

    Google Scholar 
    27.Ony, M. et al. Habitat fragmentation influences genetic diversity and differentiation: Fine-scale population structure of Cercis canadensis (eastern redbud). Ecol. Evol. 10, 3655–3670. https://doi.org/10.1002/ece3.6141 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Amos, W. et al. Automated binning of microsatellite alleles: Problems and solutions. Mol. Ecol. Resour. 7, 10–14. https://doi.org/10.1111/j.1471-8286.2006.01560.x (2007).Article 
    CAS 

    Google Scholar 
    29.R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2019).30.Kamvar, Z., Tabima, J. & Grünwald, N. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281. https://doi.org/10.7717/peerj.281 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Kamvar, Z., Brooks, J. & Grünwald, N. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6, 208. https://doi.org/10.3389/fgene.2015.00208 (2015).Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 
    32.Tsui, C. et al. Population structure and migration pattern of a conifer pathogen, Grosmannia clavigera, as influenced by its symbiont, the mountain pine beetle. Mol. Ecol. 21, 71–86. https://doi.org/10.1111/j.1365-294X.2011.05366.x (2012).Article 
    PubMed 

    Google Scholar 
    33.Nei, M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590 (1978).Article 
    CAS 

    Google Scholar 
    34.Shannon, C. E. A mathematical theory of communication. Bell System Tech. J. 27, 379–423 (1948).MathSciNet 
    Article 

    Google Scholar 
    35.Goudet, J. Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x (2005).Article 

    Google Scholar 
    36.Hurlbert, S. The nonconcept of species diversity: A critique and alternative parameters. Ecology 52, 577–586. https://doi.org/10.2307/1934145 (1971).Article 

    Google Scholar 
    37.El Mousadik, A. & Petit, R. High level of genetic differentiation for allelic richness among populations of the Argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor. Appl. Genet. 92, 832–839. https://doi.org/10.1007/BF00221895 (1996).Article 
    PubMed 

    Google Scholar 
    38.Bird, C., Karl, S., Smouse, P. & Toonen, R. In Phylogeography and Population Genetics in Crustacea Vol. 19 (eds Held Christoph, Koenemann Stefan, & Schubart Christoph) pp. 31–55 (Boca Raton, FL: CRC Press, 2011).39.Meirmans, P. & Hedrick, P. Assessing population structure: FST and related measures. Mol. Ecol. Resour. 11, 5–18. https://doi.org/10.1111/j.1755-0998.2010.02927.x (2011).Article 
    PubMed 

    Google Scholar 
    40.Pritchard, J., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).Article 
    CAS 

    Google Scholar 
    41.Earl, D. & Bridgett, V. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7 (2012).Article 

    Google Scholar 
    42.Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x (2005).Article 
    CAS 

    Google Scholar 
    43.Francis, R. Pophelper: An R package and web app to analyse and visualize population structure. Mol. Ecol. Resour. 17, 27–32. https://doi.org/10.1111/1755-0998.12509 (2017).Article 
    PubMed 
    CAS 

    Google Scholar 
    44.Becker, R. & Wilks, A. MAPS: An R Package to Drae Geographical Maps (Version package 3.3.0, 2018).45.Lemon, J. Plotrix: An R Package for Various Plotting Functions (Version R package 3.8–1, 2006).46.Bruvo, R., Michiels, N., D’souza, T. & Schulenburg, H. A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol. Ecol. 13, 2101–2106. https://doi.org/10.1111/j.1365-294X.2004.02209.x (2004).Article 
    PubMed 
    CAS 

    Google Scholar 
    47.Grünwald, N., Everhart, S., Knaus, B. & Kamvar, Z. Best practices for population genetic analyses. Phytopathology 107, 1000–1010. https://doi.org/10.1094/PHYTO-12-16-0425-RVW (2017).Article 
    PubMed 

    Google Scholar 
    48.Jombart, T. & Ahmed, I. adegenet 1.3–1: New tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3072. https://doi.org/10.1093/bioinformatics/btr521 (2011).Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 
    49.Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 9. https://doi.org/10.1186/1471-2156-11-94 (2010).Article 

    Google Scholar 
    50.Cullingham, C., Cooke, J. & Coltman, D. Effects of introgression on the genetic population structure of two ecologically and economically important conifer species: Lodgepole pine (Pinus contorta var. latifolia) and jack pine (Pinus banksiana). Genome 56, 577–585. https://doi.org/10.1139/gen-2013-0071 (2013).Article 
    PubMed 
    CAS 

    Google Scholar 
    51.Diniz-Filho, J. et al. Mantel test in population genetics. Genet. Mol. Biol. 36, 475–485. https://doi.org/10.1590/S1415-47572013000400002 (2013).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Mantel, N. The detection of disease clustering and a generalized regression approach. Can. Res. 27, 209–220 (1967).CAS 

    Google Scholar 
    53.Vegan: Community ecology package v. R package version 2.5–3 (R package version 2.5–3). (2018).54.Excoffier, L., Smouse, P. & Quattro, J. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131, 479–491 (1992).Article 
    CAS 

    Google Scholar 
    55.Cornuet, J., Ravigné, V. & Estoup, A. Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinform. 11, 401–411. https://doi.org/10.1186/1471-2105-11-401 (2010).Article 
    CAS 

    Google Scholar 
    56.Cornuet, J. et al. DIYABC v2.0: A software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30, 1187–1189. https://doi.org/10.1093/bioinformatics/btt763 (2014).Article 
    PubMed 
    CAS 

    Google Scholar 
    57.Dickson, J. In Silvics of North America Vol. 2 (eds Burns, R. & Honkala, B.) 266–269 (United States Department of Agriculture-Forest Service, 1990).58.Thomson, A., Dick, C. & Dayanandan, S. A similar phylogeographical structure among sympatric North American birches (Betula) is better explained by introgression than by shared biogeographical history. J. Biogeogr. 42, 339–350. https://doi.org/10.1111/jbi.12394 (2015).Article 

    Google Scholar 
    59.Petit, R. et al. Glacial refugia: Hotspots but not melting pots of genetic diversity. Science 300, 1563–1565 (2003).ADS 
    Article 
    CAS 

    Google Scholar 
    60.David, R. & Hamann, A. Glacial refugia and modern genetic diversity of 22 western North American tree species. Proc. R. Soc. B Biol. Sci. 282, 20142903. https://doi.org/10.1098/rspb.2014.2903 (2015).Article 

    Google Scholar 
    61.Lumibao, C., Hoban, S. & McLachlan, J. Ice ages leave genetic diversity ‘hotspots’ in Europe but not in Eastern North America. Ecol. Lett. 20, 1459–1468. https://doi.org/10.1111/ele.12853 (2017).Article 
    PubMed 

    Google Scholar 
    62.Bialozyt, R., Ziegenhagen, B. & Petit, R. Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J. Evol. Biol. 19, 12–20. https://doi.org/10.1111/j.1420-9101.2005.00995.x (2006).Article 
    PubMed 
    CAS 

    Google Scholar 
    63.Petit, R. Early insights into the genetic consequences of range expansions. Heredity 106, 203–204. https://doi.org/10.1038/hdy.2010.60 (2011).Article 
    PubMed 
    CAS 

    Google Scholar 
    64.Dubreuil, M. et al. Genetic effects of chronic habitat fragmentation revisited: Strong genetic structure in a temperate tree, Taxus baccata (Taxaceae), with great dispersal capability. Am. J. Bot. 97, 303–310. https://doi.org/10.3732/ajb.0900148 (2010).Article 
    PubMed 

    Google Scholar 
    65.Hamrick, J., Godt, M. & Sherman-Broyles, S. In Population Genetics of Forest Trees Vol. 42 (eds Adams, W., Strauss, S., Copes, D. & Griffin, A) 95–124 (Springer, Dordrecht, 1992).66.Hamrick, J. & Godt, M. Effects of life history traits on genetic diversity in plant species. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 351, 1291–1298 (1996).ADS 
    Article 

    Google Scholar 
    67.Spaulding, H. & Rieske, L. The aftermath of an invasion: Structure and composition of central appalachian hemlock forests following establishment of the hemlock woolly adelgid, Aelges tsugae. Biol. Invasions 12, 3135–3143. https://doi.org/10.1007/s10530-010-9704-0 (2010).Article 

    Google Scholar 
    68.Hadziabdic, D. et al. Analysis of genetic diversity in flowering dogwood natural stands using microsatellites: The effects of dogwood anthracnose. Genetica 138, 1047–1057. https://doi.org/10.1007/s10709-010-9490-8 (2010).Article 
    PubMed 
    CAS 

    Google Scholar 
    69.Marquardt, P., Echt, C., Epperson, B. & Pubanz, D. Genetic structure, diversity, and inbreeding of eastern white pine under different management conditions. Can. J. For. Res. 37, 2652–2662 (2007).Article 
    CAS 

    Google Scholar 
    70.Potter, K. et al. Widespread inbreeding and unexpected geographic patterns of genetic variation in eastern hemlock (Tsuga canadensis), an imperiled North American conifer. Conserv. Genet. 13, 475–498. https://doi.org/10.1007/s10592-011-0301-2 (2012).Article 

    Google Scholar 
    71.Thammina, C., Kidwell-Slak, D., Lura, S. & Pooler, M. SSR markers reveal the genetic diversity of asian Cercis taxa at the US National Arboretum. HortScience 52, 498–502. https://doi.org/10.21273/hortsci11441-16 (2017).Article 

    Google Scholar 
    72.Chang, C., Bongarten, B. & Hamrick, J. Genetic structure of natural populations of black locust (Robinia pseudoacacia L.) at Coweeta, North Carolina. J. Plant Res. 111, 17–24. https://doi.org/10.1007/BF02507146.pdf (1998).Article 

    Google Scholar 
    73.Marquardt, P. & Epperson, B. Spatial and population genetic structure of microsatellites in white pine. Mol. Ecol. 13, 3305–3315. https://doi.org/10.1111/j.1365-294X.2004.02341.x (2004).Article 
    PubMed 
    CAS 

    Google Scholar 
    74.Victory, E., Glaubitz, J., Rhodes-Jr, O. & Woeste, K. Genetic homogeneity in Juglans nigra (Juglandaceae) at nuclear microsatellites. Am. J. Bot. 93, 118–126. https://doi.org/10.3732/ajb.93.1.118 (2006).Article 
    CAS 

    Google Scholar 
    75.Hadziabdic, D. et al. Genetic diversity of flowering dogwood in the Great Smoky Mountains National Park. Tree Genet. Genomes 8, 855–871. https://doi.org/10.1007/s11295-012-0471-1 (2012).Article 

    Google Scholar 
    76.Nybom, H. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol. Ecol. 13, 1143–1155. https://doi.org/10.1111/j.1365-294X.2004.02141.x (2004).Article 
    PubMed 
    CAS 

    Google Scholar 
    77.Donselman, H. Variation in native populations of eastern redbud (Cercis canadensis L.) as influenced by geographic location [USA]. In Proceedings, of the Florida State Horticulture Society Vol. 89. 370–373 (1976).78.Dirr, M. Manual of Woody Landscape Plants: Their Identification, Ornamental Characteristics, Culture, Propagation and Uses (Stipes Publishing Co, Champaign, 1990).
    Google Scholar 
    79.Fritsch, P., Schiller, A. & Larson, K. Taxonomic implications of morphological variation in Cercis canadensis (Fabaceae) from Mexico and adjacent parts of Texas. Syst. Bot. 34, 510–520. https://doi.org/10.1600/036364409789271254 (2009).Article 

    Google Scholar 
    80.Nevo, E. et al. Drought and light anatomical adaptive leaf strategies in three woody species caused by microclimatic selection at evolution canyon, Israel. Israel J. Plant Sci. 48, 33–46 (2000).
    Google Scholar 
    81.Fritsch, P. et al. Leaf adaptations and species boundaries in North American Cercis: Implications for the evolution of dry floras. Am. J. Bot. 105, 1577–1594. https://doi.org/10.1002/ajb2.1155 (2018).Article 
    PubMed 

    Google Scholar 
    82.Raulston, J. Redbud. Am. Nurseryman 171, 39–51 (1990).
    Google Scholar 
    83.Robertson, K. Cercis: The redbuds. Arnoldia 36, 37–49 (1976).
    Google Scholar 
    84.Davis, C., Fritsch, P., Li, J. & Donoghue, M. Phylogeny and biogeography of Cercis (Fabaceae): Evidence from nuclear ribosomal ITS and chloroplast ndhF sequence data. Syst. Bot. 27, 289–302. https://doi.org/10.1043/0363-6445-27.2.289 (2002).Article 

    Google Scholar 
    85.Hopkins, M. In Rhodora Vol. 44 (eds M Fernald, C Eatherby, L Griscom, & S Marris) 193–211 (New England Botanical Club, Inc., 1942).86.Griffin, J., Ranney, T. & Pharr, D. Heat and drought influence photosynthesis, water relations, and soluble carbohydrates of two ecotypes of redbud (Cercis canadensis). J. Am. Soc. Hortic. Sci. 129, 497–502. https://doi.org/10.21273/JASHS.129.4.0497 (2004).Article 
    CAS 

    Google Scholar 
    87.Fritsch, P. & Cruz, B. Phylogeny of Cercis based on DNA sequences of nuclear ITS and four plastid regions: Implications for transatlantic historical biogeography. Mol. Phylogenet. Evol. 62, 816–825. https://doi.org/10.1016/j.ympev.2011.11.016 (2012).Article 
    PubMed 

    Google Scholar 
    88.Chung, M., Chung, M., Oh, G. & Epperson, B. Spatial genetic structure in a Neolitsea sericea population (Lauraceae). Heredity 85, 490–497. https://doi.org/10.1046/j.1365-2540.2000.00781.x (2000).Article 
    PubMed 

    Google Scholar 
    89.Dean, D. et al. Analysis of genetic diversity and population structure for the native tree Viburnum rufidulum occurring in Kentucky and Tennessee. J. Am. Soc. Hortic. Sci. 140, 523–531. https://doi.org/10.21273/JASHS.140.6.523 (2015).Article 
    CAS 

    Google Scholar 
    90.Hagler, J., Mueller, S., Teuber, L., Machtley, S. & Van-Deynze, A. Foraging range of honey bees, Apis mellifera, in alfalfa seed production fields. J. Insect Sci. 11, 144. https://doi.org/10.1673/031.011.14401 (2011).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    91.Pasquet, R. et al. Long-distance pollesn flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proc. Natl. Acad. Sci. 105, 13456–13461 (2008).ADS 
    Article 

    Google Scholar 
    92.Hayden, W. Redbud seedpods hold surprises. Bull. Virginia Native Plant Soc. 32, 1–6 (2013).
    Google Scholar 
    93.Schnabel, A., Laushman, R. & Hamrick, J. Comparative genetic structure of two co-occurring tree species, Maclura pomifera (Moraceae) and Gleditsia triacanthos (Leguminosae). Heredity 67, 357–364. https://doi.org/10.1038/hdy.1991.99 (1991).Article 

    Google Scholar 
    94.Nakanishi, A., Tomaru, N., Yoshimaru, H., Manabe, T. & Yamamoto, S. Effects of seed- and pollen-mediated gene dispersal on genetic structure among Quercus salicina saplings. Heredity 102, 182–189. https://doi.org/10.1038/hdy.2008.101 (2008).Article 
    PubMed 
    CAS 

    Google Scholar 
    95.Vekemans, X. & Hardy, O. New insights from fine-scale spatial genetic structure analyses in plant populations. Mol. Ecol. 13, 921–935. https://doi.org/10.1046/j.1365-294X.2004.02076.x (2004).Article 
    PubMed 
    CAS 

    Google Scholar 
    96.Gonzales, E., Hamrick, J., Smouse, P., Trapnell, D. & Peakall, R. The impact of landscape disturbance on spatial genetic structure in the Guanacaste tree, Enterolobium cyclocarpum (Fabaceae). J. Hered. 101, 133–143. https://doi.org/10.1093/jhered/esp101 (2009).Article 
    PubMed 
    CAS 

    Google Scholar 
    97.Post, D. Change in nutrient content of foods stored by eastern woodrats (Neotoma floridana). J. Mammal. 73, 835–839 (1992).Article 

    Google Scholar 
    98.Surrency, D. & Owsley, C. (ed. Natural Resources Conservation Service United States Department of Agriculture) 146 (United States Department of Agriculture, Natural Resources Conservation Service, 2001).99.Wakeland, B. & Swihart, R. Ratings of white-tailed deer preferences for woody browse in Indiana. Proceedings of the Indiana Academy of Science 118, 96–101 (2009).
    Google Scholar 
    100.Wright, V., Fleming, E. & Post, D. Survival of Rhyzopertha dominica (Coleoptera, Bostrichidae) on fruits and seeds collected from woodrat nests in Kansas. J. Kansas Entomol. Soc. 63, 344–347 (1990).
    Google Scholar 
    101.Sullivan, J. (ed. Forest Service U.S. Department of Agriculture, Rocky Mountain Research Station) (U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. Fire Sciences Laboratory, 1994).102.Weir, B. & Ott, J. Genetic data analysis II. Trends Genet. 13, 379 (1997).Article 

    Google Scholar 
    103.Magni, C., Ducousso, A., Caron, H., Petit, R. & Kremer, A. Chloroplast DNA variation of Quercus rubra L. in North America and comparison with other Fagaceae. Mol. Ecol. 14, 513–524. https://doi.org/10.1111/j.1365-294X.2005.02400.x (2005).Article 
    PubMed 
    CAS 

    Google Scholar 
    104.Peterson, B. & Graves, W. Chloroplast phylogeography of Dirca palustris L. indicates populations near the glacial boundary at the Last Glacial Maximum in eastern North America. Journal of Biogeography 43, 314–327, doi:https://doi.org/10.1111/jbi.12621 (2016).105.Shaw, J. & Small, R. Chloroplast DNA phylogeny and phylogeography of the North American plums (Prunus subgenus Prunus section Prunocerasus, Rosaceae). Am. J. Bot. 92, 2011–2030. https://doi.org/10.3732/ajb.92.12.2011 (2005).Article 
    PubMed 
    CAS 

    Google Scholar 
    106.Rowe, K., Heske, E., Brown, P. & Paige, K. Surviving the ice: Northern refugia and postglacial colonization. Proc. Natl. Acad. Sci. 101, 10355–10359 (2004).ADS 
    Article 
    CAS 

    Google Scholar 
    107.Graignic, N., Tremblay, F. & Bergeron, Y. Influence of northern limit range on genetic diversity and structure in a widespread North American tree, sugar maple (Acer saccharum Marshall). Ecol. Evol. 8, 2766–2780. https://doi.org/10.1002/ece3.3906 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    108.Bemmels, J., Knowles, L. & Dick, C. Genomic evidence of survival near ice sheet margins for some, but not all, North American trees. Proc. Natl. Acad. Sci. 116, 8431–8436. https://doi.org/10.7302/Z2JS9NNG (2019).Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 
    109.Jia, H. & Steven, R. Fossil leaves and fruits of Cercis L. (Leguminosae) from the Eocene of western North America. International Journal of Plant Sciences 175, 601–612, doi:https://doi.org/10.1086/675693 (2014).110.Kraemer, M. & Favi, F. Emergence phenology of Osmia lignaria subsp lignaria (Hymenoptera: Megachilidae), its parasitoid Chrysura kyrae (Hymenoptera: Chrysididae), and bloom of Cercis canadensis. Environ. Entomol. 39, 351–358. https://doi.org/10.1603/en09242 (2010).Article 
    PubMed 
    CAS 

    Google Scholar 
    111.USDA. Census of horticultural specialties. Volume 3 AC-12-SS-3, Washington, DC (2014). More

  • in

    ‘I have to use a torch and watch my step’: netting seabirds at night

    Download PDF

    Netting seabirds is great fun. And it’s crucial for science and conservation.In this photo, taken in July, I’m heading out to capture birds on Inishtrahull, Ireland’s northernmost island. Lying about 10 kilometres northeast of the mainland, the island is home to thousands of seabirds during the summer nesting season, including storm petrels (Hydrobates pelagicus), Manx shearwaters (Puffinus puffinus) and fulmars (Fulmarus glacialis). The fulmars are experiencing a population crash, which I’m investigating.Migratory birds are protected here, but we need to know where they go when they leave their nests. I attach an identification band and a light-level geolocator — a sensor that helps to estimate location from day length — to every bird I catch. A few birds get GPS monitors, but we dole those out carefully, because each costs about £1,000 (US$1,368).The birds tend to nest on cliffs, and on a bad day I’ll catch just three. Some days I get as many as 12. Shearwaters are a challenge, because they nest only at night: I have to use a torch and watch my step.The birds don’t enjoy getting caught, but the stress is only temporary. The data they provide help us to understand their migration patterns. Fulmars spend almost their entire lives at sea. I’m interested in finding out how often they share waters with long-line fishers, which would be a potentially fatal scenario for the birds. That’s not the only threat: a study has found that more than half of beached North Sea fulmars have large amounts of plastic in their stomachs (see go.nature.com/3cosy8j).The lighthouse behind me is now home to the Inishtrahull Bird Observatory, a base for birdwatchers. I’m the founding chairman, but the observatory, part of a network of monitoring spots stretching 1,200 kilometres from Scotland to southern Ireland, will outlive me. It will be a centre for science and education for years to come.

    Nature 599, 340 (2021)
    doi: https://doi.org/10.1038/d41586-021-03055-8

    Related Articles

    Tracking Chernobyl’s effects on wildlife

    Preserving pieces of history in eggshells and birds’ nests

    Subjects

    Careers

    Ecology

    Ocean sciences

    Latest on:

    Careers

    Tips for managing an industry move without your academic supervisor’s support
    Career Feature 02 NOV 21

    When you recommend someone for an opportunity, follow through
    Career Column 29 OCT 21

    Cassyni aims to make online seminars more findable and citable
    Career News 28 OCT 21

    Ecology

    Whales’ gigantic appetites, climate fears — the week in infographics
    News 05 NOV 21

    COP26 climate pledges: What scientists think so far
    News 05 NOV 21

    Baleen whale prey consumption based on high-resolution foraging measurements
    Article 03 NOV 21

    Ocean sciences

    A whale of an appetite revealed by analysis of prey consumption
    News & Views 03 NOV 21

    Pliocene decoupling of equatorial Pacific temperature and pH gradients
    Article 20 OCT 21

    Mercury stable isotopes constrain atmospheric sources to the ocean
    Article 29 SEP 21

    Jobs

    Staff Scientist – RNA Biology

    Baylor College of Medicine (BCM)
    Houston, TX, United States

    Postdoctoral Associate-RNA Biology

    Baylor College of Medicine (BCM)
    Houston, TX, United States

    Postdoctoral Associate-RNA Biology

    Baylor College of Medicine (BCM)
    Houston, TX, United States

    Postdoctoral Associate-RNA Biology

    Baylor College of Medicine (BCM)
    Houston, TX, United States More

  • in

    Genomic characterization between strains selected for death-feigning duration for avoiding attack of a beetle

    The present study compared DNA sequences in a whole genome between the long strain and standard genome samples as references or the short strain and standard ones in T. castaneum. The results of resequencing analysis showed variations of DNA sequence from the reference sequence in both long and short strains, and the variations were detected more frequently in the long strain in a whole genome. Small nucleotide variants (SNV), multi-nucleotide variants (MNV), deletion, insertion, and replacement were detected in a whole genome in long and short strains. The same DNA sequence variants sharing between long and short strains were removed for the analyses. The numbers of small variants in total were larger in long strains than short strains (Fig. 1, Tables S1 and S2). The most frequent type of small variants was SNV, and the proportions of SNV were 82.7% (93,233/112,783) in long strains and 82.8% (13,817/16,697) in short strains, respectively (Fig. 1A). The SNVs compared with the reference nucleotide occurred frequently between adenine and guanine or cytosine and thymine in both long and short strains (Fig. 1B), and the frequencies were up to three times as large as other base combinations, indicating more frequent transition and fewer transversion variants. Deletion and insertion ranged from one to nine bases in both long and short strains, with one base was frequently deleted or inserted (Fig. 1C). Homozygosity presented more frequently than heterozygosity in all linkage groups, but the rate of homozygosity to heterozygosity depended on the linkage groups (Fig. 1D). Homozygosity of variants was more frequent in linkage groups 3 (LG3), 5 (LG5) and 7 (LG7) than other linkage groups in both strains. The ratios of homozygosity to heterozygosity were the largest in LGX and LG2 in long and short strains, respectively.Figure 1Analytical results of small variants of DNA sequence in a whole genome level in long and short strains. Proportion of small variants as SNV, MNV, deletion, insertion, and replacement in long and short strains (A). The numbers of small variants are indicated as the diameter of a pie graph. Frequencies of the SNVs in both long and short strains were compared with the reference nucleotide (B). Insertion and deletion ranged from one to nine bases in both long and short strains (C). Frequency of homozygosity or heterozygosity and its ratio in all linkage groups in long and short strains (D).Full size imageThe variants distributed in cording and non-cording regions. Figure 2A shows the results of narrowing down the variants in genic region from the variants in a whole genome in the long and short strains, and then aggregating the variants information in the exon, intron, URT and other regions. In all genic region, numbers of variants were larger in long strain than short strain. Then, genes containing these variants were counted in each strain (Fig. 2B). In exon region, genes with nonsynonymous variants were more numerous in the long strain (3243) than the short strain (844), and 464 common genes containing different DNA sequence variants between the strains were detected (Fig. 2B). In the genes with synonymous variants or the genes with variants in intron or UTR, the numbers of genes in long strain were constantly larger than those in short strain (Fig. 2B). The functions of long-unique, short-unique and common genes with variants were sorted into four categories by enrichment analyses as gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) ongoloty (KO) terms (Fig. 2C, Table S3). In the biological process, cellular component, and molecular function, and KEGG pathway, characteristics of nonsynonymous variants in long-unique, short-unique and common genes did not basically overlap among them, indicating specific selection of gene characteristics for each strain. Characteristics of synonymous variants were also sorted, but the synonymous variants may not influence the amino acid sequence of the gene and structure of the protein translated, rather these characteristics may be necessary to maintain the strain and preserved under artificial selection. Variants in intron and UTR may have potential effects on the gene expression, but should be investigated in detail in future study. Analyses of cis-regulatory elements might be important to understand regulation of gene expression, but the information on this region in T. castaneum is not available, therefore, the variants in cis-regulatory elements could not be analyzed.Figure 2Analytical results of the position of small variants in a whole genome in long and short strains (A) Numbers of variants in genic region including exon region, intron, UTR and other non-cording regions were indicated. As shown in parentheses, some ncRNAs and tRNAs were contained in exon, intron, and UTR regions. In short strain, there were five regions where two different genes overlap in 5′-UTR and 3′-UTR, respectively. Numbers of genes with variants in exon, intron and UTR regions in long and short strains (B). Numbers of long-unique, short-unique and common genes were shown by Venn diagrams. Common genes contain variants with different DNA sequences between long and short strains. Enrichment analyses of the function of genes with variants sorted into four categories (biological process, cellular component, molecular function, and KEGG pathway) (C). The heatmap is generated using the R package “gplots” (version 3.1.1, https://cran.r-project.org/web/packages/gplots/index.html). The list of each ontology shows the ID and term. The KO id is shown by a three- or four-letter organism code, the first-letter of the genus name and the first two- or three-letters of the species name of the scientific name of the organism, with pathway number. For example, Neuroactive ligand-receptor interaction of Tribolium castaneum is shown as “tca04080”.Full size imageTo explore the position of genes with variants associated with duration of death feigning in linkage groups, bulk segregant analysis was carried out (Fig. 3). The red approximate lines of the plot data crossed over the green threshold lines (P  More