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Experimental manipulation of microbiota reduces host thermal tolerance and fitness under heat stress in a vertebrate ectotherm

  • Paaijmans, K. P. et al. Temperature variation makes ectotherms more sensitive to climate change. Glob. Change Biol. 19, 2373–2380 (2013).

    Google Scholar 

  • Clusella-Trullas, S., Blackburn, T. M. & Chown, S. L. Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am. Nat. 177, 738–751 (2011).

    PubMed 

    Google Scholar 

  • Pounds, J. A. et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Sinervo, B. et al. Erosion of lizard diversity by climate change and altered thermal niches. Science 328, 894–899 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Pacifici, M. et al. Assessing species vulnerability to climate change. Nat. Clim. Change 5, 215–224 (2015).

    Google Scholar 

  • Angilletta, M. J. Jr Thermal Adaptation: A Theoretical and Empirical Synthesis (Oxford Univ. Press, 2009).

  • Sunday, J. M., Bates, A. E. & Dulvy, N. K. Global analysis of thermal tolerance and latitude in ectotherms. Proc. R. Soc. B 278, 1823–1830 (2011).

    PubMed 

    Google Scholar 

  • Jørgensen, L. B., Malte, H. & Overgaard, J. How to assess Drosophila heat tolerance: unifying static and dynamic tolerance assays to predict heat distribution limits. Funct. Ecol. 33, 629–642 (2019).

    Google Scholar 

  • Pörtner, H.-O., Bock, C. & Mark, F. C. Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology. J. Exp. Biol. 220, 2685–2696 (2017).

    PubMed 

    Google Scholar 

  • Gangloff, E. J. & Telemeco, R. S. High temperature, oxygen, and performance: insights from reptiles and amphibians. Integr. Comp. Biol. 58, 9–24 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • Perry, G. M., Danzmann, R. G., Ferguson, M. M. & Gibson, J. P. Quantitative trait loci for upper thermal tolerance in outbred strains of rainbow trout (Oncorhynchus mykiss). Heredity 86, 333–341 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Healy, T. M. & Schulte, P. M. Factors affecting plasticity in whole-organism thermal tolerance in common killifish (Fundulus heteroclitus). J. Comp. Physiol. B 182, 49–62 (2012).

    PubMed 

    Google Scholar 

  • Hu, X. P. & Appel, A. G. Seasonal variation of critical thermal limits and temperature tolerance in Formosan and eastern subterranean termites (Isoptera: Rhinotermitidae). Environ. Entomol. 33, 197–205 (2004).

    CAS 

    Google Scholar 

  • Nyamukondiwa, C. & Terblanche, J. S. Thermal tolerance in adult Mediterranean and Natal fruit flies (Ceratitis capitata and Ceratitis rosa): effects of age, gender and feeding status. J. Therm. Biol. 34, 406–414 (2009).

    Google Scholar 

  • Greenspan, S. E. et al. Infection increases vulnerability to climate change via effects on host thermal tolerance. Sci. Rep. 7, 9349 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Padfield, D., Castledine, M. & Buckling, A. Temperature-dependent changes to host–parasite interactions alter the thermal performance of a bacterial host. ISME J. 14, 389–398 (2020).

    PubMed 

    Google Scholar 

  • Hooper, L. V., Littman, D. R. & Macpherson, A. J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Goodrich, J. K. et al. Human genetics shape the gut microbiome. Cell 159, 789–799 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Alberdi, A., Aizpurua, O., Bohmann, K., Zepeda-Mendoza, M. L. & Gilbert, M. T. P. Do vertebrate gut metagenomes confer rapid ecological adaptation? Trends Ecol. Evol. 31, 689–699 (2016).

    PubMed 

    Google Scholar 

  • Kohl, K. D. & Carey, H. V. A place for host–microbe symbiosis in the comparative physiologist’s toolbox. J. Exp. Biol. 219, 3496–3504 (2016).

    PubMed 

    Google Scholar 

  • Fontaine, S. S. & Kohl, K. D. Optimal integration between host physiology and functions of the gut microbiome. Phil. Trans. R. Soc. B 375, 20190594 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Velagapudi, V. R. et al. The gut microbiota modulates host energy and lipid metabolism in mice. J. Lipid Res. 51, 1101–1112 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Donohoe, D. R. et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 13, 517–526 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Russell, J. A. & Moran, N. A. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. R. Soc. B 273, 603–610 (2006).

    PubMed 

    Google Scholar 

  • Montllor, C. B., Maxmen, A. & Purcell, A. H. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27, 189–195 (2002).

    Google Scholar 

  • Herrera, M. et al. Unfamiliar partnerships limit cnidarian holobiont acclimation to warming. Glob. Change Biol. 26, 5539–5553 (2020).

    Google Scholar 

  • Jaramillo, A. & Castaneda, L. E. Gut microbiota of Drosophila subobscura contributes to its heat tolerance and is sensitive to transient thermal stress. Front. Microbiol. 12, 886 (2021).

    Google Scholar 

  • Moghadam, N. N. et al. Strong responses of Drosophila melanogaster microbiota to developmental temperature. Fly 12, 1–12 (2018).

    PubMed 

    Google Scholar 

  • Fontaine, S. S., Novarro, A. J. & Kohl, K. D. Environmental temperature alters the digestive performance and gut microbiota of a terrestrial amphibian. J. Exp. Biol. 221, 187559 (2018).

    Google Scholar 

  • Kohl, K. D. & Yahn, J. Effects of environmental temperature on the gut microbial communities of tadpoles. Environ. Microbiol. 18, 1561–1565 (2016).

    PubMed 

    Google Scholar 

  • Fontaine, S. S. & Kohl, K. D. The gut microbiota of invasive bullfrog tadpoles responds more rapidly to temperature than a non‐invasive congener. Mol. Ecol. 29, 2449–2462 (2020).

    PubMed 

    Google Scholar 

  • Bestion, E. et al. Climate warming reduces gut microbiota diversity in a vertebrate ectotherm. Nat. Ecol. Evol. 1, 0161 (2017).

    Google Scholar 

  • Zhu, L. et al. Environmental temperatures affect the gastrointestinal microbes of the Chinese giant salamander. Front. Microbiol. 12, 493 (2021).

    Google Scholar 

  • Moeller, A. H. et al. The lizard gut microbiome changes with temperature and is associated with heat tolerance. Appl. Environ. Microbiol. 86, e01181-20 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kokou, F. et al. Host genetic selection for cold tolerance shapes microbiome composition and modulates its response to temperature. eLife 7, e36398 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hanage, W. P. Microbiology: microbiome science needs a healthy dose of scepticism. Nature 512, 247–248 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • Pascoe, E. L., Hauffe, H. C., Marchesi, J. R. & Perkins, S. E. Network analysis of gut microbiota literature: an overview of the research landscape in non-human animal studies. ISME J. 11, 2644–2651 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Mykles, D. L., Ghalambor, C. K., Stillman, J. H. & Tomanek, L. Grand challenges in comparative physiology: integration across disciplines and across levels of biological organization. Integr. Comp. Biol. 50, 6–16 (2010).

    PubMed 

    Google Scholar 

  • Kohl, K. D. A microbial perspective on the grand challenges in comparative animal physiology. mSystems 3, e00146-17 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Gray, K. T., Escobar, A. M., Schaeffer, P. J., Mineo, P. M. & Berner, N. J. Thermal acclimatization in overwintering tadpoles of the green frog, Lithobates clamitans (Latreille, 1801). J. Exp. Zool. A 325, 285–293 (2016).

    Google Scholar 

  • Brattstrom, B. H. & Lawrence, P. The rate of thermal acclimation in anuran amphibians. Physiol. Zool. 35, 148–156 (1962).

    Google Scholar 

  • Knutie, S. A., Wilkinson, C. L., Kohl, K. D. & Rohr, J. R. Early-life disruption of amphibian microbiota decreases later-life resistance to parasites. Nat. Commun. 8, 86 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Warne, R. W., Kirschman, L. & Zeglin, L. Manipulation of gut microbiota during critical developmental windows affects host physiological performance and disease susceptibility across ontogeny. J. Anim. Ecol. 88, 845–856 (2019).

    PubMed 

    Google Scholar 

  • Morgun, A. et al. Uncovering effects of antibiotics on the host and microbiota using transkingdom gene networks. Gut 64, 1732–1743 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Kohl, K. D., Cary, T. L., Karasov, W. H. & Dearing, M. D. Restructuring of the amphibian gut microbiota through metamorphosis. Environ. Microbiol. Rep. 5, 899–903 (2013).

    PubMed 

    Google Scholar 

  • Vences, M. et al. Gut bacterial communities across tadpole ecomorphs in two diverse tropical anuran faunas. Sci. Nat. 103, 25 (2016).

    Google Scholar 

  • Fontaine, S. S., Mineo, P. M. & Kohl, K. D. Changes in the gut microbial community of the eastern newt (Notophthalmus viridescens) across its three distinct life stages. FEMS Microbiol. Ecol. 97, fiab021 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Anderson, M. J. & Walsh, D. C. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol. Monogr. 83, 557–574 (2013).

    Google Scholar 

  • Sepulveda, J. & Moeller, A. H. The effects of temperature on animal gut microbiomes. Front. Microbiol. 11, 384 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Arango, R. A., Schoville, S. D., Currie, C. R. & Carlos-Shanley, C. Experimental warming reduces survival, cold tolerance, and gut prokaryotic diversity of the eastern subterranean termite, Reticulitermes flavipes (Kollar). Front. Microbiol. 12, 1116 (2021).

    Google Scholar 

  • Stothart, M. R. et al. Stress and the microbiome: linking glucocorticoids to bacterial community dynamics in wild red squirrels. Biol. Lett. 12, 20150875 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Zaneveld, J. R., McMinds, R. & Thurber, R. V. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2, 17121 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Orrock, J. L. & Watling, J. I. Local community size mediates ecological drift and competition in metacommunities. Proc. R. Soc. B 277, 2185–2191 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Deeg, C. M. et al. Chromulinavorax destructans, a pathogen of microzooplankton that provides a window into the enigmatic candidate phylum Dependentiae. PLoS Pathog. 15, e1007801 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kaboré, O. D., Godreuil, S. & Drancourt, M. Planctomycetes as host-associated bacteria: a perspective that holds promise for their future isolations, by mimicking their native environmental niches in clinical microbiology laboratories. Front. Cell. Infect. Microbiol. 10, 729 (2020).

    Google Scholar 

  • Sheremet, A. et al. Ecological and genomic analyses of candidate phylum WPS‐2 bacteria in an unvegetated soil. Environ. Microbiol. 22, 3143–3157 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Correa, D. T. et al. Multilevel community assembly of the tadpole gut microbiome. Preprint at bioRxiv https://doi.org/10.1101/2020.07.05.188698 (2020).

  • Contijoch, E. J. et al. Gut microbiota density influences host physiology and is shaped by host and microbial factors. eLife 8, e40553 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Warne, R. W., Kirschman, L. & Zeglin, L. Manipulation of gut microbiota reveals shifting community structure shaped by host developmental windows in amphibian larvae. Integr. Comp. Biol. 57, 786–794 (2017).

    PubMed 

    Google Scholar 

  • Trevelline, B. K., Fontaine, S. S., Hartup, B. K. & Kohl, K. D. Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc. R. Soc. B 286, 20182448 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Lutterschmidt, W. I. & Hutchison, V. H. The critical thermal maximum: history and critique. Can. J. Zool. 75, 1561–1574 (1997).

    Google Scholar 

  • Gosner, K. L. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190 (1960).

    Google Scholar 

  • Daloso, D. M. The ecological context of bilateral symmetry of organ and organisms. Nat. Sci. 6, 43340 (2014).

    Google Scholar 

  • Goldstein, J. A., Hoff, K. v. S. & Hillyard, S. D. The effect of temperature on development and behaviour of relict leopard frog tadpoles. Conserv. Physiol. 5, cow075 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Harkey, G. A. & Semlitsch, R. D. Effects of temperature on growth, development, and color polymorphism in the ornate chorus frog Pseudacris ornata. Copeia 1998, 1001–1007 (1988).

    Google Scholar 

  • Marian, M. & Pandian, T. Effect of temperature on development, growth and bioenergetics of the bullfrog tadpole Rana tigrina. J. Therm. Biol. 10, 157–161 (1985).

    Google Scholar 

  • Alvarez, D. & Nicieza, A. Effects of temperature and food quality on anuran larval growth and metamorphosis. Funct. Ecol. 16, 640–648 (2002).

    Google Scholar 

  • Kohl, K. D., Brun, A., Bordenstein, S. R., Caviedes‐Vidal, E. & Karasov, W. H. Gut microbes limit growth in house sparrow nestlings (Passer domesticus) but not through limitations in digestive capacity. Integr. Zool. 13, 139–151 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Potti, J. et al. Bacteria divert resources from growth for Magellanic penguin chicks. Ecol. Lett. 5, 709–714 (2002).

    Google Scholar 

  • Coates, M. E., Fuller, R., Harrison, G., Lev, M. & Suffolk, S. A comparison of the growth of chicks in the Gustafsson germ-free apparatus and in a conventional environment, with and without dietary supplements of penicillin. Br. J. Nutr. 17, 141–150 (1963).

    CAS 
    PubMed 

    Google Scholar 

  • Gaskins, H., Collier, C. & Anderson, D. Antibiotics as growth promotants: mode of action. Anim. Biotechnol. 13, 29–42 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Gitsels, A., Sanders, N. & Vanrompay, D. Chlamydial infection from outside to inside. Front. Microbiol. 10, 2329 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Denver, R. J. Proximate mechanisms of phenotypic plasticity in amphibian metamorphosis. Am. Zool. 37, 172–184 (1997).

    CAS 

    Google Scholar 

  • Chevalier, C. et al. Gut microbiota orchestrates energy homeostasis during cold. Cell 163, 1360–1374 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Khakisahneh, S., Zhang, X.-Y., Nouri, Z. & Wang, D.-H. Gut microbiota and host thermoregulation in response to ambient temperature fluctuations. mSystems 5, e00514–e00520 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Xie, B. et al. Chlamydomonas reinhardtii thermal tolerance enhancement mediated by a mutualistic interaction with vitamin B12-producing bacteria. ISME J. 7, 1544–1555 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gutiérrez‐Pesquera, L. M. et al. Testing the climate variability hypothesis in thermal tolerance limits of tropical and temperate tadpoles. J. Biogeogr. 43, 1166–1178 (2016).

    Google Scholar 

  • Litmer, A. R. & Murray, C. M. Critical thermal tolerance of invasion: comparative niche breadth of two invasive lizards. J. Therm. Biol. 86, 102432 (2019).

    PubMed 

    Google Scholar 

  • Semlitsch, R. D. Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Can. J. Zool. 68, 1027–1030 (1990).

    Google Scholar 

  • Cabrera-Guzmán, E., Crossland, M. R., Brown, G. P. & Shine, R. Larger body size at metamorphosis enhances survival, growth and performance of young cane toads (Rhinella marina). PLoS ONE 8, e70121 (2013).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Tejedo, M. Effects of body size and timing of reproduction on reproductive success in female natterjack toads (Bufo calamita). J. Zool. 228, 545–555 (1992).

    Google Scholar 

  • Warne, R. W., Crespi, E. J. & Brunner, J. L. Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles. Funct. Ecol. 25, 139–146 (2011).

    Google Scholar 

  • Urban, M. C. Accelerating extinction risk from climate change. Science 348, 571–573 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Pearce, T. A. & Paustian, M. E. Are temperate land snails susceptible to climate change through reduced altitudinal ranges? A Pennsylvania example. Am. Malacol. 31, 213–224 (2013).

    Google Scholar 

  • Wolfe, D. W. et al. Projected change in climate thresholds in the northeastern US: implications for crops, pests, livestock, and farmers. Mitig. Adapt. Strateg. Glob. Change 13, 555–575 (2008).

    Google Scholar 

  • Huey, R. B. & Kingsolver, J. G. Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4, 131–135 (1989).

    CAS 
    PubMed 

    Google Scholar 

  • Bennett, A. F. Thermal dependence of locomotor capacity. Am. J. Physiol. 259, R253–R258 (1990).

    CAS 
    PubMed 

    Google Scholar 

  • Seebacher, F. & Walter, I. Differences in locomotor performance between individuals: importance of parvalbumin, calcium handling and metabolism. J. Exp. Biol. 215, 663–670 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Husak, J. F., Fox, S. F., Lovern, M. B. & Bussche, R. A. V. D. Faster lizards sire more offspring: sexual selection on whole‐animal performance. Evolution 60, 2122–2130 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • Mineo, P. M., Waldrup, C., Berner, N. J. & Schaeffer, P. J. Differential plasticity of membrane fatty acids in northern and southern populations of the eastern newt (Notophthalmus viridescens). J. Comp. Physiol. B 189, 249–260 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Chung, D. J., Sparagna, G. C., Chicco, A. J. & Schulte, P. M. Patterns of mitochondrial membrane remodeling parallel functional adaptations to thermal stress. J. Exp. Biol. 221, 174458 (2018).

    Google Scholar 

  • Gladwell, R., Bowler, K. & Duncan, C. Heat death in crayfish Austropotamobius pallipes: ion movements and their effects on excitable tissues during heat death. J. Therm. Biol. 1, 79–94 (1976).

    CAS 

    Google Scholar 

  • Wang, Z. et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57–63 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pörtner, H. Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88, 137–146 (2001).

    PubMed 

    Google Scholar 

  • Gräns, A. et al. Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut. J. Exp. Biol. 217, 711–717 (2014).

    PubMed 

    Google Scholar 

  • Jutfelt, F. et al. Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology. J. Exp. Biol. 221, 169615 (2018).

    Google Scholar 

  • St-Pierre, J., Charest, P.-M. & Guderley, H. Relative contribution of quantitative and qualitative changes in mitochondria to metabolic compensation during seasonal acclimatisation of rainbow trout Oncorhynchus mykiss. J. Exp. Biol. 201, 2961–2970 (1998).

    CAS 

    Google Scholar 

  • Grim, J., Miles, D. & Crockett, E. Temperature acclimation alters oxidative capacities and composition of membrane lipids without influencing activities of enzymatic antioxidants or susceptibility to lipid peroxidation in fish muscle. J. Exp. Biol. 213, 445–452 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • LeMoine, C. M., Genge, C. E. & Moyes, C. D. Role of the PGC-1 family in the metabolic adaptation of goldfish to diet and temperature. J. Exp. Biol. 211, 1448–1455 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • McClelland, G. B., Craig, P. M., Dhekney, K. & Dipardo, S. Temperature‐ and exercise‐induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J. Physiol. 577, 739–751 (2006).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pichaud, N. et al. Cardiac mitochondrial plasticity and thermal sensitivity in a fish inhabiting an artificially heated ecosystem. Sci. Rep. 9, 17832 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Seebacher, F., Guderley, H., Elsey, R. M. & Trosclair, P. L. Seasonal acclimatisation of muscle metabolic enzymes in a reptile (Alligator mississippiensis). J. Exp. Biol. 206, 1193–1200 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • Berner, N. J. & Bessay, E. P. Correlation of seasonal acclimatization in metabolic enzyme activity with preferred body temperature in the eastern red spotted newt (Notophthalmus viridescens viridescens). Comp. Biochem. Physiol. A 144, 429–436 (2006).

    Google Scholar 

  • Vigelsø, A., Andersen, N. B. & Dela, F. The relationship between skeletal muscle mitochondrial citrate synthase activity and whole body oxygen uptake adaptations in response to exercise training. Int. J. Physiol. Pathophysiol. Pharmacol. 6, 84–101 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Li, Y., Park, J.-S., Deng, J.-H. & Bai, Y. Cytochrome c oxidase subunit IV is essential for assembly and respiratory function of the enzyme complex. J. Bioenerg. Biomembr. 38, 283–291 (2006).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pryor, G. S. & Bjorndal, K. A. Symbiotic fermentation, digesta passage, and gastrointestinal morphology in bullfrog tadpoles (Rana catesbeiana). Physiol. Biochem. Zool. 78, 201–215 (2005).

    PubMed 

    Google Scholar 

  • Clark, A. & Mach, N. The crosstalk between the gut microbiota and mitochondria during exercise. Front. Physiol. 8, 319 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Payne, N. L. et al. Temperature dependence of fish performance in the wild: links with species biogeography and physiological thermal tolerance. Funct. Ecol. 30, 903–912 (2016).

    Google Scholar 

  • Van Dijk, P., Tesch, C., Hardewig, I. & Portner, H. Physiological disturbances at critically high temperatures: a comparison between stenothermal Antarctic and eurythermal temperate eelpouts (Zoarcidae). J. Exp. Biol. 202, 3611–3621 (1999).

    PubMed 

    Google Scholar 

  • Schulte, P. M. The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment. J. Exp. Biol. 218, 1856–1866 (2015).

    PubMed 

    Google Scholar 

  • Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Hoppeler, H. & Weibel, E. R. Scaling functions to body size: theories and facts. J. Exp. Biol. 208, 1573–1574 (2005).

    PubMed 

    Google Scholar 

  • Hopkins, W. A., Rowe, C. L. & Congdon, J. D. Elevated trace element concentrations and standard metabolic rate in banded water snakes (Nerodia fasciata) exposed to coal combustion wastes. Environ. Toxicol. Chem. 18, 1258–1263 (1999).

    CAS 

    Google Scholar 

  • Sokolova, I. Bioenergetics in environmental adaptation and stress tolerance of aquatic ectotherms: linking physiology and ecology in a multi-stressor landscape. J. Exp. Biol. 224, 236802 (2021).

    Google Scholar 

  • Sokolova, I. M. & Lannig, G. Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: implications of global climate change. Clim. Res. 37, 181–201 (2008).

    Google Scholar 

  • Peralta-Maraver, I. & Rezende, E. L. Heat tolerance in ectotherms scales predictably with body size. Nat. Clim. Change 11, 58–63 (2021).

    Google Scholar 

  • Bahrndorff, S., Alemu, T., Alemneh, T. & Lund Nielsen, J. The microbiome of animals: implications for conservation biology. Int. J. Genomics 2016, 5304028 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hauffe, H. C. & Barelli, C. Conserve the germs: the gut microbiota and adaptive potential. Conserv. Genet. 20, 19–27 (2019).

    Google Scholar 

  • Jiménez, R. R. & Sommer, S. The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers. Conserv. 26, 763–786 (2017).

    Google Scholar 

  • Swaddle, J. P. Fluctuating asymmetry, animal behavior, and evolution. Adv. Study Behav. 32, 169–205 (2003).

    Google Scholar 

  • R Core Team R: A Language and Environment for Statistical Computing v.3.4.3 (R Foundation for Statistical Computing, 2019).

  • Bates, D., Machler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. Preprint at https://arxiv.org/abs/1406.5823 (2014).

  • Pinheiro, J. et al. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3 (2017).

  • Hulbert, A., Pamplona, R., Buffenstein, R. & Buttemer, W. Life and death: metabolic rate, membrane composition, and life span of animals. Physiol. Rev. 87, 1175–1213 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Oksanen, J. et al. vegan: Community Ecology Package. R package version 2 (2013).

  • Mary-Huard, T., Daudin, J.-J., Baccini, M., Biggeri, A. & Bar-Hen, A. Biases induced by pooling samples in microarray experiments. Bioinformatics 23, i313–i318 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Singer, J. D. & Willett, J. B. It’s about time: using discrete-time survival analysis to study duration and the timing of events. J. Educ. Stat. 18, 155–195 (1993).

    Google Scholar 

  • Mallick, H. et al. Multivariable association discovery in population-scale meta-omics studies. PLoS Comput. Biol. 17, e100442 (2021).

    Google Scholar 


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