Heat over heritability: Increasing body size in response to global warming is not stabilized by genetic effects in Bechstein's bats.

Bayesian animal model chiroptera climate change evolutionary potential extinction risk heritability phenotypic plasticity

Journal

Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 21 10 2022
accepted: 17 05 2023
pubmed: 21 6 2023
medline: 21 6 2023
entrez: 21 6 2023
Statut: ppublish

Résumé

How well populations can cope with global warming will often depend on the evolutionary potential and plasticity of their temperature-sensitive, fitness-relevant traits. In Bechstein's bats (Myotis bechsteinii), body size has increased over the last decades in response to warmer summers. If this trend continues it may threaten populations as larger females exhibit higher mortality. To assess the evolutionary potential of body size, we applied a Bayesian 'animal model' to estimate additive genetic variance, heritability and evolvability of body size, based on a 25-year pedigree of 332 wild females. Both heritability and additive genetic variance were reduced in hot summers compared to average and cold summers, while evolvability of body size was generally low. This suggests that the observed increase in body size was mostly driven by phenotypic plasticity. Thus, if warm summers continue to become more frequent, body size likely increases further and the resulting fitness loss could threaten populations.

Identifiants

pubmed: 37340689
doi: 10.1111/gcb.16824
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4939-4948

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : RTG 2010

Informations de copyright

© 2023 The Authors. Global Change Biology published by John Wiley & Sons Ltd.

Références

Alston, J. M., Dillon, M. E., Keinath, D. A., Abernethy, I. M., & Goheen, J. R. (2022). Daily torpor reduces the energetic consequences of microhabitat selection for a widespread bat. Ecology, 103, e3677. https://doi.org/10.1002/ecy.3677
Ballinger, M. A., & Nachman, M. W. (2022). The contribution of genetic and environmental effects to Bergmann's rule and Allen's rule in house mice. The American Naturalist, 199(5), 691-704. https://doi.org/10.1086/719028
Bohnenstengel, T. (2012). Roost selection by the forest-dwelling bat Myotis bechsteinii (Mammalia: Chiroptera): Implications for its conservation in managed forests. Bulletin de La Societe Neuchâteloise des Sciences Naturelles, 132(January), 47-62.
Cava, J. A., Perlut, N. G., & Travis, S. E. (2019). Heritability and evolvability of morphological traits of Savannah sparrows (Passerculus sandwichensis) breeding in agricultural grasslands. PLoS One, 14(1), 1-10. https://doi.org/10.1371/journal.pone.0210472
Chapuis, M., Pélissié, B., Piou, C., Chardonnet, F., Pagès, C., Foucart, A., Chapuis, E., & Jourdan-Pineau, H. (2021). Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregaria. Ecology and Evolution, 11(20), 13930-13947. https://doi.org/10.1002/ece3.8099
Charmantier, A., & Garant, D. (2005). Environmental quality and evolutionary potential: Lessons from wild populations. Proceedings of the Royal Society B: Biological Sciences, 272(1571), 1415-1425. https://doi.org/10.1098/rspb.2005.3117
Chevin, L. M., Lande, R., & Mace, G. M. (2010). Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLoS Biology, 8(4), e1000357. https://doi.org/10.1371/journal.pbio.1000357
de Villemereuil, P. (2018). Quantitative genetic methods depending on the nature of the phenotypic trait. Annals of the New York Academy of Sciences, 1422(1), 29-47. https://doi.org/10.1111/nyas.13571
de Villemereuil, P., Morrissey, M. B., Nakagawa, S., & Schielzeth, H. (2018). Fixed-effect variance and the estimation of repeatabilities and heritabilities: Issues and solutions. Journal of Evolutionary Biology, 31(4), 621-632. https://doi.org/10.1111/jeb.13232
Fischer, K., Kreyling, J., Beaulieu, M., Beil, I., Bog, M., Bonte, D., Holm, S., Knoblauch, S., Koch, D., Muffler, L., Mouginot, P., Paulinich, M., Scheepens, J. F., Schiemann, R., Schmeddes, J., Schnittler, M., Uhl, G., van der Maaten-Theunissen, M., Weier, J. M., … Gienapp, P. (2021). Species-specific effects of thermal stress on the expression of genetic variation across a diverse group of plant and animal taxa under experimental conditions. Heredity, 126(1), 23-37. https://doi.org/10.1038/s41437-020-0338-4
Fleischer, T., Gampe, J., Scheuerlein, A., & Kerth, G. (2017). Rare catastrophic events drive population dynamics in a bat species with negligible senescence. Scientific Reports, 7(1), 1-9. https://doi.org/10.1038/s41598-017-06392-9
Green, W. C. H., & Rothstein, A. (1991). Trade-offs between growth and reproduction in female bison. Oecologia, 86(4), 521-527. https://doi.org/10.1007/BF00318318
Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33(2), 1-22. https://doi.org/10.18637/jss.v033.i02
Hoffmann, A. A., & Merilä, J. (1999). Heritable variation and evolution under favourable and unfavourable conditions. Trends in Ecology & Evolution, 14(3), 96-101.
Hoffmann, A. A., & Sgró, C. M. (2011). Climate change and evolutionary adaptation. Nature, 470(7335), 479-485. https://doi.org/10.1038/nature09670
Houle, D. (1992). Comparing evolvability and variability of quantitative traits. Genetics, 130(1), 195-204. https://doi.org/10.1093/genetics/130.1.195
IPCC. (2021). Climate Change 2021: The physical science basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press. https://doi.org/10.1017/9781009157896
Kalinowski, S. T., Taper, M. L., & Marshall, T. C. (2007). Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16(5), 1099-1106. https://doi.org/10.1111/j.1365-294X.2007.03089.x
Kerth, G. (2022). Long-term field studies in bat research: Importance for basic and applied research questions in animal behavior. Behavioral Ecology and Sociobiology, 76, 75.
Kerth, G., & König, B. (1999). Fission, fusion and nonrandom associations in female Bechstein's bats (Myotis bechsteinii). Behaviour, 136(9), 1187-1202. https://doi.org/10.1163/156853999501711
Kerth, G., Mayer, F., & König, B. (2000). Mitochondrial DNA (mtDNA) reveals that female Bechstein's bats live in closed societies. Molecular Ecology, 9(6), 793-800. https://doi.org/10.1046/j.1365-294X.2000.00934.x
Kerth, G., & Morf, L. (2004). Behavioural and genetic data suggest that Bechstein's bats predominantly mate outside the breeding habitat. Ethology, 110(12), 987-999. https://doi.org/10.1111/j.1439-0310.2004.01040.x
Kerth, G., Perony, N., & Schweitzer, F. (2011). Bats are able to maintain long-term social relationships despite the high fission-fusion dynamics of their groups. Proceedings of the Royal Society B: Biological Sciences, 278(1719), 2761-2767. https://doi.org/10.1098/rspb.2010.2718
Kerth, G., Safi, K., & König, B. (2002). Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein's bat (Myotis bechsteinii). Behavioral Ecology and Sociobiology, 52(3), 203-210. https://doi.org/10.1007/s00265-002-0499-6
Kerth, G., & Van Schaik, J. (2012). Causes and consequences of living in closed societies: Lessons from a long-term socio-genetic study on Bechstein's bats. Molecular Ecology, 21(3), 633-646. https://doi.org/10.1111/j.1365-294X.2011.05233.x
Kerth, G., Weissmann, K., & König, B. (2001). Day roost selection in female Bechstein's bats (Myotis bechsteinii): A field experiment to determine the influence of roost temperature. Oecologia, 126(1), 1-9. https://doi.org/10.1007/s004420000489
Kruuk, L. E. B. (2004). Estimating genetic parameters in natural populations using the "animal model". Philosophical Transactions of the Royal Society B: Biological Sciences, 359(1446), 873-890. https://doi.org/10.1098/rstb.2003.1437
Kruuk, L. E. B., Clutton-Brock, T. H., Rose, K. E., & Guinness, F. E. (1999). Early determinants of lifetime reproductive success differ between the sexes in red deer. Proceedings of the Royal Society B: Biological Sciences, 266(1429), 1655-1661. https://doi.org/10.1098/rspb.1999.0828
Kruuk, L. E. B., Slate, J., & Wilson, A. J. (2008). New answers for old questions: The evolutionary quantitative genetics of wild animal populations. Annual Review of Ecology, Evolution, and Systematics, 39(1), 525-548. https://doi.org/10.1146/annurev.ecolsys.39.110707.173542
Malenfant, R. M., Davis, C. S., Richardson, E. S., Lunn, N. J., & Coltman, D. W. (2018). Heritability of body size in the polar bears of Western Hudson Bay. Molecular Ecology Resources, 18, 854-866. https://doi.org/10.1111/1755-0998.12889
Meng, F., Zhu, L., Huang, W., Irwin, D. M., & Zhang, S. (2016). Bats: Body mass index, forearm mass index, blood glucose levels and SLC2A2 genes for diabetes. Scientific Reports, 6(July), 1-12. https://doi.org/10.1038/srep29960
Morrissey, M. B., & Wilson, A. J. (2010). Pedantics: An R package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing. Molecular Ecology Resources, 10(4), 711-719. https://doi.org/10.1111/j.1755-0998.2009.02817.x
Mundinger, C., Fleischer, T., Scheuerlein, A., & Kerth, G. (2022). Global warming leads to larger bats with a faster life history pace in the long-lived Bechstein's bat (Myotis bechsteinii). Communications Biology, 5(1), 682. https://doi.org/10.1038/s42003-022-03611-6
Mundinger, C., Scheuerlein, A., & Kerth, G. (2021). Long-term study shows that increasing body size in response to warmer summers is associated with a higher mortality risk in a long-lived bat species. Proceedings of the Royal Society B: Biological Sciences, 288(1952), 20210508. https://doi.org/10.1098/rspb.2021.0508
Petrov, B., Jasja, D., Suren, G., Hamidovic, D., Javier, J., Julia, H., Meelis, L., & Ferdia, M. (2018). Action plan for the conservation of all bat species in the European Union, October, 1-74. https://www.eurobats.org/sites/default/files/documents/news/EU%20Bats%20Action%20Plan_Complementary%20document.pdf
Postma, E. (2014). Four decades of estimating heritabilities in wild vertebrate populations: Improved methods, more data, better estimates? In A. Charmantier, D. Garant, & L. Kruuk (Eds.), Quantitative genetics in the wild (pp. 16-33). Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199674237.003.0002
Pretzlaff, I., Kerth, G., & Dausmann, K. H. (2010). Communally breeding bats use physiological and behavioural adjustments to optimise daily energy expenditure. Naturwissenschaften, 97(4), 353-363. https://doi.org/10.1007/s00114-010-0647-1
R Core Development Team. (2021). A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.r-project.org
Racey, P. A. (1973). Environmental factors affecting the length of gestation in heterothermic bats. Journal of Reproduction and Fertility. Supplement, 19(January), 175-189.
Racey, P. A., & Swift, S. M. (1981). Variations in gestation length in a colony of pipistrelle bats (Pipistrellus pipistrellus) from year to year. Journal of Reproduction and Fertility, 61(1), 123-129. https://doi.org/10.1530/jrf.0.0610123
Radchuk, V., Reed, T., Teplitsky, C., van de Pol, M., Charmantier, A., Hassall, C., Adamík, P., Adriaensen, F., Ahola, M. P., Arcese, P., Miguel Avilés, J., Balbontin, J., Berg, K. S., Borras, A., Burthe, S., Clobert, J., Dehnhard, N., de Lope, F., Dhondt, A. A., … Kramer-Schadt, S. (2019). Adaptive responses of animals to climate change are most likely insufficient. Nature Communications, 10(1), 1-14. https://doi.org/10.1038/s41467-019-10924-4
Rowiński, P. K., & Rogell, B. (2017). Environmental stress correlates with increases in both genetic and residual variances: A meta-analysis of animal studies. Evolution, 71(5), 1339-1351. https://doi.org/10.1111/evo.13201
Rubalcaba, J. G., Gouveia, S. F., Villalobos, F., Cruz-Neto, A. P., Castro, M. G., Amado, T. F., Martinez, P. A., Navas, C. A., Dobrovolski, R., Diniz-Filho, J. A. F., & Olalla-Tárraga, M. (2022). Physical constraints on thermoregulation and flight drive morphological evolution in bats. Proceedings of the National Academy of Sciences of the United States of America, 119(15), e2103745119. https://doi.org/10.1073/pnas.2103745119
Teplitsky, C., Mills, J. A., Yarrall, J. W., & Merilä, J. (2009). Heritability of fitness components in a wild bird population. Evolution, 63(3), 716-726. https://doi.org/10.1111/j.1558-5646.2008.00581.x
Visscher, P. M., Hill, W. G., & Wray, N. R. (2008). Heritability in the genomics era-Concepts and misconceptions. Nature Reviews Genetics, 9(4), 255-266. https://doi.org/10.1038/nrg2322
Wang, J. (2011). coancestry: A program for simulating, estimating and analysing relatedness and inbreeding coefficients. Molecular Ecology Resources, 11(1), 141-145. https://doi.org/10.1111/j.1755-0998.2010.02885.x
Welti, E. A. R., Zajicek, P., Frenzel, M., Ayasse, M., Bornholdt, T., Buse, J., Classen, A., Dziock, F., Engelmann, R. A., Englmeier, J., Fellendorf, M., Förschler, M. I., Fricke, U., Ganuza, C., Hippke, M., Hoenselaar, G., Kaus-Thiel, A., Kerner, J., Kilian, D., … Haase, P. (2021). Temperature drives variation in flying insect biomass across a German malaise trap network. Insect Conservation and Diversity, 15(2), 168-180. https://doi.org/10.1111/icad.12555
Williams, S. E., Shoo, L. P., Isaac, J. L., Hoffmann, A. A., & Langham, G. (2008). Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biology, 6(12), 2621-2626. https://doi.org/10.1371/journal.pbio.0060325
Willis, C. K. R., & Brigham, R. M. (2005). Physiological and ecological aspects of roost selection by reproductive female hoary bats (Lasiurus cinereus). Journal of Mammalogy, 86(1), 85-94. https://doi.org/10.1644/1545-1542(2005)086<0085:PAEAOR>2.0.CO;2
Willis, C. K. R., Brigham, R. M., & Geiser, F. (2006). Deep, prolonged torpor by pregnant, free-ranging bats. Naturwissenschaften, 93(2), 80-83. https://doi.org/10.1007/s00114-005-0063-0
Wilson, A. J. (2008). Why h2 does not always equal VA/VP? Journal of Evolutionary Biology, 21(3), 647-650. https://doi.org/10.1111/j.1420-9101.2008.01500.x
Wilson, A. J., & Poissant, J. (2016). Quantitative genetics in natural populations. In R. Kliman (Ed.), Encyclopedia of evolutionary biology (Vol. 3, pp. 361-371). Academic Press. https://doi.org/10.1016/B978-0-12-800049-6.00046-9
Wilson, A. J., Réale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., Kruuk, L. E. B., & Nussey, D. H. (2010). An ecologist's guide to the animal model. Journal of Animal Ecology, 79(1), 13-26. https://doi.org/10.1111/j.1365-2656.2009.01639.x
Wray, N., & Visscher, P. (2008). Estimating trait heritability. Nature Education, 1(1), 3-5.

Auteurs

Carolin Mundinger (C)

Applied Zoology and Nature Conservation, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany.

Jaap van Schaik (J)

Applied Zoology and Nature Conservation, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany.

Alexander Scheuerlein (A)

Applied Zoology and Nature Conservation, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany.

Gerald Kerth (G)

Applied Zoology and Nature Conservation, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany.

Classifications MeSH