Strong phenotypic trait correlations between mating partners do not result from assortative mating in wild great tits (Parus major).
assortative mating
indirect effects
multivariate mixed model
repeatability
variance partitioning
Journal
Journal of evolutionary biology
ISSN: 1420-9101
Titre abrégé: J Evol Biol
Pays: Switzerland
ID NLM: 8809954
Informations de publication
Date de publication:
04 2022
04 2022
Historique:
revised:
10
07
2021
received:
09
10
2020
accepted:
15
07
2021
pubmed:
31
7
2021
medline:
15
4
2022
entrez:
30
7
2021
Statut:
ppublish
Résumé
There is considerable debate about the occurrence of assortative mating between phenotypic traits measured within natural populations. Meta-analyses have implied that assortative mating occurs generally in natural populations, but recent work indicates these conclusions largely result from biased data. Specifically, estimates of phenotypic correlations between mating partners do not solely result from nonrandom associations between individual-level traits of partners but also from other biological processes (joint phenotypic plasticity, indirect genetic effects), methodological practices (observer bias) and other unexplained residual correlations (e.g. correlated measurement error). This paper puts this critique to test. First, we estimated the overall phenotypic correlation between phenotypic traits of mating partners for a wild population of great tits. Second, we estimated various key variance components to reveal the extent to which phenotypic correlations between partners resulted from assortative mating, reversible plasticity, social partner effects and methodological practices. We performed our analyses for a range of phenotypic traits (body mass, breathing rate, exploration behaviour, wing and tarsus length) to derive general conclusions not hinging on the specifics of the traits involved. Our analyses support the conclusion that patterns of assortative mating exist at first glance but occur because of the biasing effects of correlated residuals likely caused by a combination of phenotypic responses to unknown environmental factors or measurement error-not because of intrinsic patterns of assortative mating.
Banques de données
Dryad
['10.5061/dryad.1vhhmgqt9']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
552-560Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : DI 1694/1-1
Organisme : Deutsche Forschungsgemeinschaft
ID : HO 6288/1-1
Organisme : Max-Planck-Society
Informations de copyright
© 2021 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.
Références
Araya-Ajoy, Y. G., Westneat, D. F., & Wright, J. (2020). Pathways to social evolution and their evolutionary feedbacks. Evolution, 74, 1894-1907. https://doi.org/10.1111/evo.14054
Bailey, N. W., Marie-Orleach, L., & Moore, A. J. (2018). Indirect genetic effects in behavioral ecology: Does behavior play a special role in evolution? Behavioral Ecology, 29, 1-11. https://doi.org/10.1093/beheco/arx127
Both, C., Dingemanse, N. J., Drent, P. J., & Tinbergen, J. M. (2005). Pairs of extreme avian personalities have highest reproductive success. Journal of Animal Ecology, 74, 667-674. https://doi.org/10.1111/j.1365-2656.2005.00962.x
Brommer, J. E. (2013). Variation in plasticity of personality traits implies that the ranking of personality measures changes between environmental contexts: Calculating the cross-environmental correlation. Behavioral Ecology and Sociobiology, 67, 1709-1718. https://doi.org/10.1007/s00265-013-1603-9
Burghardt, G. M., Bartmess-LeVasseur, J. N., Browning, S. A., Morrison, K. E., Stec, C. L., Zachau, C. E., & Freeberg, T. M. (2012). Perspectives - minimizing observer bias in behavioral studies: A review and recommendations: Minimizing observer bias in behavioral research. Ethology, 118, 511-517. https://doi.org/10.1111/j.1439-0310.2012.02040.x
Class, B., & Brommer, J. E. (2018). Shared environmental effects bias phenotypic estimates of assortative mating in a wild bird. Biology Letters, 14(7), 20180106-https://doi.org/10.1098/rsbl.2018.0106
Class, B., Dingemanse, N. J., Araya-Ajoy, Y. G., & Brommer, J. E. (2017). A statistical methodology for estimating assortative mating for phenotypic traits that are labile or measured with error. Methods in Ecology and Evolution, 8, 1910-1919. https://doi.org/10.1111/2041-210X.12837
Clutton-Brock, T., & Sheldon, B. C. (2010). Individuals and populations: The role of long-term, individual-based studies of animals in ecology and evolutionary biology. Special Issue: Long-term Ecological Research, 25, 562-573.
Crespi, B. J. (1989). Causes of assortative mating in arthropods. Animal Behavior, 38, 980-1000. https://doi.org/10.1016/S0003-3472(89)80138-1
Culina, A., Adriaensen, F., Bailey, L. D., Burgess, M. D., Charmantier, A., Cole, E. F., Eeva, T., Matthysen, E., Nater, C. R., Sheldon, B. C., Saether, B. E., Vriend, S. J. G., Zajkova, Z., Adamík, P., Aplin, L. M., Angulo, E., Artemyev, A., Barba, E., Barišić, S., … Visser, M. E. (2020). Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub. Journal of Animal Ecology, 1-13.
Dingemanse, N. J., & Araya-Ajoy, Y. G. (2015). Interacting personalities: Behavioural ecology meets quantitative genetics. Trends in Ecology & Evolution, 30, 88-97. https://doi.org/10.1016/j.tree.2014.12.002
Dingemanse, N. J., Class, B., & Holtmann, B. (2021). Nonrandom mating for behavior in the wild? Trends in Ecology & Evolution, 36, 177-179. https://doi.org/10.1016/j.tree.2020.11.007
Dingemanse, N. J., & Dochtermann, N. A. (2013). Quantifying individual variation in behaviour: Mixed-effect modelling approaches. Journal of Animal Ecology, 82, 39-54. https://doi.org/10.1111/1365-2656.12013
Dingemanse, N. J., Dochtermann, N. A., & Nakagawa, S. (2012). Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behavioral Ecology and Sociobiology, 66, 1543-1548. https://doi.org/10.1007/s00265-012-1416-2
Dingemanse, N. J., Moiron, M., Araya-Ajoy, Y. G., Mouchet, A., & Abbey-Lee, R. N. (2020). Individual variation in age-dependent reproduction: Fast explorers live fast but senesce young? Journal of Animal Ecology, 89(2), 601-613. https://doi.org/10.1111/1365-2656.13122
Edelaar, P., Siepielski, A. M., & Clobert, J. (2008). Matching habitat choice causes directed gene flow: A neglected dimension in evolution and ecology. Evolution, 62, 2462-2472. https://doi.org/10.1111/j.1558-5646.2008.00459.x
Guay, P.-J., McLeod, E. M., Cross, R., Formby, A. J., Maldonado, S. P., Stafford-Bell, R. E., St-James-Turner, Z. N., Robinson, R. W., Mulder, R. A., & Weston, M. A. (2013). Observer effects occur when estimating alert but not flight-initiation distances. Wildlife Research, 40, 289-293. https://doi.org/10.1071/WR13013
Hadfield, J. D. (2010). MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. 2010 33: 22.
Holtmann, B., Santos, E. S. A., Lara, C. E., & Nakagawa, S. (2017). Personality-matching habitat choice, rather than behavioural plasticity, is a likely driver of a phenotype-environment covariance. Proceedings of the Royal Society B: Biological Sciences, 284: 20170943.
Ihle, M., Kempenaers, B., & Forstmeier, W. (2015). Fitness benefits of mate choice for compatibility in a socially monogamous species. PLoS Biology, 13, e1002248. https://doi.org/10.1371/journal.pbio.1002248
Janicke, T., Marie-Orleach, L., Aubier, T. G., Perrier, C., & Morrow, E. H. (2019). Assortative mating in animals and its role for speciation. The American Naturalist, 194, 865-875. https://doi.org/10.1086/705825
Jiang, Y., Bolnick, D. I., & Kirkpatrick, M. (2013). Assortative mating in animals. The American Naturalist, 181, E125-E138. https://doi.org/10.1086/670160
Kopp, M., Servedio, M. R., Mendelson, T. C., Safran, R. J., Rodríguez, R. L., Hauber, M. E., Scordato, E. C., Symes, L. B., Balakrishnan, C. N., Zonana, D. M., & van Doorn, G. S. (2018). Mechanisms of assortative mating in speciation with gene flow: Connecting theory and empirical research. The American Naturalist, 191(1), 1-20.
Laubu, C., Dechaume-Moncharmont, F.-X., Motreuil, S., & Schweitzer, C. (2016). Mismatched partners that achieve postpairing behavioral similarity improve their reproductive success. Science Advances, 2, e1501013. https://doi.org/10.1126/sciadv.1501013
McGlothlin, J. W., Moore, A. J., Wolf, J. B., & Brodie, E. D. III. (2010). Interacting phenotypes and the evolutionary process. III. Social evolution. Evolution, 64(9), 2558-2574. https://doi.org/10.1111/j.1558-5646.2010.01012.x
Moiron, M., Araya-Ajoy, Y. G., Teplitsky, C., Bouwhuis, S., & Charmantier, A. (2020). Understanding the social dynamics of breeding phenology: Indirect genetic effects and assortative mating in a long-distance migrant. The American Naturalist, 196(5), 566-576. https://doi.org/10.1086/711045
Moore, A. J., Brodie, E. D. III, & Wolf, J. B. (1997). Interacting phenotypes and the evolutionary process: i. direct and indirect genetic effects of social interactions. Evolution, 51(5), 1352-1362. https://doi.org/10.1111/j.1558-5646.1997.tb01458.x
Munson, A. A., Jones, C., Schraft, H., & Sih, A. (2020). You’re just my type: Mate choice and behavioral types. Trends in Ecology & Evolution, 35, 823-833. https://doi.org/10.1016/j.tree.2020.04.010
Nakagawa, S., & Schielzeth, H. (2010). Repeatability for Gaussian and non-Gaussian data: A practical guide for biologists. Biological Reviews, 85, 935-956. https://doi.org/10.1111/j.1469-185X.2010.00141.x
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Santostefano, F., Wilson, A. J., Araya-Ajoy, Y. G., & Dingemanse, N. J. (2016). Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets. Behavioral Ecology, 27(4), 1235-1246. https://doi.org/10.1093/beheco/arw037
Schielzeth, H. (2010). Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution, 1, 103-113. https://doi.org/10.1111/j.2041-210X.2010.00012.x
Searle, S. R. (1961). Phenotypic, genetic and environmental correlations. Biometrics, 17, 474-480.
Spoon, T. R., Millam, J. R., & Owings, D. H. (2006). The importance of mate behavioural compatibility in parenting and reproductive success by cockatiels, Nymphicus hollandicus. Animal Behavior, 71, 315-326.
Stuber, E. F., Araya-Ajoy, Y. G., Mathot, K. J., Mutzel, A., Nicolaus, M., Wijmenga, J. J., Mueller, J. C., & Dingemanse, N. J. (2013). Slow explorers take less risk: A problem of sampling bias in ecological studies. Behavioral Ecology, 24, 1092-1098. https://doi.org/10.1093/beheco/art035
Taborsky, B., Guyer, L., & Taborsky, M. (2009). Size-assortative mating in the absence of mate choice. Animal Behavior, 77, 439-448. https://doi.org/10.1016/j.anbehav.2008.10.020
Tuyttens, F. A. M., de Graaf, S., Heerkens, J. L. T., Jacobs, L., Nalon, E., Ott, S., Stadiga, L., Van Laera, E., & Ampea, B. (2014). Observer bias in animal behaviour research: Can we believe what we score, if we score what we believe? Animal Behavior, 90, 273-280.
Wang, D., Forstmeier, W., Valcu, M., Dingemanse, N. J., Bulla, M., Both, C., Duckworth, R. A., Kiere, L. M., Karell, P., Albrecht, T., & Kempenaers, B. (2019). Scrutinizing assortative mating in birds. PLoS Biology, 17, e3000156. https://doi.org/10.1371/journal.pbio.3000156
Wilson, A. J., Gelin, U., Perron, M.-C., & Réale, D. (2009). Indirect genetic effects and the evolution of aggression in a vertebrate system. Proceedings of the Royal Society of London. Series B: Biological Sciences, 276, 533-541. https://doi.org/10.1098/rspb.2008.1193
Wolf, J. B., Brodie, E. D. III, Cheverud, J. M., Moore, A. J., & Wade, M. J. (1998). Evolutionary consequences of indirect genetic effects. Trends in Ecology & Evolution, 13, 64-69. https://doi.org/10.1016/S0169-5347(97)01233-0
Wolf, J. B., Brodie, E. D. III, Moore, A. J., & Mark, A. M. Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. The American Naturalist, 153(3), 254-266. https://doi.org/10.1086/303168