Balancing selection maintains polymorphisms at neurogenetic loci in field experiments
Lonn, E., Koskela, E., Mappes, T., Mökkönen, M., Sims, A., & Watts, P. (2017). Balancing selection maintains polymorphisms at neurogenetic loci in field experiments. Proceedings of the National Academy of Sciences of the United States of America, 114(14), 3690-3695. https://doi.org/10.1073/pnas.1621228114
© the Authors, 2017. Freely available online through the PNAS open access option.
Most variation in behavior has a genetic basis, but the processes determining the level of diversity at behavioral loci are largely unknown for natural populations. Expression of arginine vasopressin receptor 1a (Avpr1a) and oxytocin receptor (Oxtr) in specific regions of the brain regulates diverse social and reproductive behaviors in mammals, including humans. That these genes have important fitness consequences and that natural populations contain extensive diversity at these loci implies the action of balancing selection. In Myodes glareolus, Avpr1a and Oxtr each contain a polymorphic microsatellite locus located in their 5′ regulatory region (the regulatory region-associated microsatellite, RRAM) that likely regulates gene expression. To test the hypothesis that balancing selection maintains diversity at behavioral loci, we released artificially bred females and males with different RRAM allele lengths into field enclosures that differed in population density. The length of Avpr1a and Oxtr RRAMs was associated with reproductive success, but population density and the sex interacted to determine the optimal genotype. In general, longer Avpr1a RRAMs were more beneficial for males, and shorter RRAMs were more beneficial for females; the opposite was true for Oxtr RRAMs. Moreover, Avpr1a RRAM allele length is correlated with the reproductive success of the sexes during different phases of reproduction; for males, RRAM length correlated with the numbers of newborn offspring, but for females selection was evident on the number of weaned offspring. This report of density-dependence and sexual antagonism acting on loci within the arginine vasopressin–oxytocin pathway explains how genetic diversity at Avpr1a and Oxtr could be maintained in natural populations. ...
PublisherNational Academy of Sciences
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Related funder(s)Academy of Finland
Funding program(s)Academy Project, AoF
Additional information about fundingWe thank the staff of the Experimental Animal Unit and Konnevesi Research Station, University of Jyväskylä, and S. Huttunen, S. Kyröläinen, P. Lehmann, M. Väätäinen, and T. Niittynen for logistical support; A. van t’Hof for cloning and sequencing; and E. Kallio, B. Crespi, the Crawford laboratory, three anonymous reviewers for insightful comments, and J. Valkonen for statistical advice. This work was supported by the Biological Interactions Doctoral Programme (E.L.); by Academy of Finland Grants 257340, 119200, 115961, and 140767 (to E.K.), 257729 (to M.M.), and 118603, 109165, 204284, and 268670 (to T.M.); and by the Center of Excellence in Evolutionary Research of the Academy of Finland. ...
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