Adaptive radiations often follow the evolution of key traits, such as the origin of the amniotic egg and the subsequent radiation of terrestrial vertebrates. The mechanism by which a species determines the sex of its offspring has been linked to critical ecological and life-history traits1,2,3 but not to major adaptive radiations, in part because sex-determining mechanisms do not fossilize. Here we establish a previously unknown coevolutionary relationship in 94 amniote species between sex-determining mechanism and whether a species bears live young or lays eggs. We use that relationship to predict the sex-determining mechanism in three independent lineages of extinct Mesozoic marine reptiles (mosasaurs, sauropterygians and ichthyosaurs), each of which is known from fossils to have evolved live birth4,5,6,7. Our results indicate that each lineage evolved genotypic sex determination before acquiring live birth. This enabled their pelagic radiations, where the relatively stable temperatures of the open ocean constrain temperature-dependent sex determination in amniote species. Freed from the need to move and nest on land4,5,8, extreme physical adaptations to a pelagic lifestyle evolved in each group, such as the fluked tails, dorsal fins and wing-shaped limbs of ichthyosaurs. With the inclusion of ichthyosaurs, mosasaurs and sauropterygians, genotypic sex determination is present in all known fully pelagic amniote groups (sea snakes, sirenians and cetaceans), suggesting that this mode of sex determination and the subsequent evolution of live birth are key traits required for marine adaptive radiations in amniote lineages.
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We thank M. Everhart, R. Shine, M. Laurin, T. Quental, L. Cooper, S. Faul, M. Patten, N. Hobbs and C. Venditti for comments that improved the clarity of this paper. D.E.J. and C.L.O. thank S. V. Edwards for postdoctoral support. We thank the Department of Organismic and Evolutionary Biology and the Museum of Comparative Zoology at Harvard University for providing support that enabled this research, and the Centre for Advanced Computing and Emerging Technologies (ACET) at the University of Reading for making the ThamesBlue supercomputer available for our use. This research was supported in part by a travel grant from the Museum of Comparative Zoology at Harvard University, National Institutes of Health Postdoctoral Fellowships (1 F32 GM075490-01 to C.L.O., and 5 F32 GM072494 to D.E.J.), and Natural Environment Research Council grant NE/C51992X/1 to M.P.
Author Contributions All authors contributed to the design of the project. A.M. wrote the computer code. C.L.O., A.M. and M.P. performed the analyses.
This file contains Supplementary Figure 1, which is an outline of Supplementary Methods, Supplementary Figure 2 and Legend, Supplementary Data, Supplementary Tables 1-3 and Supplementary References. (PDF 1761 kb)
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Organ, C., Janes, D., Meade, A. et al. Genotypic sex determination enabled adaptive radiations of extinct marine reptiles. Nature 461, 389–392 (2009). https://doi.org/10.1038/nature08350
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