Genotypic sex determination enabled adaptive radiations of extinct marine reptiles

A Corrigendum to this article was published on 08 October 2009

Abstract

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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Figure 1: Distribution of viviparity and GSD within amniotes.
Figure 2: Posterior distributions of evolutionary transition rates between sex-determining mechanism and reproductive mode in extant amniote species.
Figure 3: A specimen of Stenopterygius quadriscissus , an extinct ichthyosaur from the Early to Middle Jurassic Period.

References

  1. 1

    Janzen, F. J. & Phillips, P. C. Exploring the evolution of environmental sex determination, especially in reptiles. J. Evol. Biol. 19, 1775–1784 (2006)

    CAS  Article  Google Scholar 

  2. 2

    Robert, K. A. & Thompson, M. B. Viviparous lizard selects sex of embryos. Nature 412, 698–699 (2001)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Warner, D. A. & Shine, R. The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451, 566–568 (2008)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Caldwell, M. W. & Lee, M. S. Y. Live birth in Cretaceous marine lizards (mosasauroids). Proc. R. Soc. B 268, 2397–2401 (2001)

    CAS  Article  Google Scholar 

  5. 5

    Cheng, Y.-n., Wu, X.-c. & Ji, Q. Triassic marine reptiles gave birth to live young. Nature 432, 383–386 (2004)

    ADS  CAS  Article  Google Scholar 

  6. 6

    Dal Sasso, C. & Pinna, G. Besanosaurus leptorhynchus n. gen. n. sp., a new shastasaurid ichthyosaur from the Middle Triassic of Besano. Paleontol. Lombarda 4, 1–24 (1996)

    Google Scholar 

  7. 7

    Maxwell, E. E. & Caldwell, M. W. First record of live birth in Cretaceous ichthyosaurs: closing an 80 million year gap. Proc. R. Soc. B 270, S104–S107 (2003)

    Article  Google Scholar 

  8. 8

    Andrews, R. M. & Mathies, T. Natural history of reptilian development: constraints on the evolution of viviparity. Bioscience 50, 227–238 (2000)

    Article  Google Scholar 

  9. 9

    Shine, R. in Biology of the Reptilia Vol. 15 (eds Gans, C. & Billett, F.) 605–694 (Wiley, 1985)

    Google Scholar 

  10. 10

    Hodges, W. L. Evolution of viviparity in horned lizards (Phrynosoma): testing the cold climate hypothesis. J. Evol. Biol. 17, 1230–1237 (2004)

    CAS  Article  Google Scholar 

  11. 11

    Janzen, F. J. & Krenz, J. G. in Temperature-Dependent Sex Determination in Vertebrates (eds Valenzuela, N. & Lance, V. A.) 121–130 (Smithsonian Books, 2004)

    Google Scholar 

  12. 12

    Organ, C. L. & Janes, D. E. Evolution of sex chromosomes in Sauropsida. Integr. Comp. Biol. 48, 512–519 (2008)

    Article  Google Scholar 

  13. 13

    Clobert, J., Garland, T. & Barbault, R. The evolution of demographic tactics in lizards: a test of some hypotheses concerning life history evolution. J. Evol. Biol. 11, 329–364 (1998)

    Article  Google Scholar 

  14. 14

    Wapstra, E. et al. Maternal basking behaviour determines offspring sex in a viviparous reptile. Proc. R. Soc. B 271, S230–S232 (2004)

    Article  Google Scholar 

  15. 15

    Everhart, M. J. Oceans of Kansas: a Natural History of the Western Interior Sea (Indiana Univ. Press, 2005)

    Google Scholar 

  16. 16

    Bell, G. L. J., Sheldon, M. A., Lamb, J. P. & Martin, J. E. The first direct evidence of live birth in Mosasauridae (Squamata): exceptional preservation in Cretaceous Pierre Shale of South Dakota. J. Vertebr. Paleontol. 16 (suppl. 3). 21A (1996)

    Google Scholar 

  17. 17

    Harrison, R. J. in The Biology of Marine Mammals (ed. Andersen, H.) 253–348 (Academic, 1969)

    Google Scholar 

  18. 18

    Lee, M. S. Y. & Shine, R. Reptilian viviparity and Dollo’s Law. Evolution Int. J. Org. Evolution 52, 1441–1450 (1998)

    Article  Google Scholar 

  19. 19

    Blackburn, D. G. Evolutionary origins of viviparity in the reptilia. II. Serpentes, Amphisbaenia, and Ichthyosauria. Amphib.-reptil. 6, 259–291 (1985)

    Article  Google Scholar 

  20. 20

    Kennett, R., Christian, K. & Bedford, G. Underwater nesting by the Australian freshwater turtle Chelodina rugosa: effect of prolonged immersion and eggshell thickness on incubation period, egg survivorship, and hatchling size. Can. J. Zool. 76, 1019–1023 (1998)

    Article  Google Scholar 

  21. 21

    Blackburn, D. G., Vitt, J. L. & Beuchat, C. A. Eutherian-like reproductive specializations in a viviparous reptile. Proc. Natl Acad. Sci. USA 81, 4860–4863 (1984)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Motani, R. Evolution of fish-shaped reptiles (Reptilia: Ichthyopterygia) in their physical environments and constraints. Annu. Rev. Earth Planet. Sci. 33, 395–420 (2005)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Nicholls, E. L. & Manabe, M. Giant ichthyosaurs of the Triassic—a new species of Shonisaurus from the Pardonet Formation (Norian: Late Triassic) of British Columbia. J. Vertebr. Paleontol. 24, 838–849 (2004)

    Article  Google Scholar 

  24. 24

    Quinn, A. E. et al. Temperature sex reversal implies sex gene dosage in a reptile. Science 316, 411 (2007)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Maddision, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. Version 2.5. <http://mesquiteproject.org> (2008)

  26. 26

    Lee, M. S. Y. The phylogeny of varanoid lizards and the affinities of snakes. Phil. Trans. R. Soc. B 352, 53–91 (1997)

    ADS  Article  Google Scholar 

  27. 27

    Pagel, M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. B 255, 37–45 (1994)

    ADS  Article  Google Scholar 

  28. 28

    Pagel, M. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006)

    PubMed  Google Scholar 

Download references

Acknowledgements

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.

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Correspondence to Chris L. Organ or Mark Pagel.

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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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