Journal Article

Genotypic sex determination enabled adaptive radiations of extinct marine reptiles

Janes, Daniel E., Meade, Andrew, Pagel, Mark, Organ, Chris L.

2009

Overview

Extinct reptiles, sea and sex Land vertebrates have returned to the sea many times over the ages. Modern seals and whales, as mammals, are live-bearing, and their sex is determined by genotype. But what of the many reptiles that once thronged the seas, such as the mosasaurs, ichthyosaurs and plesiosaurs? Sex determination might be environmentally or genotypically determined, and birth might be live, or through eggs. Based on phylogenetic analysis, Organ et al . propose that the sea-going reptiles of the past were not only live-bearers (which we know from the fossil record) but had genotypic sex determination. This would have freed them from the need to return to land to give birth (amniote eggs perish under water) and enabled their morphological transformation into highly evolved fish-like forms. Adaptive radiations often follow the evolution of key traits. The mechanism by which a species determines the sex of its offspring has been linked to critical ecological and life-history traits but not to major adaptive radiations. A coevolutionary relationship is now established in 94 amniote species between the sex-determining mechanism and whether a species bears live young or lays eggs. This is used to predict the evolution of genotypic sex determination before the acquisition of live birth in three extinct marine reptiles. 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 traits 1 , 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 birth 4 , 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 land 4 , 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.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: Adaptation, Physiological - genetics / Adaptation, Physiological - physiology / Algorithms / Amniota / Animals / Aquatic reptiles / Bayes Theorem / Biological Evolution / Births / Cetacea / Earth sciences / Earth, ocean, space / Endangered & extinct species / Evolution / Exact sciences and technology / Extinct animals / Extinction, Biological / Female / Fossils / Genetic aspects / Genotype / Genotype & phenotype / History, Ancient / Humanities and Social Sciences / letter / Life history / Male / Marine / Marine Biology / Markov Chains / Mesozoic / Methods / Monte Carlo Method / multidisciplinary / Offspring / Origin of species / Oviposition - genetics / Oviposition - physiology / Paleontology / Phylogeny / Reptiles / Reptiles & amphibians / Reptiles - classification / Reptiles - genetics / Reptiles - physiology / Science / Science (multidisciplinary) / Sex Chromosomes - genetics / Sex Determination Processes / Sex determination, Genetic / Sex Ratio / Temperature / Vertebrate paleontology / Viviparity, Nonmammalian - genetics / Viviparity, Nonmammalian - physiology