Reproductive mode evolution and reversal demonstrate the genetic toolkits of egg-laying and live-bearing

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Laying eggs or giving birth to live young are two fundamentally different ways for females to produce their offspring. All birds, crocodilians, turtles, monotreme mammals (such as duck-billed platypus), and many lizards and snakes are egg-laying, as were most dinosaurs. In contrast, all placental mammals (like humans), marsupials, and some lizards and snakes are live-bearing. From studying embryos we know that many molecular and developmental aspects of these reproductive modes arose deep within the tree of life. For example, ancient egg-making structures are still retained within mammalian placenta, and the genes activated by pregnancy in lizards are the same as those activated by pregnancy in mammals and seahorses. Yet, clearly, substantial reproductive differences evolved between species; though it is not known how or why because the core genetic controls of these reproductive modes remain unknown. This major and obvious gap in our biological knowledge has persisted into the genomic era - where we can now study the entire DNA sequence of an organism - because we lacked an informative experimental model. Simply put, to test the genetic basis of traits that differ, the definitive experiment is to make a cross between the two different types. In the case of reproductive mode this is usual not possible, because species are too divergent to successfully breed. For example, no one can make a genetic cross of a platypus and a snake to test if the 'egg making DNA' is the same in both species.Our proposal seeks to shed light on the genetic basis of these fundamental reproductive traits using an exceptional species: the humbly-named 'common lizard'. Native to all of Eurasia, including the British Isles, this species harbours a secret underneath its simple brown scales: some populations are egg-laying and others are live-bearing. Like all reptiles, egg-laying is the original, or ancestral, mode. This means that many millions of years ago all common lizard females laid eggs. Then, about three million years ago, some females discarded the egg-laying tactic; no longer encircling their embryos in eggshells, the females retained their babies inside their bodies until fully developed. Why and how this happened is not known, but is presumed to be an adaptation that allowed mothers to better protect their embryos from cold and challenging environments. Amazingly, evolutionary reconstructions suggest that another million years later, some common lizards abandoned the live-bearing strategy and reversed back to egg-laying. Today we have populations with the original egg-laying strategy (mostly in the Alps), the live-bearers (across most of Eurasia), and those few that reversed back to egg-laying from live-bearing (found in the Pyrenees). Importantly, because they are closely related, individuals from all of these populations can interbreed.To test long-standing ideas about the genetic basis of fundamental reproductive traits, we plan to do controlled functional studies of the different types found within these lizards and make experimental crosses between them. By comparing the two lineages of egg-laying lizards we will be able to identify the genes necessary for egg-laying. This is due to the fact that the core genes should be found in the genomes of both and, if they are shared, these genes should be expressed in similar places and times. Then, using all the information we gain about how and where genes are active, we will use computational approaches to retrace the evolution of 'egg-laying' and 'live-bearing' genes across the history of the entire species. This will reveal how changes in a species' DNA give rise to changes in reproductive mode. Because of the ancient origins and sharing of reproductive genes across species, the lessons learned from these lizards will provide new and valuable insights into the biology, reproductive health, and evolution of all vertebrates.