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

Lead Research Organisation: University of Glasgow
Department Name: College of Medical, Veterinary &Life Sci

Abstract

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.

Planned Impact

BENEFICIARIES OF THIS RESEARCH
A major research goal of evolutionary biology is to understand the genetic basis of complex phenotypes in natural populations; how they arise and how they change. This research will contribute new knowledge to the question of how the molecular basis of different reproductive modes evolves and will aim to significantly advance our understanding of evolution. The results of this research will be relevant and beneficial to the academic community in the UK and internationally.
Many members of the general public have a fascination about biodiversity, herpetology, and animal reproductive biology and so will be very interested in the results of this research. Glasgow in particular is home to an engaged citizenship with regard to natural history, herpetology, and science, both for local groups (e.g. Glasgow Natural History, Glasgow Herpetology) and national groups (e.g. FrogLife, British Herpetology Society). International beneficiaries include local citizens at our Austrian field site, and the international herpetology community that participate in the non-scientific meetings. Through our impact activities (see Pathways to Impact), this project will contribute to increasing public awareness and understanding of science and environmental issues.
The economic and societal impacts of our research project will reach out to, or draw from, the beneficiaries in the following manners:
Advancing public appreciation of biodiversity: Through media communication and outreach events (public or with amateur naturalists) we will contribute to the social and intellectual understanding of evolution and biodiversity in adults and children alike. Appreciation of the importance of genetic and evolutionary processes has diverse impacts on public perception of evidence-based policy and the role evolution can play in health, agriculture, and societal decisions.
Influencing Public Policy: Conservation priorities, legislation and policy will be impacted by the genetic and evolutionary results. The common lizard is UK BAP Priority and the UK has international obligations for protecting the species (http://jncc.defra.gov.uk/); UK BAP and ARC both propose that more genetic research is required for this species. The current project will provide estimates of diversity across the species and its relevance to reproduction - an important benchmark for future analyses nationally and internationally. This project has relevance for conservation biology as oviparous and viviparous species are predicted to respond differently to climate change challenges, but the potential for species to adapt by transitions between reproductive modes is not known. Our research and outreach activities internationally, particularly in Austria and France, will have local impacts through knowledge sharing and conservation interest. Conserving biodiversity has important benefits to society as a whole by contributing to a healthy and resilient natural world.
Commercial, Economic and Industry: Poultry scientists and stakeholders involved in the poultry industry will benefit from this study as the results will a) inform our understanding of the unique status of the avian egg in the evolution of the vertebrate reproduction, b) bring us closer to understanding the genetic control of key eggshell quality traits in a range of species (including chickens, turkeys, ducks, and quail), and c) bring poultry breeding companies closer to adopting a genome-wide approach in selecting for improved eggshell quality and efficiency of production.

Publications

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