From egg-laying to live-bearing: Unravelling the genetics of a major evolutionary transition

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

Abstract

The process of reproduction is incredibly complex. From attracting the right mate, being genetically compatibility, and incubating a baby, there are many steps that must all work in concert. Each step is under stark natural selection because if unsuccessful then an individual's genes are not passed to the next generation. Tinkering with this process sees like tempting a Darwinian dead-end. So how can major, transformative changes in reproductive process happen during evolution?
The evolution of live-bearing (viviparity) from egg-laying (oviparity) in animals is an example of such a transformation, which has profound and wide-ranging consequences for a species. Yet live-bearing has evolved many times independently, in fishes, amphibians, early in the origin of therian mammals, and more than 100 times in reptiles.
Usually there is no opportunity to watch how changes from egg-laying to live-bearing happen because they occurred deep in the evolutionary past. Lizards are are an exception as some species have evolved live-bearing quite recently. Most species are completely either egg-laying or live-bearing: eggs are incubated for a relatively short time and then laid with a thick, calcified shell (oviparity) or babies are nurtured in the uterus until fully developed and then born covered with only a thin membrane (viviparity). The genetic basis of live-bearing is not known in any vertebrate.
The recent revolution in genomic sequencing technologies is allowing evolutionary biologists to address questions never before possible. One of these is the extent to which similar, complex adaptations have evolved from the same genetic bases across lineages. This issue is pivotal to understand how, and at what rate, natural selection shapes genomes so animals can adapt to their environment. Despite the 300 million years of evolutionary distance between reptiles and mammals, the basic structures, physiology, and molecular mechanisms of pregnancy are comparable between lizards and mammals, so the answer is relevant beyond just reptiles. The first step is to identify the genetic basis of live-bearing in a single species.
Europe's common lizard (Zootoca vivipara) has the remarkable attribute of both reproductive modes within one species. The reproductive modes are genetically fixed and egg-layer and live-bearers are found in different geographic areas, except in one part of the Alps where oviparous and viviparous individuals come into contact and interbreed. This hybrid zone offers a unique and amazing 'natural experiment' where the genetics of reproductive traits can be studied.
This project will be the first to identify the genetic mechanisms of reproductive mode To do so we will focus on the common lizard. Our objectives are to:
(1) Characterise the genetic basis of reproductive mode and its traits shown by mothers, such as eggshell structure and the developmental stage at which embryos are laid as eggs or born as fully developed neonates. This is done by an experiment in the hybrid zone;
(2) Quantify how oviparous individuals' and viviparous individuals' genomes mix through hybridization, and locate the genetic variations that are under strong natural selection in either reproductive mode;
(3) Resolve the phylogenetic tree of the entire species complex and determine the timing and order of changes in reproductive style. Surprisingly, there is some evidence that reversals back to oviparity might occur in common lizards, but the evidence has not been well supported. Our genomic experiments will identify if multiple independent origins of viviparity, or a reversal to oviparity, have occurred in the species' history. We will identify whether those transitions involve the same genetic mechanism each time.
This research will examine for the first time the genetic architecture of reproductive mode, with direct relevance to biodiversity adaptation and reproductive biology.

Planned Impact

BENEFICIARIES OF THIS RESEARCH
Academia: A major research goal of evolutionary biology is to link adaptive phenotypes with the breadth of genetic variation found in nature. This research will contribute new knowledge to the question of how different reproductive modes evolve 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.
Training: 'Omics skills enhance the economic and scientific competitiveness of UK researchers.
Biodiversity conservation: Biodiversity conservation science as a field will benefit from this research, which is the first genomic analysis of the common lizard and will include information about an important wild population.
Agriculture: The eggshell is a prominent model for biomineralization because of its importance for avian reproduction and the commercial sectors' interest in improving eggshell quality and safety.
General public: 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 regional groups with local chapters (e.g. National Trust for Scotland, FrogLife, British Herpetology Society).
Corporate collaborators: Chivas Brothers Ltd in Dumbarton is a nearby business with global trade links, and which is committed to 'preserving the environment 'and 'promoting sustainable agriculture'. They recognise the value of this research project for UK biodiversity and conservation and are keen to affiliate with the research team (especially MB).
Given the early stage of this research project, the full societal and economic benefits of this research project may not come clear until later in the research programme.

MEANS OF BENEFITING
The economic and societal impacts of our research project will reach out to, or draw from, the beneficiaries in the following manners:
Influencing Public Policy: Conservation priorities, legislation and policy will be impacted by the genetic, evolutionary and ecological results. The common lizard is a UK Biodiversity Action Plan Priority (BAP) and the UK has international obligations for protecting the species (http://jncc.defra.gov.uk/); UK BAP and Amphibian and Reptile Conservation (ARC) both propose that research at the landscape scale is required for this species. The current project will provide estimates of genome-wide genetic diversity and its relevance to reproduction - an important benchmark for future analyses nationally and internationally. 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) brings 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. Our involvement with Chivas Brothers will provide the corporation with links to non-profit scientific research through which they can evidence their corporate ethic of responsibility to environment and community.
Academia and training: Science is in the midst of a revolution in genetics, facilitated by major advances in DNA and RNA sequencing technology. Academic advancements in this field, outputs, and training, are of major benefit to the UK's scientific competitiveness.

Publications

10 25 50
 
Description NERC Biomolecular Analysis Facility Pilot Grant
Amount £5,600 (GBP)
Funding ID NBAF1018 
Organisation Natural Environment Research Council 
Department NERC Biomolecular Analysis Facility (NBAF)
Sector Public
Country United Kingdom
Start 11/2016 
End 03/2017