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

繁殖的过程非常复杂。从吸引合适的伴侣，基因兼容性，孵化婴儿，有许多步骤必须协调一致。每一步都是在自然选择下完成的，因为如果不成功，那么个体的基因就不会传递给下一代。对这一过程的修补就像是在引诱达尔文主义的死胡同。那么，在进化过程中，生殖过程中的重大变革是如何发生的呢？动物从产卵（卵生）进化为活产（胎生）就是这种转变的一个例子，它对一个物种产生了深远而广泛的影响。然而，在鱼类、两栖动物、兽目哺乳动物的早期起源中，以及爬行动物中100多次独立地进化出了活的生育。通常没有机会观察从产卵到生儿育女的变化是如何发生的，因为它们发生在进化的过去。蜥蜴是一个例外，因为一些物种最近已经进化出了活体。大多数物种要么完全产卵，要么完全活产：卵孵化相对较短的时间，然后产下一个厚的钙化壳（卵生），或者婴儿在子宫中培育，直到完全发育，然后出生时只有一层薄薄的膜（胎生）。在任何脊椎动物中，活产的遗传基础都是未知的。基因组测序技术的最新革命使进化生物学家能够解决以前不可能解决的问题。其中之一是在何种程度上，相似的，复杂的适应性已经从相同的遗传基础跨谱系进化。这个问题对于理解自然选择如何以及以何种速度塑造基因组，使动物能够适应环境至关重要。尽管爬行动物和哺乳动物之间有3亿年的进化距离，但蜥蜴和哺乳动物之间的基本结构，生理学和怀孕的分子机制是相似的，因此答案不仅仅与爬行动物有关。第一步是确定单个物种中活产的遗传基础。欧洲常见的蜥蜴（Zootoca vivipara）具有同一物种内两种生殖模式的显著属性。繁殖模式是遗传固定的，产卵和活熊在不同的地理区域，除了在阿尔卑斯山的一个部分，卵生和胎生个体接触和杂交。这个杂交区提供了一个独特而惊人的“自然实验”，可以研究生殖特征的遗传学。这个项目将是第一个确定生殖模式的遗传机制，为了做到这一点，我们将集中在共同的蜥蜴。我们的目标是：（1）描述生殖方式的遗传基础及其母亲所表现的特征，例如蛋壳结构和胚胎作为卵产下或作为完全发育的新生儿出生的发育阶段。这是通过杂交区的实验来完成的;（2）量化卵生个体和胎生个体的基因组如何通过杂交混合，并定位在任一繁殖模式下受到强烈自然选择的遗传变异;（3）解析整个物种复合体的系统发育树，并确定繁殖方式变化的时间和顺序。令人惊讶的是，有一些证据表明，逆转回卵生可能发生在普通蜥蜴，但证据没有得到很好的支持。我们的基因组实验将确定在该物种的历史中是否发生了多个独立的胎生起源或卵生逆转。我们将确定这些转变是否每次都涉及相同的遗传机制。这项研究将首次研究生殖模式的遗传结构，与生物多样性适应和生殖生物学直接相关。

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.