Alien gene introgression promotes rapid adaptation: an unconscious experiment on Fire-bellied toad (Bombina bombina) at the northern edge of its distribution range

本提案通过评估特定假设，重点关注快速变化的适应性变异的基因组来源（专题组3），即：(1)物种分布边缘的小型孤立种群可能受到缺乏长期遗传变异的限制；(2)外来等位基因的渗入可能增强此类种群的适应潜力。在基因渗入的情况下，杂合度和等位基因多样性瞬间增加，有性繁殖产生由不同组的原生和异源等位基因组合而成的马赛克基因型，为快速适应提供了原料。我们研究的是火腹蟾蜍bomina bomina，它在欧洲有两个不同的进化谱系，即，南部的谱系分布在巴尔干国家和奥地利，北部的谱系从乌克兰穿过波兰到达北部分布范围的边缘，在德国北部和瑞典南部。对20个不相关基因位点的初步遗传分析揭示了南方谱系（假定是奥地利）基因型向三个当地北方谱系人群的渗透，这可能是由于业余爬虫学家独立的非官方（和非法）释放所致。有趣的是，这些渐渗种群(1)在几个位点上的渐渗等位基因是固定的，(2)具有正的种群趋势，因此它们的表现优于当地权威种群。这个场景提供了一个复制的无意识实验，模拟了从南方谱系（可能适应更温暖的夏季环境）到北方种群的长距离扩散和随后的渗透。我们将对原生和渐渗的bomina种群进行基因组扫描（RAD-seq）和表达谱分析（RNA-seq），以在基因组尺度上辨别来自原生的渐渗等位基因/表达模式。在全基因组关联研究（GWAS）中，我们将把这些模式与健康相关的特征（体型、质量、状况）联系起来。这些数据将被输入到我们的合作者（Stephan教授）开发的理论模型中，以辨别在快速适应中选择性扫描与多基因选择的相对重要性。通过对候选基因（包括MHC和热休克蛋白基因）的深入分析，将揭示基因渐渗（异源）等位基因在自然选择中被偏爱和原生等位基因在自然选择中被保留的功能分类。这将为我们提供一个因果理解的原因，为什么在分布范围的北部边缘，火腹蟾蜍的渐渗种群优于非渐渗种群。最后，该项目的重点是将基因渗入作为一种增加常备遗传变异数量的机制，从而为快速适应提供适应性遗传物质。

This proposal focusses on genomic sources of adaptive variation for rapid change (thematic group 3), by evaluating particular hypotheses, i.e., (1) small isolated populations at the margin of a species distribution might be constrained by a lack of standing genetic variation and (2) introgression of allochthonous alleles may enhance the adaptive potential of such populations. In case of introgression, heterozygosity and allelic diversity increase instantly and sexual reproduction creates mosaic genotypes combining different sets of authochthonous and allochthonous alleles, providing the raw material for rapid adaptation. Our study organism is the Fire-bellied toad Bombina bombina, which occurs in Europe in two distinct evolutionary lineages, i.e., a southern lineage distributed in the Balkan states and Austria, and a northern lineage reaching from Ukraine through Poland to the edges of the northern distribution range in Northern Germany and Southern Sweden. Initial genetic analyses at 20 unlinked genetic loci unraveled an introgression of southern lineage (putatively Austrian) genotypes into three local northern lineage populations, presumably due to independent unofficial (and illegal) release by amateur herpetologists. Interestingly, these introgressed populations (1) are fixed for introgressed alleles at several loci and (2) have a positive population trend, such that they outperform local authochthonous populations. This scenario provides a replicated unconscious experiment, mimicking long-distance dispersal and subsequent introgression from a southern lineage (potentially adapted to warmer summer conditions) to a northern population. We will perform genomic scans (RAD-seq) and expression profiling (RNA-seq) for both the authochthonous and the introgressed Bombina populations to discern, on a genomic scale, introgressed alleles/expression patterns from authochthonous ones. In genome-wide association studies (GWAS), we will relate these patterns to fitness related traits (body size, mass, condition). These data will be fed into theoretical models developed by our collaborator (Prof. Stephan) to discern the relative importance of selective sweeps vs. polygenic selection in rapid adaptation. In-depth analysis of candidate genes (including MHC and heat shock protein genes) will unravel the functional classes, in which introgressed (allochthonous) alleles will be favored by selection, and in which ones authochthonous alleles are maintained. This will provide us with a causal understanding of the reason, why introgressed populations of the Fire-bellied toad at the northern edge of the distribution range outperform the non-introgressed ones. Ultimately, the project focusses on the relevance of introgression as a mechanism to increase the amount of standing genetic variation and thus to contribute adaptive genetic material for rapid adaptation.