Data from: Adaptive introgression from distant Caribbean islands contributed to the diversification of a microendemic adaptive radiation of trophic specialist pupfishes

Rapid diversification often involves complex histories of gene flow that leave variable and conflicting signatures of evolutionary relatedness across the genome. Identifying the extent and source of variation in these evolutionary relationships can provide insight into the evolutionary mechanisms involved in rapid radiations. Here we compare the discordant evolutionary relationships associated with species phenotypes across 42 whole genomes from a sympatric adaptive radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas and several outgroup pupfish species in order to understand the rarity of these trophic specialists within the larger radiation of Cyprinodon. 82% of the genome depicts close evolutionary relationships among the San Salvador Island species reflecting their geographic proximity, but the vast majority of variants fixed between specialist species lie in regions with discordant topologies. Top candidate adaptive introgression regions include signatures of selective sweeps and adaptive introgression of genetic variation from a single population in the northwestern Bahamas into each of the specialist species. Hard selective sweeps of genetic variation on San Salvador Island contributed 5 times more to speciation of trophic specialists than adaptive introgression of Caribbean genetic variation; however, four of the 11 introgressed regions came from a single distant island and were associated with the primary axis of oral jaw divergence within the radiation. For example, standing variation in a proto-oncogene (ski) known to have effects on jaw size introgressed into one San Salvador Island specialist from an island 300 km away approximately 10 kya. The complex emerging picture of the origins of adaptive radiation on San Salvador Island indicates that multiple sources of genetic variation contributed to the adaptive phenotypes of novel trophic specialists on the island. Our findings suggest that a suite of factors, including rare adaptive introgression, may be necessary for adaptive radiation in addition to ecological opportunity.

快速物种多样化（rapid diversification）通常伴随复杂的基因流历史，这类历史会在全基因组范围内留下演化亲缘关系的可变且不一致的信号。明确这类演化亲缘关系变异的范围与来源，能够帮助我们理解快速辐射演化（rapid radiation）背后的机制。本研究对42个全基因组数据展开比较分析，这些基因组来自巴哈马圣萨尔瓦多岛特有的谷鳉属（Cyprinodon）鳉鱼的同域适应性辐射（sympatric adaptive radiation）类群，以及多个外类群（outgroup）鳉鱼，旨在探究这些食性特化类群（trophic specialist）在更大尺度的谷鳉属辐射演化中为何较为罕见。全基因组中有82%的区域显示圣萨尔瓦多岛各类群间存在紧密的演化亲缘关系，这与其地理邻近性相符；但食性特化类群间固定的绝大多数变异，都位于演化拓扑结构不一致的基因组区域中。核心候选适应性基因渐渗（adaptive introgression）区域，包含选择性清除（selective sweep）信号，以及来自巴哈马西北部单一种群的遗传变异向各食性特化类群的适应性渐渗痕迹。圣萨尔瓦多岛本地遗传变异的硬选择性清除（hard selective sweep）对食性特化类群物种形成的贡献，是加勒比地区遗传变异适应性渐渗的5倍；但11个渐渗区域中有4个来自单个偏远岛屿，且与该辐射演化类群中口颌分化的主要轴相关。例如，一个已知可影响颌骨大小的原癌基因（proto-oncogene）ski的现存遗传变异（standing genetic variation），于约1万年前从300公里外的一座岛屿渐渗进入圣萨尔瓦多岛的一个食性特化类群中。圣萨尔瓦多岛适应性辐射起源的复杂图景表明，多种来源的遗传变异共同塑造了该岛上新型食性特化类群的适应性表型。本研究结果表明，除生态机会外，包括罕见适应性渐渗在内的一系列因素，可能是适应性辐射发生的必要条件。