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.

快速物种分化通常伴随复杂的基因流演化历史，这类历史会在全基因组范围内留下演化亲缘关系的异质性与冲突性信号。明确此类演化关系变异的范围与来源，可为解析快速辐射演化的内在机制提供关键洞见。本研究针对巴哈马（Bahamas）圣萨尔瓦多岛（San Salvador Island）特有底鳉（Cyprinodon）属鳉鱼的同域适应性辐射（sympatric adaptive radiation）类群，以及多个外类群（outgroup）鳉鱼物种，对42份全基因组中与物种表型相关的冲突性演化亲缘关系进行比较分析，旨在阐释此类营养特化物种（trophic specialists）在更大尺度的底鳉属辐射演化中为何稀缺。全基因组中有82%的区域显示圣萨尔瓦多岛鳉鱼物种间亲缘关系紧密，这与其地理邻近的特征相符；但特化物种间固定的绝大多数变异位点，却位于拓扑结构存在冲突的基因组区域中。核心候选适应性基因渐渗（adaptive introgression）区域，兼具选择性清除（selective sweep）信号与来自巴哈马西北部单一种群的遗传变异向各特化物种的适应性渐渗特征。圣萨尔瓦多岛种群内遗传变异的硬选择性清除，对营养特化物种形成的贡献度是加勒比海（Caribbean）遗传变异适应性基因渐渗的5倍；但11个渐渗区域中有4个源自单一偏远岛屿，且与辐射演化类群内口颌分化的主要轴相关。例如，已知可影响颌部大小的原癌基因（proto-oncogene）ski所携带的保留遗传变异，于约10千年前（kya）从300公里外的一座岛屿渐渗至圣萨尔瓦多岛的某一特化物种中。圣萨尔瓦多岛适应性辐射起源的复杂图景表明，多种遗传变异来源共同塑造了该岛上新型营养特化物种的适应性表型。本研究结果显示，除生态机遇外，包括罕见适应性基因渐渗在内的一系列因素，或为适应性辐射发生的必要条件。