Investigating closely related species that rapidly evolved divergent feeding morphology is a powerful approach to identify genetic variation underlying variation in complex traits. This can also lead to the discovery of novel candidate genes influencing natural and clinical variation in human craniofacial phenotypes. We combined whole-genome resequencing of 258 individuals with 50 transcriptomes to identify candidate cis-acting genetic variation underlying rapidly evolving craniofacial phenotypes within an adaptive radiation of Cyprinodon pupfishes. This radiation consists of a dietary generalist species and two derived trophic niche specialists – a molluscivore and a scale-eating species. Despite extensive morphological divergence, these species only diverged 10 kya and produce fertile hybrids in the laboratory. Out of 9.3 million genome-wide SNPs and 80,012 structural variants, we found very few alleles fixed between species – only 157 SNPs and 87 deletions. Comparing gene expression across 38 purebred F1 offspring sampled at three early developmental stages, we identified 17 fixed variants within 10 kilobases of 12 genes that were highly differentially expressed between species. By measuring allele-specific expression in F1 hybrids from multiple crosses, we found that the majority of expression divergence between species was explained by trans-regulatory mechanisms. We also found strong evidence for two cis-regulatory alleles affecting expression divergence of two genes with putative effects on skeletal development (dync2li1 and pycr3). These results suggest that SNPs and structural variants contribute to the evolution of novel traits and highlight the utility of the San Salvador Island pupfish system as an evolutionary model for craniofacial development.

中文翻译：

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营养专家specialist之间很少有固定的变异显示出快速的颅面发散基础的候选顺式调控等位基因。

研究迅速演变的不同进食形态的密切相关物种是一种确定复杂性状变异背后遗传变异的有力方法。这也可以导致发现影响人类颅面表型自然和临床变异的新候选基因。我们结合了258个个体的全基因组重测序和50个转录组，以识别在适应性Cyprinodon内快速演变的颅面表型基础上的候选顺式作用遗传变异fish鱼。这种辐射包括饮食上的通配物种和两个衍生的营养利基专家-软体动物和食鳞动物。尽管形态差异很大，但这些物种在实验室仅分化了10 kya并产生了可育的杂种。在930万个全基因组SNP和80,012个结构变异中，我们发现在物种之间固定的等位基因很少-只有157个SNP和87个缺失。比较在三个早期发育阶段采样的38个纯种F1后代的基因表达，我们在12种基因的10千碱基内确定了17种固定变异，这些变异在物种之间高度差异表达。通过测量来自多个杂交的F1杂种中的等位基因特异性表达，我们发现物种之间的大多数表达差异可以通过反式解释调节机制。我们还找到了两个顺式调控等位基因影响两个基因的表达差异并对骨骼发育（dync2li1和pycr3）具有推定作用的有力证据。这些结果表明，单核苷酸多态性和结构变异有助于新性状的进化，并突出了圣萨尔瓦多岛p鱼系统作为颅面发育的进化模型的实用性。