Department of Integrative Biology, University of California, Berkeley, Berkeley, United States.
Museum of Vertebrate Zoology, University of California, Berkeley, Berkeley, United States.
Elife. 2022 May 26;11:e72905. doi: 10.7554/eLife.72905.
Estimating the complex relationship between fitness and genotype or phenotype (i.e. the adaptive landscape) is one of the central goals of evolutionary biology. However, adaptive walks connecting genotypes to organismal fitness, speciation, and novel ecological niches are still poorly understood and processes for surmounting fitness valleys remain controversial. One outstanding system for addressing these connections is a recent adaptive radiation of ecologically and morphologically novel pupfishes (a generalist, molluscivore, and scale-eater) endemic to San Salvador Island, Bahamas. We leveraged whole-genome sequencing of 139 hybrids from two independent field fitness experiments to identify the genomic basis of fitness, estimate genotypic fitness networks, and measure the accessibility of adaptive walks on the fitness landscape. We identified 132 single nucleotide polymorphisms (SNPs) that were significantly associated with fitness in field enclosures. Six out of the 13 regions most strongly associated with fitness contained differentially expressed genes and fixed SNPs between trophic specialists; one gene () was also misexpressed in lab-reared hybrids, suggesting a potential intrinsic genetic incompatibility. We then constructed genotypic fitness networks from adaptive alleles and show that scale-eating specialists are the most isolated of the three species on these networks. Intriguingly, introgressed and de novo variants reduced fitness landscape ruggedness as compared to standing variation, increasing the accessibility of genotypic fitness paths from generalist to specialists. Our results suggest that adaptive introgression and de novo mutations alter the shape of the fitness landscape, providing key connections in adaptive walks circumventing fitness valleys and triggering the evolution of novelty during adaptive radiation.
估计适应度与基因型或表型（即适应景观）之间的复杂关系是进化生物学的核心目标之一。然而，连接基因型与生物适应性、物种形成和新生态位的适应性游走仍然知之甚少，克服适应度低谷的过程仍存在争议。一个解决这些联系的突出系统是最近在巴哈马圣萨尔瓦多岛特有的生态和形态新颖的小鱼（一种兼性的、食软体动物者和食鳞者）的适应性辐射。我们利用了来自两个独立现场适应性实验的 139 个杂种的全基因组测序，以确定适应度的基因组基础，估计基因型适应度网络，并测量适应度景观上适应性游走的可及性。我们确定了 132 个与野外围栏中适应度显著相关的单核苷酸多态性（SNP）。与适应度最密切相关的 13 个区域中有 6 个区域包含了营养专家之间差异表达的基因和固定 SNP；一个基因（）在实验室饲养的杂种中也表达错误，表明存在潜在的内在遗传不兼容性。然后，我们从适应性等位基因构建了基因型适应度网络，并表明食鳞者在这些网络中是三个物种中最孤立的。有趣的是，与现有变异相比，渗入和从头变异降低了适应度景观的崎岖度，增加了从杂食者到专家的基因型适应度路径的可及性。我们的研究结果表明，适应性渗入和从头突变改变了适应度景观的形状，为绕过适应度低谷的适应性游走提供了关键连接，并在适应性辐射过程中触发了新颖性的进化。
