Data from: Population genomics of local adaptation versus speciation in coral reef fishes (Hypoplectrus spp, Serranidae)

Are the population genomic patterns underlying local adaptation and the early stages of speciation similar? Addressing this question requires a system in which i. local adaptation and the early stages of speciation can be clearly identified and distinguished, ii. the amount of genetic divergence driven by the two processes is similar, and iii. comparisons can be repeated both taxonomically (for local adaptation) and geographically (for speciation). Here, we report just such a situation in the hamlets (Hypoplectrus spp), brightly colored reef fishes from the wider Caribbean. Close to 100,000 SNPs genotyped in 126 individuals from three sympatric species sampled in three repeated populations provide genome-wide levels of divergence that are comparable among allopatric populations (Fst estimate = 0.0042) and sympatric species (Fst estimate = 0.0038). Population genetic, clustering and phylogenetic analyses reveal very similar patterns for local adaptation and speciation, with a large fraction of the genome undifferentiated (Fst estimate ≈ 0), a very small proportion of Fst outlier loci (0.05-0.07%), and remarkably few repeated outliers (1-3). Nevertheless, different loci appear to be involved in the two processes in Hypoplectrus, with only 7% of the most differentiated SNPs and outliers shared between populations and species comparisons. In particular, a tropomyosin (Tpm4) and a previously identified hox (HoxCa) locus emerge as candidate loci (repeated outliers) for local adaptation and speciation, respectively. We conclude that marine populations may be locally adapted notwithstanding shallow levels of genetic divergence, and that from a population genomic perspective this process does not appear to differ fundamentally from the early stages of speciation.驱动局部适应与物种形成早期阶段的群体基因组模式是否具有相似性？要解答这一问题，需构建满足以下条件的研究体系：其一，可清晰识别并区分局部适应与物种形成早期阶段；其二，两种过程引发的遗传分化程度相近；其三，既可通过分类学重复比较（适配局部适应研究），也可通过地理学重复比较（适配物种形成研究）。 本研究针对广泛分布于加勒比海海域的色彩艳丽礁栖鱼类——皂鲈属（Hypoplectrus spp.）物种，报告了恰好符合上述条件的研究案例。我们对来自3个重复种群的3个同域分布物种的126个个体进行基因分型，共获得近10万个单核苷酸多态性（Single Nucleotide Polymorphism, SNP）位点；结果显示，异域种群（Fst估计值=0.0042）与同域物种（Fst估计值=0.0038）的全基因组分化水平相当。 群体遗传学、聚类分析与系统发育分析结果表明，局部适应与物种形成过程呈现高度相似的基因组模式：绝大多数基因组区域未发生分化（Fst估计值≈0），Fst异常位点占比极低（0.05%~0.07%），且重复出现的异常位点仅1~3个。尽管如此，皂鲈属中参与两类过程的基因座并不相同，群体比较与物种比较之间仅共享7%的高分化SNP位点与异常位点。 具体而言，原肌球蛋白（Tpm4）基因座与此前已报道的同源框（HoxCa）基因座分别成为局部适应与物种形成过程的候选基因座（重复异常位点）。本研究最终得出结论：即便遗传分化程度极低，海洋种群仍可实现局部适应；且从群体基因组学视角来看，局部适应过程与物种形成早期阶段并无本质差异。