Data from: A test of genomic modularity among life-history adaptations promoting speciation with gene flow

Speciation with gene flow may require adaptive divergence of multiple traits to generate strong ecologically based reproductive isolation. Extensive negative pleiotropy or physical linkage of genes in the wrong phase affecting these diverging traits may therefore hinder speciation, while genetic independence or “modularity” among phenotypic traits may reduce constraints and facilitate divergence. Here, we test whether the genetics underlying two components of diapause life history, initial diapause intensity and diapause termination timing, constrain differentiation between sympatric hawthorn and apple-infesting host races of the fly Rhagoletis pomonella through analysis of 10,256 SNPs measured via genotyping-by-sequencing (GBS). Loci genetically associated with diapause termination timing were mainly observed for SNPs mapping to chromosomes 1–3 in the genome, most notably for SNPs displaying higher levels of linkage disequilibrium (LD), likely due to inversions. In contrast, selection on initial diapause intensity affected loci on all five major chromosomes of the genome, specifically those showing low levels of LD. This lack of overlap in genetically associated loci suggests that the two diapause phenotypes are largely modular. On chromosome 2, however, intermediate level LD loci and a subgroup of high LD loci displayed significant negative relationships between initial diapause intensity and diapause termination time. These gene regions on chromosome 2 therefore affected both traits, while most regions were largely independent. Moreover, loci associated with both measured traits also tended to exhibit highly divergent allele frequencies between the host races. Thus, the presence of nonoverlapping genetic modules likely facilitates simultaneous, adaptive divergence for the measured life-history components.

存在基因流的物种形成过程，往往需要多个性状发生适应性分化，才能形成基于生态作用的强效生殖隔离。因此，广泛存在的负多效性，或是调控此类分化性状的基因处于错误连锁相位的物理连锁，可能会阻碍物种形成；而表型性状间的遗传独立性或‘模块化（modularity）’，则可减轻演化限制并推动性状分化。本研究针对滞育生活史的两个组分——初始滞育强度与滞育终止时间背后的遗传基础，通过对10256个单核苷酸多态性（single nucleotide polymorphism, SNP）开展基因型分型测序（genotyping-by-sequencing, GBS）分析，检验该遗传基础是否限制了同域分布的山楂寄主宗与苹果寄主宗实蝇（Rhagoletis pomonella）种群间的分化。与滞育终止时间存在遗传关联的基因座，主要定位于基因组1~3号染色体的SNP位点中，其中尤以连锁不平衡（linkage disequilibrium, LD）水平较高的SNP最为显著，该现象大概率由染色体倒位所致。与之相反，作用于初始滞育强度的选择所影响的基因座，分布于基因组全部5条主要染色体上，且集中于LD水平较低的位点。遗传关联基因座不存在重叠的现象，表明这两个滞育表型在很大程度上具有模块化特征。但在2号染色体上，中等LD水平的基因座以及一类高LD水平的亚组位点，呈现出初始滞育强度与滞育终止时间间的显著负相关关系。因此，2号染色体上的这些基因区域同时调控了两个性状，而绝大多数基因区域则彼此独立。此外，同时与两个被测性状相关联的基因座，在两个寄主宗之间的等位基因频率也往往存在显著分化。综上，非重叠遗传模块化的存在，大概率推动了被测生活史组分的同步适应性分化。