Data from: Quantitative genetic analysis indicates natural selection on leaf phenotypes across wild tomato species (Solanum sect. Lycopersicon; Solanaceae)

Adaptive evolution requires both raw genetic material and an accessible path of high fitness from one fitness peak to another. In this study, we used an introgression line (IL) population to map quantitative trait loci (QTL) for leaf traits thought to be associated with adaptation to precipitation in wild tomatoes (Solanum sect. Lycopersicon; Solanaceae). A QTL Sign Test showed that several traits likely evolved under directional natural selection. Leaf traits correlated across species do not share a common genetic basis, consistent with a scenario in which selection maintains trait covariation unconstrained by pleiotropy or linkage disequilibrium. Two large effect QTL for stomatal distribution colocalized with key genes in the stomatal development pathway, suggesting promising candidates for the molecular bases of adaptation in these species. Furthermore, macroevolutionary transitions between vastly different stomatal distributions may not be constrained when such large effect mutations are available. Finally, genetic correlations between stomatal traits measured in this study and data on carbon isotope discrimination from the same ILs, support a functional hypothesis that the distribution of stomata affects the resistance to CO2 diffusion inside the leaf, a trait implicated in climatic adaptation in wild tomatoes. Along with evidence from previous comparative and experimental studies, this analysis indicates that leaf traits are an important component of climatic niche adaptation in wild tomatoes, and demonstrates that some trait transitions between species could have involved few, large effect genetic changes, allowing rapid responses to new environmental conditions.

适应性进化既依赖原始遗传物质，也需要一条可及的高适合度路径，以实现从一个适合度峰到另一个适合度峰的演化。本研究利用渐渗系（introgression line, IL）群体，对野生番茄（Solanum sect. Lycopersicon；茄科Solanaceae）中被认为与降水适应相关的叶片性状开展数量性状位点（quantitative trait loci, QTL）定位分析。QTL符号检验（QTL Sign Test）结果显示，多个性状大概率在定向自然选择作用下演化。跨物种间存在相关性的叶片性状并不共享共同的遗传基础，这与“选择维持性状协变且不受多效性（pleiotropy）或连锁不平衡（linkage disequilibrium）约束”的理论情景一致。两个控制气孔分布的大效应QTL与气孔发育通路中的关键基因共定位，为解析这些物种适应的分子基础提供了极具潜力的候选靶点。此外，若存在此类大效应突变，截然不同的气孔分布之间的宏观进化转变或不受约束。本研究测定的气孔性状与同一渐渗系群体的碳同位素分馏（carbon isotope discrimination）数据之间的遗传相关性，支持一项功能假说：气孔分布会影响叶片内部的二氧化碳扩散阻力，而该性状与野生番茄的气候适应密切相关。结合此前比较研究与实验研究的证据，本分析表明叶片性状是野生番茄气候生态位适应的重要组成部分，同时证实物种间的部分性状转变可能仅涉及少量大效应遗传变异，从而能够快速响应新的环境条件。