Data from: Dissecting the basis of novel trait evolution in a radiation with widespread phylogenetic discordance

Phylogenetic analyses of trait evolution can provide insight into the evolutionary processes that initiate and drive phenotypic diversification. However, recent phylogenomic studies have revealed extensive gene tree-species tree discordance, which can lead to incorrect inferences of trait evolution if only a single species tree is used for analysis. This phenomenon—dubbed “hemiplasy”—is particularly important to consider during analyses of character evolution in rapidly radiating groups, where discordance is widespread. Here we generate whole-transcriptome data for a phylogenetic analysis of 14 species in the plant genus Jaltomata (the sister clade to Solanum), which has experienced rapid, recent trait evolution, including in fruit and nectar color, and flower size and shape. Consistent with other radiations, we find evidence for rampant gene tree discordance due to incomplete lineage sorting (ILS) and to introgression events among the well-supported subclades. Since both ILS and introgression increase the probability of hemiplasy, we perform several analyses that take discordance into account while identifying genes that might contribute to phenotypic evolution. Despite discordance, the history of fruit color evolution in Jaltomata can be inferred with high confidence, and we find evidence of de novo adaptive evolution at individual genes associated with fruit color variation. In contrast, hemiplasy appears to strongly affect inferences about floral character transitions in Jaltomata, and we identify candidate loci that could arise either from multiple lineage-specific substitutions or standing ancestral polymorphisms. Our analysis provides a generalizable example of how to manage discordance when identifying loci associated with trait evolution in a radiating lineage.

性状演化的系统发育分析可为阐明启动并推动表型多样化的演化过程提供重要洞见。然而，近期的系统基因组学研究揭示了广泛存在的基因树-物种树冲突，若仅使用单一物种树开展分析，会导致性状演化的推断出现偏差。这一被称为半趋异（hemiplasy）的现象，在冲突现象普遍存在的快速辐射类群的性状演化分析中尤其值得重视。本研究针对茄属（Solanum）的姊妹分支——夏特木属（Jaltomata）的14个物种开展系统发育分析并生成全转录组数据；该类群经历了快速且近期的性状演化，涉及果实与花蜜色泽、花部大小及形态的演变。与其他辐射类群的研究结果一致，本研究发现，因不完全谱系分选（incomplete lineage sorting, ILS）以及支持度较高的亚分支间存在基因渐渗事件，导致了大量的基因树-物种树冲突。鉴于不完全谱系分选与基因渐渗均会提升半趋异（hemiplasy）的发生概率，本研究在筛选可能参与表型演化的基因时，采用了多种纳入冲突因素的分析方法。尽管存在基因树-物种树冲突，我们仍可高置信度推断夏特木属（Jaltomata）的果实色泽演化历史，并发现与果实色泽变异相关的单个基因存在从头适应性演化的证据。与之形成对比的是，半趋异（hemiplasy）似乎对夏特木属（Jaltomata）的花部性状转变推断造成了显著影响，本研究筛选出的候选基因座既可能源自多个类群特异性替换事件，也可能来自现存的祖先多态性。本研究为在辐射演化类群中筛选与性状演化相关的基因座时，如何处理基因树-物种树冲突提供了一个可推广的范例。