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

Abstract

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 colour, 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. As 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 colour evolution in Jaltomata can be inferred with high confidence, and we find evidence of de novo adaptive evolution at individual genes associated with fruit colour 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.

A simple genetic architecture and low constraint allow rapid floral evolution in a diverse and recently radiating plant genus

“…First, floral trait variation within Jaltomata shows clear hallmarks of selection imposed by pollinator differentiation. Of the two main lineages within the genus, nearly all species in the Central and South American clade have relatively small, ancestrally rotate flowers with small amounts of lightly colored nectar (Wu et al ., ), and hymenopterans have been observed visiting several of these species in their native range (T. Mione, pers. comm.).…”

“…Despite only having diversified with the last 5 Myr (Sarkinen et al ., ; Wu et al ., ), species of Jaltomata are highly phenotypically diverse, including extensive variation in the size, shape, and color of floral traits that is absent among their close relatives within Solanum and Capsicum . Indeed, phylogenetic analyses suggest numerous transitions in floral traits within the genus, including several instances of convergent evolution (Miller et al ., ; Wu et al ., ). Importantly, many of these transitions appear to involve parallel changes in several different traits within a lineage (e.g.…”

Chance and predictability in evolution: The genomic basis of convergent dietary specializations in an adaptive radiation

“…Our approach allows detecting genetic changes in the genes expressed in adults (either in the same gene or in equivalent gene functions) matching the phenotypic convergence observed in dietary specialist Dysdera . Nevertheless, it is largely known that hemiplasy can also produce such matching patterns, inducing false evidence of convergent evolution (Mendes et al, ; Wu et al, ). Indeed, the high level of gene‐tree discordance caused by ancestral polymorphisms could potentially explain some of the repeated changes identified in D. gomerensis and D. tilosensis .…”

“…We aimed to detect those evolutionary changes required to explain a repeated character state in the two specialist lineages, either a gene expression profile or a selective constraint pattern, matching phenotypic convergence. Nevertheless, both incomplete lineage sorting (ILS; Maddison, 1997) and species hybridization can produce fundamental discordances between gene trees and the species tree, a phenomenon commonly referred to as "hemiplasy" (Avise & Robinson, 2008), giving rise to the illusion of homoplasy and the erroneous inference of convergence (Mendes, Hahn, & Hahn, 2016;Wu, Kostyun, Hahn, & Moyle, 2018).…”

A multilocus phylogeny of the fish genus Poeciliopsis: Solving taxonomic uncertainties and preliminary evidence of reticulation

“…Another species with high placentation whose evolutionary history might have involved reticulation is P. prolifica (also a member of the Leptorhaphis complex). Clearly the addition of many more loci is necessary to resolve the evolutionary history of this genus and strengthen its value as a system for macroevolutionary questions, which should take into account reticulate histories when inferring the mode and tempo of evolution of traits of interest (see Wu, Kostyun, Hahn, & Moyle, 2017). We consider that P. balsas and P. new species should be protected.…”