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 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 several 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.

A Combinatorial View on Speciation and Adaptive Radiation

“…For instance, the monkeyflower Mimulus guttatus speciated in the past 150 years as a consequence of a pre-existing hybrid lethality mutation hitchhiking to high frequency in a copper mine population by physical linkage to a novel copper tolerance allele [40]. In two clades of wild tomato, introgression between early-branching lineages, adaptive sorting of standing genetic variation and evolution of genes through selection on de novo mutations all contributed to their adaptive radiation [41,42]. For many examples of recent speciation and rapid adaptive radiation, either the reproductive isolation loci have not yet been identified, or the timing of their evolution has not yet been reconstructed.…”

Decision letter: Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)

“…Several internal nodes of our species tree topology were supported by less than 1% of all gene trees, and only the most recent branching events were supported by more than 10% of gene trees. High levels of discordance, likely driven by introgression and incomplete lineage sorting, are common during ongoing species radiations, with many recent plant examples reporting similar findings (Novikova et al 2016, Pease et al 2016, Copetti et al 2017, Wu et al 2018. The abundance of polyploid species in our phylogeny (at least 21 out of 48, Figure 5) may have further exacerbated levels of discordance.…”

“…Hemiplasy may result in the overestimation of a trait's evolutionary rate (Mendes et al 2018), and results must be evaluated with caution. However, even though trait evolution within Erysimum almost certainly has been significantly more complex than can be represented by a simple bifurcating species tree (Novikova et al 2016, Pease et al 2016, Wu et al 2018, we believe our results remain robust in three key points.…”

“…Closely related species were therefore more likely to share similar cardenolide chemotypes. Given the high levels of gene discordance in our phylogeny, it seems probable that at least the glucosinolate results may have been affected by hemiplasy, i.e., a phenomenon where a trait is determined by genes whose topologies does not match the species tree (Avise and Robinson 2008, Pease et al 2016, Wu et al 2018. Hemiplasy may result in the overestimation of a trait's evolutionary rate (Mendes et al 2018), and results must be evaluated with caution.…”

Collection ofJaltomata darcyana(Solanaceae), previously unrecorded in cultivation, from a home garden in Chicago, IL

“…In Mexico, J. procumbens is typically found in disturbed habitats, including as a weed in agricultural fields where it is deliberately not removed so that its fruits can be consumed (Davis and Bye, 1982; Williams, 1985; Mione, fieldwork in Mexico). J. darcyana is the only species of the black/purple fruited lineage of Jaltomata (Mione, 1992; Miller et al ., 2011; Wu et al ., 2018) that lacks a day of protogyny. The two species are self-compatible, autogamous, and have similar fruits.…”