Determining the probability of hemiplasy in the presence of incomplete lineage sorting and introgression

Abstract

The incongruence of character states with phylogenetic relationships is often interpreted as evidence of convergent evolution. However, trait evolution along discordant gene trees can also generate these incongruences -a phenomenon known as hemiplasy. Classic phylogenetic comparative methods do not account for discordance, resulting in incorrect inferences about the number of times a trait has evolved, and therefore about convergence. Biological sources of discordance include incomplete lineage sorting (ILS) and introgression, but only ILS has received theoretical consideration in the context of hemiplasy. Here, we derive expectations for the probabilities of hemiplasy and homoplasy with ILS and introgression acting simultaneously. We find that introgression makes hemiplasy more likely, suggesting that methods that account for discordance due to ILS alone will be conservative. We also present a method for making statistical inferences about the relative probabilities of hemiplasy and homoplasy in empirical datasets. Our method is implemented in the software package HeIST (Hemiplasy Inference Simulation Tool), and estimates the most probable number of transitions among character states given a set of relationships with discordance. HeIST can accommodate ILS and introgression simultaneously, and can be applied to large phylogenies. We apply this tool to a phylogeny of New Guinea lizards that have evolved green blood from a red-blooded ancestor, and find that hemiplasy is likely to explain the observed trait incongruence.

Phylogenomic Assessment of the Role of Hybridization and Introgression in Trait Evolution

“…To tease these two processes apart, assuming introgression did not play a role, the HRF can be evaluated with respect to the species tree. Furthermore, a similar analysis of both displayed trees can provide a way for assessing the role of hemiplasy in the presence of introgression [29]. In our case, we are interested in answering a different question: How much does a reticulate evolutionary history involving hybridization and introgression explain the evolution of a trait as opposed to a strictly treelike evolutionary history?…”

“…Gene flow may explain some trait evolution [26], and methods analyzing trait evolution along a species network have been introduced [27, 28]. Such methods do not account for ILS, but the HRF framework was recently extended to fold introgression into hemiplasy and homoplasy [29]. However, hemiplasy was originally circumscribed to discordances that arise from idiosyncratic lineage sorting [11].…”

Highly replicated evolution of parapatric ecotypes

“…Considering a single lineage from each of the four populations starting at the present, we condition on the migrant status of the sampled lineages to calculate coalescent probabilities of gene tree topologies that result in a grouping in which the two populations of the derived ecotype are not monophyletic in the gene genealogy. These methods recapitulate recent more formal treatments of the probability of hemiplasy (non-monophyly despite a single mutational origin for a trait) under incomplete lineage sorting and introgression (Guerrero and Hahn 2018;Hibbins et al 2020), though we have considered a scenario involving four populations to reflect the nature of parapatric pairs. Moreover, our emphasis is placed on the implications of gene flow for the original inference of the species tree itself, rather than how it pertains to the history of a selected locus of interest under an inferred phylogeny.…”

Introgression is widespread in the radiation of carnivorous Nepenthes pitcher plants

“…In Quercus, for example, introgression confounds naive inference of phylogeography and clade ages (McVay et al, 2017). Recent work substantiates the concern that phylogenetic comparative analyses for both Mendelian and quantitative traits can be flawed by ILS (Mendes et al, 2018) as well as introgression (Hibbins et al, 2020). Therefore, future studies that utilize Nepenthes phylogenies for evolutionary inference should aim to mitigate the risks of hemiplasy (e.g.…”