The perils of intralocus recombination for inferences of molecular convergence

Abstract

Accurate inferences of convergence require that the appropriate tree topology be used. If there is a mismatch between the tree a trait has evolved along and the tree used for analysis, then false inferences of convergence (‘hemiplasy’) can occur. To avoid problems of hemiplasy when there are high levels of gene tree discordance with the species tree, researchers have begun to construct tree topologies from individual loci. However, due to intralocus recombination, even locus-specific trees may contain multiple topologies within them. This implies that the use of individual tree topologies discordant with the species tree can still lead to incorrect inferences about molecular convergence. Here, we examine the frequency with which single exons and single protein-coding genes contain multiple underlying tree topologies, in primates and Drosophila , and quantify the effects of hemiplasy when using trees inferred from individual loci. In both clades, we find that there are most often multiple diagnosable topologies within single exons and whole genes, with 91% of Drosophila protein-coding genes containing multiple topologies. Because of this underlying topological heterogeneity, even using trees inferred from individual protein-coding genes results in 25% and 38% of substitutions falsely labelled as convergent in primates and Drosophila , respectively. While constructing local trees can reduce the problem of hemiplasy, our results suggest that it will be difficult to completely avoid false inferences of convergence. We conclude by suggesting several ways forward in the analysis of convergent evolution, for both molecular and morphological characters. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.

Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression

“…However, in our initial analyses we used maximum likelihood to infer the individual gene trees. Because protein-coding genes are themselves often a combination of multiple different underlying topologies [75], ML gene trees may be biased, and using them as input to gene tree-based methods may still lead to incorrect inferences of the species tree [76]. Therefore, we used the same 1,730 loci as above to infer gene trees using maximum parsimony with MPBoot [77].…”

Convergent evolution in the genomics era: new insights and directions

“…Multiple contributions in this issue point out, and begin to solve, some methodological challenges both arising from technical concerns and from interpretation. For one, Mendes et al highlight the problem hemiplasy (which arises from discordance between gene trees and species trees) poses for studies of convergent evolution [37]. This discordance creates a tendency to make false inferences of molecular convergence, and they show that the rate of false positives can be alarmingly high.…”

Intragenic conflict in phylogenomic datasets

“…Discussion 271 analyzed here overlap in taxon sampling but vary greatly in the frequency of intragenic conflict (e.g., 273 MAM1 and MAM2) suggesting that, while biological processes may play a role in generating conflict 274 (Mendes et al 2019), non-biological errors are likely to be a major source of incongruence. For example, 275 MAM2 has been thoroughly analyzed to uncover errors exist within the dataset assembly (Springer and 276 Gatesy, 2018).…”

“…Scornavacca and Galtier 2016, Mendes et al 2019). Without having generated the original datasets, 303…”

“…To facilitate this, several methods have been developed (e.g., Husmeier the species level, the impact of recombination has on phylogenetic inference remains debated (Edwards 36 2009, Lanier and Knowles, 2012; Wu 2013). Scornavacca and Galtier (2017) showed that exons within 37 the same gene may present different genealogies, a pattern confirmed by Mendes et al (2019). Despite 38 this proliferation of methods, many are not tractable for phylogenomic datasets and/or assume the conflict 39 arose from a biological process.…”