Abstract
Trait evolution among a set of species—a central theme in evolutionary biology—has long been understood and analyzed with respect to a species tree. However, the field of phylogenomics, which has been propelled by advances in sequencing technologies, has ushered in the era of species/gene tree incongruence and, consequently, a more nuanced understanding of trait evolution. For a trait whose states are incongruent with the branching patterns in the species tree, the same state could have arisen independently in different species (homoplasy) or followed the branching patterns of gene trees, incongruent with the species tree (hemiplasy). Another evolutionary process whose extent and significance are better revealed by phylogenomic studies is gene flow between different species. In this work, we present a phylogenomic method for assessing the role of hybridization and introgression in the evolution of polymorphic or monomorphic binary traits. We apply the method to simulated evolutionary scenarios to demonstrate the interplay between the parameters of the evolutionary history and the role of introgression in a binary trait’s evolution (which we call xenoplasy). Very importantly, we demonstrate, including on a biological data set, that inferring a species tree and using it for trait evolution analysis in the presence of gene flow could lead to misleading hypotheses about trait evolution.
Highlights
Evolutionary biology began with the study of traits, and both descriptive and mechanistic explanations of trait evolution are key foci of macroevolutionary studies today
We show how sampling trait polymorphism improves the informativeness of the global xenoplasy risk factor (G-XRF), and the importance of inferring a species network where gene flow occurs for elucidating trait evolution
We find that the probability density of the major tree is lower than the true or inferred networks in either case, suggesting that the G-XRF is powerful enough to detect the potential for specific traits to be introgressed, since it is derived from those probability densities
Summary
Evolutionary biology began with the study of traits, and both descriptive and mechanistic explanations of trait evolution are key foci of macroevolutionary studies today. Modern systematics synthesizes genomic data into informative species trees [5, 6], revealing the complex relationship between speciation and trait evolution. This is a welcome development as statistical methods for elucidating interspecific trait evolution without making use of the species tree can produce misleading results [7, 8]. Many trait patterns are “incongruent” and may be examples of convergent evolution, where traits have been gained or lost independently This kind of explanation is termed homoplasy, referring to a pattern of similarity which is not the result of common descent [9]. While the trait pattern is incongruent with the species tree, it is congruent with gene trees that differ from the species tree
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