Power of Bayesian and Heuristic Tests to Detect Cross-Species Introgression with Reference to Gene Flow in the Tamias quadrivittatus Group of North American Chipmunks.

In the past two decades, genomic data have been widely used to detect historical gene flow between species in a variety of plants and animals. The Tamias quadrivittatus group of North America chipmunks, which originated through a series of rapid speciation events, are known to undergo massive amounts of mitochondrial introgression. Yet in a recent analysis of targeted nuclear loci from the group, no evidence for cross-species introgression was detected, indicating widespread cytonuclear discordance. The study used the heuristic method HYDE to detect gene flow, which may suffer from low power. Here we use the Bayesian method implemented in the program BPP to re-analyze these data. We develop a Bayesian test of introgression, calculating the Bayes factor via the Savage-Dickey density ratio using the Markov chain Monte Carlo (MCMC) sample under the model of introgression. We take a stepwise approach to constructing an introgression model by adding introgression events onto a well-supported binary species tree. The analysis detected robust evidence for multiple ancient introgression events affecting the nuclear genome, with introgression probabilities reaching 63%. We estimate population parameters and highlight the fact that species divergence times may be seriously underestimated if ancient cross-species gene flow is ignored in the analysis. We examine the assumptions and performance of HYDE and demonstrate that it lacks power if gene flow occurs between sister lineages or if the mode of gene flow does not match the assumed hybrid-speciation model with symmetrical population sizes. Our analyses highlight the power of likelihood-based inference of cross-species gene flow using genomic sequence data. [Bayesian test; BPP; chipmunks; introgression; MSci; multispecies coalescent; Savage-Dickey density ratio.].

Rapid divergence and gene flow at high latitudes shape the history of Holarctic ground squirrels (Urocitellus).

Across the animal tree of life, the prevalence and evolutionary role(s) of hybridization remain incompletely understood. Rapidly radiating clades can serve as important systems for investigating these issues; however, such groups are often characterized by additional, widespread sources of gene tree discordance (e.g., incomplete lineage sorting). In this paper, we employed a multilocus dataset, Bayesian gene tree inference, and multiple species tree reconstruction methods to infer phylogeny of Holarctic ground squirrels (Urocitellus). We tested phylogenetic hypotheses based on previous morphological, cytological and single-locus datasets, and began to parse the causes of pervasive gene tree discordance that was observed. There is widespread incomplete lineage sorting in Urocitellus, consistent with rapid diversification embedded within the larger radiation of marmotine ground squirrels. We also recovered strong support for 2 instances of mitonuclear discord due to ancient hybridization among members of the high-latitude parryii-richardsonii-elegans clade. These results add to a growing number of documented hybridization events in ground squirrels, suggesting their radiation is a fertile system for understanding the interplay of diversification and hybridization in animal evolution.