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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 heuristic methods that analyze summaries of the multilocus sequence data to detect gene flow, which may suffer from low power. Here we use the full likelihood method implemented in the Bayesian program BPP to reanalyze these data. 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 65%. 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. Our analyses highlight the importance of using adequate statistical methods to reach reliable biological conclusions concerning cross-species gene flow.

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.]

Conservation efforts rely on robust taxonomic assessments that should be based on critical assessment of interspecific boundaries, infraspecific variation, and potentially distinctive peripheral populations. The meadow vole (Microtus pennsylvanicus) is widely distributed across North America, including 28 morphologically defined subspecies and numerous isolated populations. Because some subspecies are of high conservation concern, we examined geographic variation across the range of the species to test existing infraspecific taxonomy in terms of local and regional diversification. We sequenced mitochondrial DNA (mtDNA) from 20 subspecies of M. pennsylvanicus and contextualized infraspecific variation through comparison of pairwise genetic distances derived from an extended data set of 63 species of Microtus. We found strong support for at least three divergent clades within M. pennsylvanicus, with observed intraspecific clade divergence exceeding that between several pairwise comparisons of sister species within Microtus. Six nuclear genes were then sequenced to test the validity of mtDNA structure and to further evaluate the possibility of cryptic, species-level diversity using Bayes factor species delimitation (BFD) analyses. BFD consistently and decisively supported multiple species based on the multilocus approach. We propose that taxonomic revision of the meadow vole is required, with the eastern clade now identified as M. pennsylvanicus (Ord 1815), the western clade as M. drummondii (Audubon and Bachman 1853), and the coastal Florida clade as M. dukecampbelli (Woods, Post, and Kilpatrick 1982). We suggest that such an arrangement would more closely reflect evolutionary history and provide critical context for further examination of distinctive southern peripheral populations that harbor novel evolutionary legacies and adaptive potential.

The Beringian Coevolution Project (BCP), a field program underway in the high northern latitudes since 1999, has focused on building key scientific infrastructure for integrated specimen-based studies on mammals and their associated parasites. BCP has contributed new insights across temporal and spatial scales into how ancient climate and environmental change have shaped faunas, emphasizing processes of assembly, persistence, and diversification across the vast Beringian region. BCP collections also represent baseline records of biotic diversity from across the northern high latitudes at a time of accelerated environmental change. These specimens and associated data form an unmatched resource for identifying hidden diversity, interpreting past responses to climate oscillations, documenting contemporary conditions, and anticipating outcomes for complex biological systems in a regime of ecological perturbation. Because of its dual focus on hosts and parasites, the BCP record also provides a foundation for comparative analyses that can document the effects of dynamic change on the geographic distribution, transmission dynamics, and emergence of pathogens. By using specific examples from carnivores, eulipotyphlans, lagomorphs, rodents, ungulates, and their associated parasites, we demonstrate how broad, integrated field collections provide permanent infrastructure that informs policy decisions regarding human impact and the effect of climate change on natural populations.

We report the first Canadian record of the Holarctic least shrew (Sorex minutissimus Zimmermann, 1780) and associated helminth worms, collected along the Dempster Highway in central Yukon in 2014. We identify the specimen based on morphological characters, characterize the habitat, report other mammals and helminth species associated with this specimen, and use mitochondrial DNA sequences to place the specimen within a phylogenetic context and address Pleistocene refugial hypotheses. Although long considered an Eurasian endemic, the diminutive least shrew was first reported from Alaska in 1994. Our new record for Canada indicates that the species may occur at least as far east as the MacKenzie River and DNA variation suggests this species persisted only in the Beringian refugium in North America during the Last Glacial Maximum. The discovery of a new mammal and associated parasites for Canada points to the urgent need for more detailed information on high-latitude biotas in North America, data that are best obtained through museum-based field surveys, particularly for small, cryptic species.

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.