Combining Species Delimitation, Species Trees, and Tests for Gene Flow Clarifies Complex Speciation in Scrub-Jays

Abstract

Complex speciation, involving rapid divergence and multiple bouts of post-divergence gene flow, can obfuscate phylogenetic relationships and species limits. In North America, cases of complex speciation are common, due at least in part to the cyclical Pleistocene glacial history of the continent. Scrub-jays in the genus Aphelocoma provide a useful case study in complex speciation because their range throughout North America is structured by phylogeographic barriers with multiple cases of secondary contact between divergent lineages. Here, we show that a comprehensive approach to genomic reconstruction of evolutionary history, i.e., synthesizing results from species delimitation, species tree reconstruction, demographic model testing, and tests for gene flow, is capable of clarifying evolutionary history despite complex speciation. We find concordant evidence across all statistical approaches for the distinctiveness of an endemic southern Mexico lineage (A. w. sumichrasti), culminating in support for the species status of this lineage under any commonly applied species concept. We also find novel genomic evidence for the species status of a Texas endemic lineage A. w. texana, for which equivocal species delimitation results were clarified by demographic modeling and spatially explicit models of gene flow. Finally, we find that complex signatures of both ancient and modern gene flow between the non-sister California Scrub-Jay (A. californica) and Woodhouse’s Scrub-Jay (A. woodhouseii), result in discordant gene trees throughout the species’ genomes despite clear support for their overall isolation and species status. In sum, we find that a multi-faceted approach to genomic analysis can increase our understanding of complex speciation histories, even in well-studied groups. Given the emerging recognition that complex speciation is relatively commonplace, the comprehensive framework that we demonstrate for interrogation of species limits and evolutionary history using genomic data can provide a necessary roadmap for disentangling the impacts of gene flow and incomplete lineage sorting to better understand the systematics of other groups with similarly complex evolutionary histories.

Mitonuclear discordance results from incomplete lineage sorting, with no detectable evidence for gene flow, in a rapid radiation of Todiramphus kingfishers

“…Still, assignments of genomic ancestry are expected to discriminate between species with high accuracy if recent hybrid individuals are not sampled, even in cases of extensive historical gene flow (e.g. DeRaad et al, 2022). Under these circumstances, histories of gene flow between non‐sister taxa can be readily detected using ABBA‐BABA tests, which test for a statistical overrepresentation in the number of alleles shared between non‐sister lineages, based on a null assumption of ILS.…”

“…This differential gene flow could result in different patterns of relatedness between the mitochondrial and nuclear genomes(McKay & Zink, 2010;Toews & Brelsford, 2012). Here we found little indication of recently shared inter-species ancestry in the nuclear genome (Figure3), indicating strong reproductive isolation, even between recently diverged sympatric Todiramphus species(Andersen et al, 2015).Despite this limited evidence for recent introgression, individual ancestry assignments could miss signatures of rare or historical gene flow events (e.g DeRaad et al, 2022)…”

“…Despite this limited evidence for recent introgression, individual ancestry assignments could miss signatures of rare or historical gene flow events (e.g. DeRaad et al, 2022). In these cases, genomic signatures of ILS and gene flow can still be differentiated via statistical approaches (e.g.…”

Unraveling the Myotis Morass: Ultraconserved-Element Analysis Reveals Introgression, Cryptic Diversity, and Taxonomic Trouble in the Most Species-rich Bat Genus

“…This will require more collaboration and sample sharing between geneticists and taxonomists to build a system that is both robust and applicable in a genus as diverse as Myotis . DeRaad et al (2022) described a strategy using species trees, species delimitation, demographic model testing, and tests for gene flow to clarify complex speciation signatures in scrub-jays. Multi-faceted genomic strategies such as these may provide potential answers within Myotis as well.…”

An elevational shift facilitated the Mesoamerican diversification of Azure‐hooded Jays (Cyanolyca cucullata) during the Great American Biotic Interchange

“…Suggested common name: Azurebonneted Jay or Bonneted Jay. As with other recent cases where widespread jay species have been split into species with smaller geographic ranges (DeRaad et al, 2022;McCormack et al, 2008;Venkatraman et al, 2019), the resulting split would lead to a range-restricted species of conservation interest. The total range of C. cucullata, which inhabits two portions of the Talamanca Range in Costa Rica and Panama, is maybe only ~10,000 km 2 .…”