Genetic Barriers to Historical Gene Flow between Cryptic Species of Alpine Bumblebees Revealed by Comparative Population Genomics

Abstract

Evidence is accumulating that gene flow commonly occurs between recently-diverged species, despite the existence of barriers to gene flow in their genomes. However, we still know little about what regions of the genome become barriers to gene flow and how such barriers form. Here we compare genetic differentiation across the genomes of bumblebee species living in sympatry and allopatry to reveal the potential impact of gene flow during species divergence and uncover genetic barrier loci. We first compared the genomes of the alpine bumblebee Bombus sylvicola and a previously unidentified sister species living in sympatry in the Rocky Mountains, revealing prominent islands of elevated genetic divergence in the genome that co-localize with centromeres and regions of low recombination. This same pattern is observed between the genomes of another pair of closely-related species living in allopatry (B. bifarius and B. vancouverensis). Strikingly however, the genomic islands exhibit significantly elevated absolute divergence (dXY) in the sympatric, but not the allopatric, comparison indicating that they contain loci that have acted as barriers to historical gene flow in sympatry. Our results suggest that intrinsic barriers to gene flow between species may often accumulate in regions of low recombination and near centromeres through processes such as genetic hitchhiking, and that divergence in these regions is accentuated in the presence of gene flow.

Genomic, Habitat, and Leaf Shape Analyses Reveal a Possible Cryptic Species and Vulnerability to Climate Change in a Threatened Daisy

“…pannosa were not reproductively isolated, then the strong signal of genetic structure we observe between such geographically close collection localities inhabiting very similar environments is difficult to explain. The advance in sequencing technologies in recent years has led to numerous studies that have unearthed previously unrecognised 'cryptic species' [71][72][73][74][75][76][77][78][79]. These are genetically distinct taxa that are classified as the same species due to morphological similarity [80].…”

A genomic and morphometric analysis of alpine bumblebees: ongoing reductions in tongue length but no clear genetic component

“…Bumblebees were collected on seven different mountains in Colorado, USA, with an average distance of 54 km between mountains (greatest distance: 134 km, Quail Mountain -Niwot Ridge; shortest distance: 10km, Mount Democrat -Pennsylvania Mountain). The existence of "incognitus" was unknown to us when the bees were sampled but a large fraction of bees identified as B. sylvicola were subsequently assigned to "incognitus" on the basis of genetic analysis (Christmas et al, 2021). Three of these mountains (Mount Evans, Niwot Ridge, and Pennsylvania Mountain) were also sampled previously by Miller-Struttmann et al (2015).…”

“…The genetic structure of populations is an important factor for interpretation of genotypephenotype correlations and the cause of morphological shifts. We previously presented a genome assembly of B. sylvicola and analyzed genome-wide variation by resequencing 281 samples (Christmas et al, 2021). This identified the presence of a previously-undetected cryptic species, which we gave the preliminary name Bombus incognitus.…”

“…These localities have an average separation of 54 km between each other, and consist of alpine tundra separated by forest. We analyze these data together with the previously-published population genomic dataset of 284 samples of B. sylvicola and "incognitus" from the same localities (Christmas et al, 2021). We use these data to assess whole-genome variation and its connection to geographical and morphological variation in these populations, which were previously studied by Miller-Struttmann et al (2015).…”

Capturing the rapidly evolving study of adaptation

“…When genome scale datasets started accumulating, the obvious methodological choice was to score the same kind of statistics at each position of the genome as previously used on one or a few genetic markers, for instance F ST . These SNP-by-SNP "scans" of the genome -and related approaches such as averaging a given statistic over several SNPs in a window -are still common, useful and used, also in our own work (Christmas et al, 2021;Jones et al, 2019;Raffini et al, 2017;Xiong et al, 2021). However, these approaches are now being complemented by other analytical tools that capitalize on patterns of covariation.…”