Substantial genetic divergence and lack of recent gene flow support cryptic speciation in a colour polymorphic bumble bee (Bombus bifarius) species complex

Abstract

Phenotypic polymorphism can constitute an inherent challenge for species delimitation. This issue is exemplified in bumble bees (Bombus), where species can exhibit high colour variation across their range, but otherwise exhibit little morphological variation to distinguish them from close relatives. We examine the species status of one of the most abundant North American bumble bees, Bombus bifarius Cresson, which historically comprised two major taxa, bifarius s.s. and nearcticus. These lineages are recognized primarily by red and black variation in their mid-abdominal coloration; however, a continuum from black (nearcticus) to red (bifarius s.s.) variation has led to their historic synonymization. Integrating mitochondrial and nuclear data and whole-genome sequencing, we reveal a high level of both mitochondrial and nuclear divergence delimiting two morphologically cryptic species -the red bifarius s.s. and the colour-variable (black to red) nearcticus. Population genomic analysis supports an absence of recent genomic admixture and a strong population structure between the two clades, even in sympatry. Species distribution models predict partially differentiated niches between the genetically inferred clades with annual precipitation being a leading differentiating variable. The bifarius s.s. lineage also occupies significantly higher elevations, with regions of sympatry being among the highest elevations in nearcticus. Our data also support a subspecies-level divergence between the broadly distributed nearcticus and the island population vancouverensis. In this paper, we formally recognize the two species, Bombus bifarius Cresson and Bombus vancouverensis Cresson, the latter including the subspecies B. vancouverensis vancouverensis comb.n. and B. vancouverensis nearcticus comb.n., with vancouverensis the name bearer due to year priority.

De Novo Genome Assemblies for Three North American Bumble Bee Species: Bombus bifarius, Bombus vancouverensis, and Bombus vosnesenskii

“…Although haploid males allow sequencing of phased haplotypes, there was not a clear influence of ploidy of starting material (haploid male for B. bifarius, diploid worker for B. vancouverensis, two haploid males for B. vosnesenskii) on the final assembly quality in terms of N50 or BUSCO scores (Table 3). Finally, we also confirm that sequences from B. bifarius and B. vancouverensis assemblies for two genes previously employed as diagnostic evidence for species delimitation (Ghisbain, et al 2020) were representative of the diversity found in each species (Figure 3A, B).…”

“…Finally, using the completed assemblies, we tested that genomes for B. bifarius and B. vancouverensis, two sister species in a morphologically cryptic complex (Ghisbain et al 2020), were representative of diversity for their respective lineages. To confirm that our new genomes reflect these newly delimited species, we examined two nuclear genes (serrate RNA effector and sodium/ potassium-exchanging ATPase subunit alpha) that were previously determined to produce diagnostic haplotypes for B. bifarius and B. vancouverensis and were employed for species delimitation in samples from throughout the B. bifarius -B. vancouverensis range (Ghisbain et al 2020). We used blast to identify the relevant regions from the assemblies before aligning with GenBank sequences for the two species (NCBI PopSet 1803131478 for the RNA effector; PopSet 1803131398 for the ATPase) and generated a neighbor-joining distance tree (Jukes Cantor model) in Geneious Prime 2020.1.1 (Biomatters, Aukland NZ).…”

Local adaptation across a complex bioclimatic landscape in two montane bumble bee species

“…Bombus vosnesenskii and Bombus vancouverensis workers were collected as previously reported (Jackson et al, 2018), although some new localities and samples are included here that were previously excluded for small sample sizes (Table S1). Importantly, the species name B. vancouverensis was recently resurrected for the Bombus bifarius subspecies nearcticus lineage included in this study, and our samples represent the new species B. vancouverensis subspecies nearcticus (Ghisbain et al, 2020). Samples were filtered to retain one bee per colony as in Jackson et al (2018).…”

“…To investigate targets of selection we performed genome scans in two species, Bombus vancouverensis (which was recently redescribed, and corresponds to the prior name Bombus bifarius subspecies nearcticus; Ghisbain et al, 2020) and Bombus vosnesenskii, that are good models because of their broad latitudinal and elevational ranges in the Sierra-Cascade regions of California, Oregon, and Washington, U.S.A. (Jackson et al, 2018;Stephen, 1957). We employed restriction site-associated DNA sequencing (RADseq), a powerful tool for detecting selection in wild populations (Andrews, Good, Miller, Luikart, & Hohenlohe, 2016;Catchen et al, 2017).…”

Contribution to the knowledge of the bumblebee fauna of Afghanistan (Hymenoptera, Apidae, Bombus Latreille)

“…Bumblebees (Hymenoptera: Apidae: genus Bombus) constitute a key group of widespread cold-adapted insects, substantially contributing to ecosystem services around the globe through the pollination of numerous wild plants and agricultural crops (Velthuis and van Doorn 2006;Klein et al 2007). These large colorful bees, represented by ~ 260 described species worldwide (Williams et al 1998), form an increasingly popular model group for large-scale studies in the fields of biogeography (Williams et al 2017), population genetics (Ghisbain et al 2020), evolutionary biology (Tian et al 2019) and more worryingly, global change biology (Kerr et al 2015;Rasmont et al 2015). Bumblebee populations are indeed undergoing serious regressions worldwide, mostly attributable to anthropogenic disturbance such as habitat destruction or climate change (Williams and Osborne 2009;Cameron et al 2011;Cameron and Sadd 2020;Rollin et al 2020).…”