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

<p>Phenotypic polymorphism can constitute an inherent challenge for species delimitation. This issue is exemplified in bumble bees (<i>Bombus</i>), 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, <i>Bombus bifarius</i> Cresson, which historically was comprised of two major taxa, <i>bifarius</i> <i>s.s.</i> (<i>sensu stricto</i>) and <i>nearcticus</i>. These sublineages are recognized primarily by red and black variation in their mid-abdominal coloration, however, a continuum from black (<i>nearcticus</i>) to red (<i>bifarius s.s.</i>) variation has led to their historic synonymisation. 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 <i>bifarius s.s.</i> and the color variable (black to red) <i>nearcticus</i>. 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<i> bifarius</i> <i>s.s. </i>lineage also occupies significantly higher elevations, with regions of sympatry being among the highest elevations in <i>nearcticus</i>. Our data also support a subspecies-level divergence between the broadly distributed <i>nearcticus</i> and the island population <i>vancouverensis</i>. In this paper, we formally recognize the two species, <i>Bombus</i> <i>bifarius</i> Cresson and <i>Bombus</i> <i>vancouverensis </i>Cresson, the latter including the subspecies <i>B. vancouverensis vancouverensis</i> <b>comb. n.</b> and <i>B. vancouverensis nearcticus</i> <b>comb. n</b>., with <i>vancouverensis </i>the name bearer due to year priority.</p> <p> </p>