Genome sequencing and morphometric analysis of alpine bumblebees experiencing climate change reveal ongoing phenotypic shifts and a lack of population structure

Populations of the bumblebees Bombus sylvicola and Bombus balteatus in Colorado have experienced decreases in tongue length, a trait important for plant-pollinator mutualisms, in the last six decades. It is hypothesized that this reflects selection exerted by changes in floral composition under climate change. Here we combine extensive morphometric and population genomic data to investigate population structure, whether morphological change is ongoing, and the genetic basis of morphological change. We generate highly-contiguous genome assemblies of both species using long-read sequencing. We then perform whole-genome sequencing and morphometric measurements of 580 samples of these species from seven high-altitude localities. Out of 281 samples originally identified as B. sylvicola, 67 formed a separate genetic cluster comprising the newly-discovered cryptic species B. incognitus. However, there is very little additional genetic substructure, suggesting that gene flow occurs readily between mountains. We find a significant decrease in tongue length between bees collected between 2008-2014 and in 2017, indicating that morphological shifts are ongoing. We did not discover any genetic associations with tongue length, but a SNP related to production of a proteolytic digestive enzyme is implicated in body size variation. We identify evidence of covariance between kinship and both tongue length and body size, which is suggestive of a genetic component of these traits, although it is not possible to rule out shared environmental effects between colonies. Our results provide evidence for ongoing evolution of a morphological trait important for pollination and indicate that this trait likely has a complex genetic and environmental basis.