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

Abstract

Understanding evolutionary responses to variation in temperature and precipitation across species ranges is of fundamental interest given ongoing climate change. The importance of temperature and precipitation for multiple aspects of bumble bee (Bombus) biology, combined with large geographic ranges that expose populations to diverse environmental pressures, make these insects well‐suited for studying local adaptation. Here, we analyzed genome‐wide sequence data from two widespread bumble bees, Bombus vosnesenskii and Bombus vancouverensis, using multiple environmental association analysis methods to investigate climate adaptation across latitude and altitude. The strongest signatures of selection were observed in B. vancouverensis, but despite unique responses between species for most loci, we detected several shared responses. Genes relating to neural and neuromuscular function and ion transport were especially evident with respect to temperature variables, while genes relating to cuticle formation, tracheal and respiratory system development, and homeostasis were associated with precipitation variables. Our data thus suggest that adaptive responses for tolerating abiotic variation are likely to be complex, but that several parallels among species can emerge even for these complex traits and landscapes. Results provide the framework for future work into mechanisms of thermal and desiccation tolerance in bumble bees and a set of genomic targets that might be monitored for future conservation efforts.

Biogeographic parallels in thermal tolerance and gene expression variation under temperature stress in a widespread bumble bee

“…The map was created in ESRI ArcMap 10.8, with state outlines and digital elevation data obtained from https ://www.diva-gis.org/Data. The B. vosnesenskii range outline was taken from the species distribution model published perviously 3,33 . (B) Mean monthly temperatures over the course of a year for queen collecting sites.…”

“…1). B. vosnesenskii occurs across broad altitudinal ranges throughout its distribution, and is characterized by weak genetic differentiation (genome-wide F ST = 0.003), facilitating identification of strong local effects with little confounding influence from population structure 3,33 . We employed a common-garden style approach with laboratory colonies reared from queens collected at high and low elevations at both high and low latitudes to separate species-wide responses to thermal stress from population-specific differences that may reflect local adaptation.…”

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

“…Such patterns may reflect some true rearrangements between the focal species assemblies and B. terrestris genome that have occurred over 18-20 million years of divergence but may also be the result of a small number of assembly artifacts. Our focused MAUVE analysis of the region containing a high density of putatively adaptive loci from prior studies (including a possible color-associated gene Xanthine dehydrogenase/oxidase-like; Pimsler et al 2017;Ghisbain et al 2020;Jackson et al 2020) revealed a single collinear block ( Figure 5A, B). This suggests no major rearrangements in the new genomes with respect to the B. impatiens genome previously used as a reference genome for population genomics in these species.…”

“…We expect these new references will quickly become useful for bumble bee biologists. For example, the species included here have all recently been studied with genomic data to detect the influence of climate and landscape composition on dispersal and local adaptation (Jackson et al 2018;Jackson et al 2020;Mola et al 2020), however, such studies have largely been limited to genome-reduction methods (e.g., RAD-seq) and have required cross-species mapping to available reference genomes. These new assemblies will open the door for more extensive whole genome resequencing to uncover unique genomic variation that may be shaped by environmental conditions for each species (Fuentes-Pardo and Ruzzante 2017).…”

“… ( Figure 1 ). These species are among the most common bumble bees in western North America ( Koch et al 2012 ) and have been the focus of recent research that includes studies investigating gene flow, foraging range, and genetic diversity in natural and agricultural systems ( Lozier et al 2011 , 2016 ; Rao and Strange 2012 ; Jha and Kremen 2013 ; Jha 2015 ; Geib et al 2015 ; Jackson et al 2018 ; Mola et al 2020 ), climate-driven local adaptation across spatial-environmental gradients ( Jackson et al 2020 ), and color pattern variation and speciation ( Pimsler et al 2017 ; Ghisbain et al 2020 ).…”