Research
Research
Evolution
Phylogeography of Bombus huntii using whole-genome sequences from natural history collection specimens
Bumble bees are widespread pollinators, and species often span heterogeneous landscapes with varying environmental complexity. Complex topography, along with historical climate, can shape genetic diversity and act as barriers to gene flow, potentially leading to speciation. Bombus huntii is a bumble bee species featuring a broad geographic range, spanning from the southern portion of Canada, the western United States, to the central portion of Mexico. Prior microsatellite work identified signatures of population structure between the northern portion of B. huntii's range, in the United States and Canada, and the northern and central portions in Mexico. Utilizing a newly assembled reference genome and whole-genome resequencing of natural history collection specimens, we aimed to characterize patterns of population structure, genetic diversity, and inbreeding for northern and southern populations of B. huntii and test for potential speciation based on prior microsatellite results. We found strong population structure between the northern and southern lineages and identified reduced genetic diversity in the southern populations with evidence of increased inbreeding compared to the north. Our phylogenomic results lacked strong support for splitting the north and south populations into separate species, with demographic analysis suggesting some gene flow in the direction of south to north. Overall, our results suggest that while there is a lack of strong support for speciation occurring between these two geographic populations, there is evidence of decreased genetic diversity and increased levels of inbreeding in the Mexico population, indicating that these two populations do warrant consideration as evolutionary significant units.
Introduction
Introduction
Bumble bees are important pollinators in both agricultural and wildland settings. Bumble bee species often have broad geographic ranges that span heterogeneous landscapes, and for taxa that inhabit montane areas, such landscape complexity can impose barriers to gene flow between populations and potentially drive speciation. In part due to such large geographic ranges, species delimitation has historically been difficult in bumble bees, and taxonomic uncertainty has been widespread across the genus. Molecular data has facilitated investigation of species status in bumble bees by assisting with identification of evolutionary independent lineages, and several recent genetic studies within bumble bees have helped clarify existing taxonomy or identify intraspecific lineages that could be elevated to species. Even in the absence of species divergence, investigating population dynamics can be fruitful for uncovering genetically isolated populations and varying levels of genetic diversity across species ranges. The shift from small numbers of genetic markers to genome-scale data has improved the ability to reveal historical demographic patterns. Genome-wide investigation of bumble bees near the species level is becoming increasingly important for biological conservation of imperiled species and commercial development of native species for agricultural pollination. Specifically, these data have improved the capacity to identify cryptic species, evolutionary significant units, and reduced levels of genetic variation.
Bombus huntii is a widespread bumble bee found throughout western North America, ranging from southern British Columbia in Canada to the north, to the Trans-Mexican Volcanic Belt in the south. Bombus huntii is an effective agricultural pollinator due to its native abundance, capacity for captive rearing, and its effective pollination of obligate buzz-pollination crops such as tomatoes and is now a managed native pollinator in western North America. Growing recognition of this species' economic importance highlights the value of more genetic and genomic data to better assess population health, ecological traits, and evolutionary lineages. Such information can improve our understanding of B. huntii as a North American pollinator and guide efforts to preserve regional genetic diversity. Understanding regional signatures of population structure and genetic diversity is especially important when it comes to commercial pollination. Movement of commercial pollinator species into regions with differing genetic backgrounds poses the risk of eroding unique genetic variation present in the native population as well as the possibility of the commercial pollinators outcompeting the native population for local resources. Therefore, gaining a comprehensive understanding of B. huntii population structure and genetic diversity is essential for mitigating potential risks as the commercial use of B. huntii as a pollinator continues to expand.
A previous microsatellite study of B. huntii investigated population structure and diversity across the United States, Canada, and Mexico, and identified strong population structure between samples comprising populations primarily in the United States and Canada with those from Mexico. This study also identified important effects from Pleistocene climate dynamics, with populations of B. huntii in regions that have been more climatically unstable during the Pleistocene, corresponding to higher latitudes in the northern part of B. huntii's range, actually featuring greater levels of genetic diversity compared to B. huntii populations in the south, where the climate has been more stable during the last glacial-interglacial period. The contemporary distribution of climatically suitable habitat provides a hypothesis for the observed patterns of population structure, with more northern portions of B. huntii's range featuring large continuous regions of suitable habitat, while B. huntii in Mexico occupies a much more fragmented montane landscape where it largely occurs at higher elevations. Thus, in the north, B. huntii likely has the potential for widespread gene flow, while southern populations may have limited dispersal with the northern populations and each other, resulting in reduced genetic connectivity and diversity. The strong population structure identified in combined with recent discovery (or rediscovery) of other bumble bee species using molecular data, has raised some interest in testing the species status of B. huntii populations and whether these populations may harbor evolutionarily distinct genomic variation. The recent publication of a reference genome for B. huntii enables an examination of this possibility using genome-wide data to test the species status of B. huntii, similar to recent assessments in other bumble bees.
With some bumble bee species declining, developing low-harm sampling approaches that reduce the need to sacrifice bees for collecting genetic data will become an increasingly attractive avenue for researchers. The availability of bumble bees in natural history collections has the potential to open the door for genomic studies that minimize the need for new sampling from potentially sensitive natural populations. Modern shotgun library preparation methods allow whole-genome resequencing from small amounts of DNA from museum specimens, and the large amount of genetic data from whole genomes allows for robust inferences even from relatively few samples. In this study, we use specimens housed in natural history collections for whole-genome resequencing of B. huntii throughout its geographic range to examine the effectiveness of bumble bee "museomics" to pursue phylogenomic and population genomic analyses. We test the hypothesis that the B. huntii found in Mexico could be recognized as a unique species (independent evolutionary lineage) from the samples found in the United States and Canada, or if the species may otherwise harbor unique patterns of genetic diversity that warrant consideration as an evolutionary significant unit. To achieve this goal, we characterize genome-wide population genetic signatures including population structure and genetic diversity at multiple scales (locality, individual, and genome). Furthermore, to test our speciation hypothesis, we employed multiple phylogenetic tools and performed demographic reconstruction.