Genomic Signatures of Recent Adaptation in a Wild Bumblebee

Abstract

Environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects respond to environmental pressures. To understand the genomic bases of adaptation in an ecologically important pollinator, we analyzed genomes of Bombus terrestris bumblebees collected across Great Britain. We reveal extensive genetic diversity within this population, and strong signatures of recent adaptation throughout the genome affecting key processes including neurobiology and wing development. We also discover unusual features of the genome, including a region containing 53 genes that lacks genetic diversity in many bee species, and a horizontal gene transfer from a Wolbachia bacteria. Overall, the genetic diversity we observe and how it is distributed throughout the genome and the population should support the resilience of this important pollinator species to ongoing and future selective pressures. Applying our approach to more species should help understand how they can differ in their adaptive potential, and to develop conservation strategies for those most at risk.

Signatures of Adaptation, Constraints, and Potential Redundancy in the Canonical Immune Genes of a Key Pollinator

“…As a provisional step to examine different selective pressures acting on canonical immune genes, we assessed the genetic diversity found within the sequenced genomes of 33 wild-sampled B. terrestris males. We identified 1,103,300 million high-quality biallelic single-nucleotide polymorphisms (SNPs) with a sliding window-based analysis (window size: 100 kb) estimating mean genome-wide nucleotide diversity (π) as 1.71 × 10 −3 ( supplementary table S2 a , Supplementary Material online), similar to diversity estimates calculated for a British population of B. terrestris (1.51 × 10 −3 ; Colgan et al 2022 ). In terms of the canonical immune genes that were analyzed ( n = 166 genes found on chromosomal scaffolds), we found no significant difference in terms of mean nucleotide diversity between them and either all other nonimmune genes (Wilcoxon rank sum test; W = 789815, P = 0.098) or a similar number of size-matched nonimmune genes (Wilcoxon rank sum test: W = 13668, P = 0.397).…”

“…Dashed horizontal lines indicate thresholds of positive selection (| n S L | = 2) and those within the top 1% of genome-wide SNPs (| n S L | = 2.51). ( B ) The correlation of absolute | n S L | scores calculated for the present data set consisting of Bombus terrestris males sampled in Ireland (“population 1”) and publicly available scores for a British population (“population 2”) generated by Colgan et al (2022) , highlighting conservation in signatures of positive selection in geographically separated populations. Dashed vertical and horizontal lines indicate thresholds of selection (| n S L | score ≥ 2) in each population.…”

“…To determine if canonical immune genes are experiencing similar forms of selection in other populations, we compared the | n S L | scores assigned to such genes in our data set with those previously published by Colgan et al (2022) , which involved analysis of male B. terrestris sampled across the island of Great Britain. We found a significant positive correlation (Pearson correlation coefficient [ R ] = 0.48, P < 0.0001; fig.…”

“…Declines in pollinator populations, including bumblebees ( Fitzpatrick et al 2007 ; Kosior et al 2007 ; Cameron et al 2011 ), have led to concern about the sustainability of pollination services provided by insects which greatly contribute to global economies, food security, and ecosystem functioning ( Aizen et al 2009 ; Stout et al 2019 ). Our understanding of the capacity of wild bee populations to respond to ongoing environmental threats has been greatly informed by recent studies using population genomics, which have highlighted the genetic variation harbored in a population, as well as the targets of recent positive selection acting throughout the genome ( Harpur and Rehan 2021 ; Colgan et al 2022 ; Heraghty et al 2022 ; Kardum Hjort et al 2022 ), including immune genes ( Kent et al 2018 ). However, despite the importance of hymenopteran insects such as bees, wasps, and ants, focused population genetic studies on their immune genes are limited.…”

Individual-based Modeling of Genome Evolution in Haplodiploid Organisms

“…Simulations are used to generate null distributions of common measures of genetic diversity and selection ( Voight et al 2006 ; Bank et al 2014 ; Ferrer-Admetlla et al 2014 ), to compare competing hypotheses about the demographic and evolutionary histories of populations ( Excoffier et al 2013 ; Enard et al 2014 ; Adrion et al 2020 ), and to predict the effects of environmental changes on different species ( DeAngelis and Mooij 2005 ; Owens and Samuk 2020 ). The absence of a simulation framework incorporating haplodiploidy has limited the exploration of genomic models of social evolution and the accurate interpretation of population genomic data for bees, ants, and other important species ( Favreau et al 2018 ; López-Osorio and Wurm 2020 ; Colgan et al 2022 ).…”