Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Abstract

Most theories used to explain the evolution of eusociality rest upon two key assumptions: mutations affecting the phenotype of sterile workers evolve by positive selection if the resulting traits benefit fertile kin, and that worker traits provide the primary mechanism allowing social insects to adapt to their environment. Despite the common view that positive selection drives phenotypic evolution of workers, we know very little about the prevalence of positive selection acting on the genomes of eusocial insects. We mapped the footprints of positive selection in Apis mellifera through analysis of 40 individual genomes, allowing us to identify thousands of genes and regulatory sequences with signatures of adaptive evolution over multiple timescales. We found Apoidea- and Apis-specific genes to be enriched for signatures of positive selection, indicating that novel genes play a disproportionately large role in adaptive evolution of eusocial insects. Worker-biased proteins have higher signatures of adaptive evolution relative to queen-biased proteins, supporting the view that worker traits are key to adaptation. We also found genes regulating worker division of labor to be enriched for signs of positive selection. Finally, genes associated with worker behavior based on analysis of brain gene expression were highly enriched for adaptive protein and cis-regulatory evolution. Our study highlights the significant contribution of worker phenotypes to adaptive evolution in social insects, and provides a wealth of knowledge on the loci that influence fitness in honey bees.

Keywords: kin selection; natural selection; social evolution; taxonomically restricted genes.

Fig. 1.

Loci underpinning adaptive evolution in honey bees. Histogram of (A) the population-size scaled selection coefficient (γ) for 12,303 genes; γ ranges from −1.64 to 11.8, but we truncated the histogram at γ = 3 for readability. There are 88 genes with γ > 3. (B) Histogram of pairwise genetic differentiation (F_ST) between African and West European honey bees for 3,392,632 SNPs. F_ST histograms for the other five pairwise comparisons are found in Fig. S2. Areas in red represent outlier loci with signatures of adaptive evolution.

Fig. 2.

(A) Taxonomically restricted genes have higher rates of adaptive evolution. For genes with signs of positive selection (γ > 0), γ is significantly higher in Apis-restricted and Apoidea-restricted genes, intermediate in Hymenoptera-restricted genes, and lowest for genes found in other insect orders. (B) For genes with signs of negative selection (γ < 0), Apis-restricted genes have the highest levels of negative selection. Error bars denote SEM.

Fig. 3.

Genes associated with worker phenotypes show signs of adaptive evolution in honey bees. (A) Worker-biased proteins have significantly higher selection coefficients relative to queen-biased proteins, and nondifferentially expressed proteins (NDEG). Error bars denote SEM; **P < 0.01. (B) Genes causally associated with worker division of labor have very high selection coefficients in the honey bee.