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. Significance Most hypotheses explaining the evolution of sociality in insects assume that positive selection drives the evolution of worker traits. Yet we know little about the extent of natural selection acting on social insects. We produced a map of positive selection for the honey bee through analysis of 40 individual genomes. We found strong evidence of positive selection acting on genes and regulatory sequences, and we discovered that mutations in worker-biased proteins tend to have greater fitness effects than mutations in queen-biased proteins. We also found many instances of positive selection acting on genes that influence worker traits, suggesting that worker phenotypes represent a major vector for adaptation in social insects.

The rise of insect societies, marked by the formation of reproductive and sterile castes, represents a major unsolved mystery in evolution. Across several independent origins of sociality, the genomes of social hymenopterans share two peculiar attributes: high recombination and low but heterogeneous GC content. For example, the genome of the honey bee,Apis mellifera, represents a mosaic of GC-poor and GC-rich regions with rates of recombination an order of magnitude higher than in humans. However, it is unclear how heterogeneity in GC content arises, and how it relates to the expression and evolution of worker traits. Using population genetic analyses, we demonstrate a bias in the allele frequency and fixation rate of derived C or G mutations in high-recombination regions, consistent with recombination’s causal influence on GC-content evolution via biased gene conversion. We also show that recombination and biased gene conversion actively maintain the heterogeneous GC content of the honey bee genome despite an overall A/T mutation bias. Further, we found that GC-rich genes and intergenic regions have higher levels of genetic diversity and divergence relative to GC-poor regions, also consistent with recombination’s causal influence on the rate of molecular evolution. Finally, we found that genes associated with behavior and those with worker-biased expression are found in GC-rich regions of the bee genome and also experience high rates of molecular evolution. Taken together, these findings suggest that recombination acts to maintain a genetically diverse and dynamic part of the genome where genes underlying worker behavior evolve more quickly.

1. Adaptation through natural selection is the natural response of bee populations to environmental changes and the challenge of pests and diseases. The richness in biodiversity of races and ecotyp...

The genomes of eusocial insects have a reduced complement of immune genes—an unusual finding considering that sociality provides ideal conditions for disease transmission. The following three hypotheses have been invoked to explain this finding: 1) social insects are attacked by fewer pathogens, 2) social insects have effective behavioral or 3) novel molecular mechanisms for combating pathogens. At the molecular level, these hypotheses predict that canonical innate immune pathways experience a relaxation of selective constraint. A recent study of several innate immune genes in ants and bees showed a pattern of accelerated amino acid evolution, which is consistent with either positive selection or a relaxation of constraint. We studied the population genetics of innate immune genes in the honey bee Apis mellifera by partially sequencing 13 genes from the bee’s Toll pathway (∼10.5 kb) and 20 randomly chosen genes (∼16.5 kb) sequenced in 43 diploid workers. Relative to the random gene set, Toll pathway genes had significantly higher levels of amino acid replacement mutations segregating within A. mellifera and fixed between A. mellifera and A. cerana. However, levels of diversity and divergence at synonymous sites did not differ between the two gene sets. Although we detect strong signs of balancing selection on the pathogen recognition gene pgrp-sa, many of the genes in the Toll pathway show signatures of relaxed selective constraint. These results are consistent with the reduced complement of innate immune genes found in social insects and support the hypothesis that some aspect of eusociality renders canonical innate immunity superfluous.