Genes involved in convergent evolution of eusociality in bees

Abstract

Eusociality has arisen independently at least 11 times in insects. Despite this convergence, there are striking differences among eusocial lifestyles, ranging from species living in small colonies with overt conflict over reproduction to species in which colonies contain hundreds of thousands of highly specialized sterile workers produced by one or a few queens. Although the evolution of eusociality has been intensively studied, the genetic changes involved in the evolution of eusociality are relatively unknown. We examined patterns of molecular evolution across three independent origins of eusociality by sequencing transcriptomes of nine socially diverse bee species and combining these data with genome sequence from the honey bee Apis mellifera to generate orthologous sequence alignments for 3,647 genes. We found a shared set of 212 genes with a molecular signature of accelerated evolution across all eusocial lineages studied, as well as unique sets of 173 and 218 genes with a signature of accelerated evolution specific to either highly or primitively eusocial lineages, respectively. These results demonstrate that convergent evolution can involve a mosaic pattern of molecular changes in both shared and lineage-specific sets of genes. Genes involved in signal transduction, gland development, and carbohydrate metabolism are among the most prominent rapidly evolving genes in eusocial lineages. These findings provide a starting point for linking specific genetic changes to the evolution of eusociality. social evolution | social insects | sociogenomics | molecular phylogenetics

A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera

“…African and European bees differed in the AST gene encoding the juvenile hormone-inhibiting allatostatin, an Ih-like dopamine regulator, and the genes for several odorant receptors. We detected a nonsynonymous variant in the neuronal gene RhoGAP100F (Rho GTPase-activating protein at 100F), which evolves rapidly in highly social insect lineages 35 . We found highly differentiated SNPs in the exonic regions of key genes in the insulin-vitellogenin signaling pathway, which is important for queen longevity and for worker labor division 36 , including a large number of highly differentiated SNPs in the 3′ UTR of IhR (encoding the insulin-like receptor) and nonsynonymous SNPs in the foxo (forkhead box, subgroup O), Vg (vitellogenin) and yl (vitellogenin receptor) genes ( Supplementary Fig.…”

“…Further highly differentiated coding SNPs were found in many innate immune defense genes within the Toll and JAK-STAT pathways, including pll (pelle) and several serine proteases. pll was earlier detected as being quickly evolving in social insects 35 . Among the top coding A versus MC SNPs, we also detect significant (P = 0.012) enrichment for genes involved in platelet plug formation, which is activated to heal wounds and form infection barriers in insects 44 , including Hml (hemolectin) (Supplementary Fig.…”

Hemimetabolous genomes reveal molecular basis of termite eusociality

“…Therefore, identifying the molecular mechanisms common to both origins of eusociality is crucial to understanding the fundamental signatures of these rare evolutionary transitions. While the availability of genomes from many eusocial and non-eusocial hymenopteran species 8 has allowed extensive research into the origins of eusociality within ants and bees [9][10][11] , a paucity of genomic data from cockroaches and termites has precluded large-scale investigations into the evolution of eusociality in this hemimetabolous clade.The conditions under which eusociality arose differ greatly between the two groups. Termites and cockroaches are hemimetabolous and so show a direct development, while holometabolous hymenopterans complete the adult body plan during metamorphosis.…”

Molecular evolutionary analyses of insect societies

“…This study analyzed ∼3,600 genes from a set of 10 social and nonsocial bee transcriptomes; these species encompass three independent origins of eusociality (21). Hundreds of genes were identified that exhibit a molecular signature of rapid evolution associated with sociality, defined as a higher ratio of nonsynonymous-to-synonymous nucleotide substitutions (d N /d S ) in social relative to nonsocial bee lineages (21). Throughout this review, evidence for rapid evolution is based on relative d N /d S and positive selection is defined as d N /d S > 1, unless otherwise specified.…”