Eusocial insects are characterized by several traits, including reproductive division of labor and caste polymorphisms, which likely modulate genome evolution. Concomitantly, evolution may act on specific genes and pathways underlying these novel, sociality-associated phenotypes. Reproductive division of labor should increase the magnitude of genetic drift and reduce the efficacy of selection by reducing effective population size. Caste polymorphism has been associated with relaxed selection and may facilitate directional selection on caste-specific genes. Here, we use comparative analyses of 22 ant genomes to test how reproductive division of labor and worker polymorphism influence positive selection and selection intensity across the genome. Our results demonstrate that worker reproductive capacity is associated with a reduction in the degree of relaxed selection but is not associated with any significant change to positive selection. We find decreases in positive selection in species with polymorphic workers, but no increase in the degree of relaxed selection. Finally, we explore evolutionary patterns in specific candidate genes associated with our focal traits in eusocial insects. Two oocyte patterning genes previously implicated in worker sterility evolve under intensified selection in species with reproductive workers. Behavioral caste genes generally experience relaxed selection associated with worker polymorphism, whereas vestigial and spalt, both associated with soldier development in Pheidole ants, experience intensified selection in worker polymorphic species. These findings expand our understanding of the genetic mechanisms underlying elaborations of sociality. The impacts of reproductive division of labor and caste polymorphisms on specific genes illuminate those genes’ roles in generating complex eusocial phenotypes.
The evolution of eusociality requires that individuals forgo some or all their own reproduction to assist the reproduction of others in their group, such as a primary egg-laying queen. A major open question is how genes and genetic pathways sculpt the evolution of eusociality, especially in rudimentary forms of sociality—those with smaller cooperative nests when compared with species such as honeybees that possess large societies. We lack comprehensive comparative studies examining shared patterns and processes across multiple social lineages. Here we examine the mechanisms of molecular convergence across two lineages of bees and wasps exhibiting such rudimentary societies. These societies consist of few individuals and their life histories range from facultative to obligately social. Using six species across four independent origins of sociality, we conduct a comparative meta-analysis of publicly available transcriptomes. Standard methods detected little similarity in patterns of differential gene expression in brain transcriptomes among reproductive and non-reproductive individuals across species. By contrast, both supervised machine learning and consensus co-expression network approaches uncovered sets of genes with conserved expression patterns among reproductive and non-reproductive phenotypes across species. These sets overlap substantially, and may comprise a shared genetic “toolkit” for sociality across the distantly related taxa of bees and wasps and independently evolved lineages of sociality. We also found many lineage-specific genes and co-expression modules associated with social phenotypes and possible signatures of shared life-history traits. These results reveal how taxon-specific molecular mechanisms complement a core toolkit of molecular processes in sculpting traits related to the evolution of eusociality.
more » « less- Award ID(s):
- 1929239
- NSF-PAR ID:
- 10469660
- Editor(s):
- Webster, Matthew
- Publisher / Repository:
- Oxford
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 15
- Issue:
- 1
- ISSN:
- 1759-6653
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/gbe/evac174
