Abstract
BackgroundReproductive division of labor in eusocial insects is a striking example of a shared genetic background giving rise to alternative phenotypes, namely queen and worker castes. Queen and worker phenotypes play major roles in the evolution of eusocial insects. Their behavior, morphology and physiology underpin many ecologically relevant colony-level traits, which evolved in parallel in multiple species.ResultsUsing queen and worker transcriptomic data from 16 ant species we tested the hypothesis that conserved sets of genes are involved in ant reproductive division of labor. We further hypothesized that such sets of genes should also be involved in the parallel evolution of other key traits. We applied weighted gene co-expression network analysis, which clusters co-expressed genes into modules, whose expression levels can be summarized by their ‘eigengenes’. Eigengenes of most modules were correlated with phenotypic differentiation between queens and workers. Furthermore, eigengenes of some modules were correlated with repeated evolution of key phenotypes such as complete worker sterility, the number of queens per colony, and even invasiveness. Finally, connectivity and expression levels of genes within the co-expressed network were strongly associated with the strength of selection. Although caste-associated sets of genes evolve faster than non-caste-associated, we found no evidence for queen- or worker-associated co-expressed genes evolving faster than one another.ConclusionsThese results identify conserved functionally important genomic units that likely serve as building blocks of phenotypic innovation, and allow the remarkable breadth of parallel evolution seen in ants, and possibly other eusocial insects as well.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-0902-7) contains supplementary material, which is available to authorized users.
Highlights
Reproductive division of labor in eusocial insects is a striking example of a shared genetic background giving rise to alternative phenotypes, namely queen and worker castes
To test the hypothesis that conserved sets of genes are involved in queen/worker phenotypic differentiation, we investigated the relationship between the eigengenes and the caste phenotypic traits, while controlling for any phylogenetic bias in the dataset, using a phylogenetic mixed model implemented in the MCMCglmm package [45]
We focused on traits most likely arising from queen–worker differences, which was the major axis of variation in the data set, it is possible that the same modules may play a role in a wide variety of other traits
Summary
Reproductive division of labor in eusocial insects is a striking example of a shared genetic background giving rise to alternative phenotypes, namely queen and worker castes. To understand the molecular mechanisms underlying social insect polymorphism, previous studies have primarily examined caste-biased gene expression patterns in a small number of distantly related species, typically across separate origins of eusociality [19,20,21,22,23,24,25]. These studies have found a small number of genes repeatedly associated with reproductive division of labor, but a comprehensive, comparative characterization of queen and worker transcriptional architecture has been lacking
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