Abstract
Eusociality has convergently evolved multiple times, but the genomic basis of caste-based division of labor and degree to which independent origins of eusociality have utilized common genes remain largely unknown. Here we characterize caste-specific transcriptomic profiles across development and adult body segments from pharaoh ants (Monomorium pharaonis) and honey bees (Apis mellifera), representing two independent origins of eusociality. We identify a substantial shared core of genes upregulated in the abdomens of queen ants and honey bees that also tends to be upregulated in mated female flies, suggesting that these genes are part of a conserved insect reproductive groundplan. Outside of this shared groundplan, few genes are differentially expressed in common. Instead, the majority of the thousands of caste-associated genes are plastically expressed, rapidly evolving, and relatively evolutionarily young. These results emphasize that the recruitment of both highly conserved and lineage-specific genes underlie the convergent evolution of novel traits such as eusociality.
Highlights
Eusociality has convergently evolved multiple times, but the genomic basis of caste-based division of labor and degree to which independent origins of eusociality have utilized common genes remain largely unknown
The number of differentially expressed genes (DEGs) between queens and workers increased throughout development, peaking in the adult abdomen (Fig. 1a)
The top enriched Gene Ontology (GO) terms for caste-associated DEGs in each species were dominated by metabolism, signaling, and developmental processes (Supplementary Tables 3, 4)
Summary
Eusociality has convergently evolved multiple times, but the genomic basis of caste-based division of labor and degree to which independent origins of eusociality have utilized common genes remain largely unknown. Previous work has mainly focused on identifying whether there is significant overlap of genes or gene pathways associated with caste-based division of labor between independent lineages[23,26,27], but there has been little effort to quantify the relative importance of shared versus unshared genes to the convergent evolution of caste-based division of labor Most of these studies have either focused on the brain or whole-body samples[15,22,24,26,33,35,36,37], expression bias between queens and workers has been shown to be dependent upon developmental stage and tissue type[34,38,39,40]. Outside of this shared core, few genes are differentially expressed in both species in the same tissue or developmental stage, and genes with high degrees of caste-biased expression tend to be weakly constrained in terms of expression profile and sequence evolution
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