Shifts in bee diet breadths are associated with gene gains and losses and positive selection across olfactory receptors.

Abstract

Bees are palynivorous insects that vary widely in the number of plant families from which they collect pollen. Their evolutionary history has been marked by multiple transitions in diet breadth between specialists that only visit specific plant genera (narrow diet breadth) and generalists that visit multiple large plant families (broad diet breadth). Understanding the evolution of sensory systems associated with changes in the detection, discrimination, and gustation of different pollen in bees can shed light on the underlying genetic mechanisms associated with transitions between narrow and broad diet breadths. We conducted a comparative study of three families of insect olfactory receptor genes (odorant receptors (ORs), gustatory receptors (GRs), and ionotropic receptors (IRs)) linked to diet breadth across 51 bee species. We calculated rates of gene gains and losses and identified genes experiencing positive selection across specialist and generalist bees. Our results show that broad generalists exhibit high rates of OR gene losses and GR gene gains. We observed accelerated rates of evolution in seven orthologous groups of genes across specialists and one group in generalists. Several orthogroups showed diversification in putative ligand-binding domains of proteins, indicating potential shifts in functional properties of the receptors. Taken together, these results indicate that dietary specialization in bees requires chemosensory system diversification of existing genes while dietary generalization is associated with the loss of ORs and gain of GRs. Our study provides important insights into the genetic architecture underlying shifts in niche occupancy across insects.