Genomic Signals of Adaptation towards Mutualism and Sociality in Two Ambrosia Beetle Complexes

Abstract

Mutualistic symbiosis and eusociality have developed through gradual evolutionary processes at different times in specific lineages. Like some species of termites and ants, ambrosia beetles have independently evolved a mutualistic nutritional symbiosis with fungi, which has been associated with the evolution of complex social behaviors in some members of this group. We sequenced the transcriptomes of two ambrosia complexes (Euwallacea sp. near fornicatus⁻Fusarium euwallaceae and Xyleborus glabratus⁻Raffaelea lauricola) to find evolutionary signatures associated with mutualism and behavior evolution. We identified signatures of positive selection in genes related to nutrient homeostasis; regulation of gene expression; development and function of the nervous system, which may be involved in diet specialization; behavioral changes; and social evolution in this lineage. Finally, we found convergent changes in evolutionary rates of proteins across lineages with phylogenetically independent origins of sociality and mutualism, suggesting a constrained evolution of conserved genes in social species, and an evolutionary rate acceleration related to changes in selective pressures in mutualistic lineages.

Keywords: ambrosia beetle complexes; mutualism; polyphagous shot hole borer; redbay ambrosia beetle; sociality evolution.

Figure 1

(a) Time-calibrated phylogeny based on 98 sequences from single-copy orthologs and mutualist-social behavior categories. (b) Single copy ortholog groups with substitution rate variations associated with mutualistic nutritional symbiosis with fungi. (c) Single copy ortholog groups with substitution rate variations associated with social behavior. α: Isoptera + Thysanoptera + Hymenoptera + Coleoptera; β: Thysanoptera +Hymenoptera + Coleoptera; γ: Coleoptera.