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.

Highlights

  • By definition, mutualistic symbiosis increases the fitness of all participant partners, at least in terms of inclusive fitness [1]

  • We identified ortholog genes among X. glabratus, E. nr. fornicatus, and other beetle species (Dendroctonus ponderosae, Leptinotarsa decemlineata, Tribolium castaneum, and Oryctes borbonicus) to gain insight into the selection acting on molecular traits related to the obligate mutualism, as well as to the facultative eusocial behavior displayed by these fungus-farming beetle species

  • We found that GlcAT-P is expressed in the head-thorax of E. nr. fornicatus, which points to an adaptation related to social behavior in ambrosia beetles

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Summary

Introduction

Mutualistic symbiosis increases the fitness of all participant partners, at least in terms of inclusive fitness [1]. Mutualistic lineages are interdependent, and natural selection drives their coevolution [2]. Nutritional mutualistic symbiosis with fungi has evolved over tens of millions of years in Attini ants, Macrotermitinae termites, and Scolytinae or Platypodinae ambrosia beetles, enabling these organisms to colonize new ecological niches [1,2]. Of these fungus-associated lineages, ambrosia beetles are probably the least studied, and constitute an interesting model system for studying the evolutionary transition to an obligate mutualism in insects

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