Genetic architecture of key social trait differs significantly between primitive and advanced eusocial species

Abstract

The one trait that differentiates social and eusocial insects from solitary insects is reproductive division of labor (i.e., one or a few individuals of a group reproduce and others work). Currently, the general consensus of the molecular and behavioral underpinnings of social evolution is based on ideas in evolutionary developmental biology in which novel traits are linked to changes in regulatory mechanisms rather than novel genes (1⇓⇓–4). This is in particular true for a trait such as reproductive division of labor, because during the early stages of social evolution all individuals had the same reproductive potential (i.e., the trait was phenotypically plastic). It was only later in social evolution when the determination of queen versus worker was shifting from behavioral interactions between omnipotent individuals to developmental mechanisms that reacted to environmental conditions provided by the colony or environment [e.g., differential feeding (5)] that phenotypic plasticity of adult individuals was reduced. For example, in some highly derived ant species, workers emerge with no or nonfunctional ovaries and thus are true “somatic cells” of a superorganism (6). In PNAS, Patalano et al. (7) sequenced the genomes, brain transcriptomes, and methylomes of two eusocial species in which caste determination is still highly plastic (Polistes) or has reversed from a caste determination with a dedicated reproductive caste (queens) to the ancestral state with omnipotent individuals competing for reproductive rights by evolutionarily “losing” the queen phenotype (Dinoponera). Hence, this study gives us a rare glimpse into the genome organization and molecular mechanisms that represent or resemble the earliest stages in social evolution where reproductive castes were not yet fixed or …