GENELAB · The genetic basis of division of labor: testing the “reproductive groundplan hypothesis” in ants

The genetic basis of division of labor: testing the “reproductive groundplan hypothesis” in ants

The evolution and maintenance of cooperation in the face of inevitable conflicts, is regarded as one of the major questions in biology today. Answering this question requires understanding both the proximate basis of cooperative behavior and its comparative biology, but studies integrating experimental and comparative approaches are rare. Social insects are one of the pinnacles of sociality, with societies characterized by reproductive division of labour, one of the major evolutionary transitions in biological organization. While most of the research in the last century has focused on the ultimate reasons favoring cooperation, the methodological advances during the last decade has provided the tools necessary to study the genetic basis of cooperation directly. The “reproductive groundplan hypothesis” (RPGH) has emerged as one potentially powerful explanation for the proximate mechanisms for the evolution of eusociality. It postulates that conserved gene networks, which underlie the reproductive physiology and behavior of solitary insects, were co-opted and modified during the evolution of eusocial insects to generate worker division of labor. This hypothesis is potentially of fundamental and far-reaching importance for our understanding of the mechanistic basis by which eusociality evolved, but empirical evidence in support of the hypothesis is still limited to only a few species. This project combined large scale phylogenetic tests of the RPGH, with endocrinology, state of the art molecular techniques (RNA interference) and classic behavioral analysis, to investigate if the RPGH applies to ants and therefore represents a general explanatory framework for the evolution of division of labour in social insects. Utilizing an integrative we found strong support for the overall association between maternal physiology and maternal behavior tasks in ant workers. These results suggest that ants, similarly to bees, utilize ancestral regulatory networks to generate alternative behavioral castes. Using hormone manipulation (juvenile hormone) and gene knock down (vitellogenin) we were able to experimentally demonstrate that the highly social black garden ant Lasius niger, as well as the primitive eusocial and Dinoponera quadriceps seem to utilize an alternative regulatory architecture, compared to the honeybee, to generate the observed behavioral tasks. While vitellogenin likely has a similar function as observed in the honeybee, JH seem to have lost its pacemaker function in both species indicating that different regulatory pathways might generate worker DOL in different social insect clades. In summary this project provided strong support for the RGPH in ants and shed light on regulatory architecture regulating worker division of labor in social insects. We conclude that the RGPH represents a general explanatory framework for the evolution of division of labor in social insects and will proved fruitful insights in one of the most fundamental transitions in evolutionary history.

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