The evolution of soldier reproduction in social thrips

We estimated the degree of reproductive differentiation between foundresses and soldiers in multiple populations of five species of haplodiploid Australian gall-forming thrips using microsatellite data, ovarian dissections, and census data. Microsatellite-based species estimates of average per capita reproductive output of soldiers relative to the foundresses ranged from 0.005 to 0.64, and dissection and census-based estimates ranged from 0.17 to 1.1. Mapping of these estimates onto a phylogeny showed that levels of soldier reproduction were apparently higher in three basal lineages than in two more derived lineages. We infer from this phylogenetic pattern that soldier morphology and behavior of thrips evolved in the presence of substantial levels of soldier reproduction. This pattern of evolutionary change is similar to that proposed for the origin of soldiers in aphids and termites, but it differs from the scenario proposed for the origin of workers in Hymenoptera, within which helping and strong reproductive division of labor apparently evolved before morphological differentiation. We suggest that this difference in evolutionary routes to eusociality between taxa with soldiers and taxa with foraging workers was driven by a weaker trade-off between helping and reproducing, and a greater ability of the helpers to withstand reproductive domination, in taxa with soldiers. This is the first study to analyze the social-evolutionary trajectories of reproductive, behavioral, and morphological differentiation in the context of a species-level phylogeny.