Thomas William Chapman

We used microsatellite data to estimate levels of inbreeding in four species of solitary gall thrips that are in the same clade as the six species with soldier castes. Three of the four species were highly inbred (F_is 0.54–0.68), and the other apparently mated randomly (F_is near zero). These estimates, combined with previous data from species with soldiers, suggest that inbreeding is a pervasive life-history feature of the gall-inducing thrips on Australian Acacia. Mapping of inbreeding estimates onto the phylogeny of the gall inducers showed that the ancestral lineage that gave rise to soldiers was apparently highly inbred, and therefore, inbreeding could have played a role in the origin of sociality within this group. Moreover, there was a trend from high levels of inbreeding at the origin of soldiers to low levels in the most derived species with soldiers, which exhibits the highest levels of reproductive division of labor and soldier altruism. These patterns are consistent with considerations from population genetics, which show that the likelihood of the origin of soldier altruism is higher in inbreeding populations but that, once soldiers have evolved, a reduction in inbreeding levels may facilitate the evolution of enhanced division of labor and reproductive skew.

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.