The Evolutionary Ecology of Eusociality in Australian Gall Thrips: a 'Model Clades' Approach

We integrate phylogenetic information with data on genetic relatedness, inbreeding, sex ratios, reproductive skew, host-plant use, gall morphology, soldier defensive behaviour, kleptoparasite pressure, and demography to evaluate hypotheses for the origin and evolution of soldier castes in Australian gall thrips. Necessary and sufficient conditions for the single origin of thrips soldiers appear to include high relatedness and inbreeding, strong kleptoparasite pressure, small brood size, and long duration of the gall. However, only brood size and gall duration apparently changed (becoming smaller) concomitant to the origin of soldiers. Reproductive skew between the foundress and soldiers was relatively low at the origin of soldiers, but increased substantially along the lineage leading to two species, K. habrus and K. intermedius. These two species also exhibit a relatively high propensity for defense by soldiers. Analysis of the associations between genetic and ecological traits that resulted from the social-adaptive radiation of gall thrips with soldiers provides two main insights. First, fewer matings by foundresses, and less mating after dispersal, result in stronger local mate competition, higher relatedness (and a higher inbreeding coefficient) among soldier females, and a stronger female bias in dispersers. Second, gall size apparently constrains the reproduction of soldiers, with less soldier reproduction favoring the evolution of more-effective, more-altruistic soldiers. Moreover, 2 when soldiers are more effective, fewer of them can be produced, leading to higher production of dispersers. Soldiers were apparently lost in two lineages, in both cases in conjunction with a shift to a phylogenetically-divergent species of Acacia host plant. Our analyses demonstrate that the evolution of soldiers in thrips is driven by a combination of selective pressures at three levels, from host-plant, to conspecific interactions, to kleptoparasites.