Social biology and sex ratios of the eusocial gall‐inducing thrips Kladothrips hamiltoni

Abstract

Summary1. Thrips comprise the only order besides Hymenoptera where females are diploid and males are haploid. This makes them useful insects for studying the roles of kin selection and ecology in social evolution.2. Kladothrips hamiltoni is one of six species of Australian gall‐inducing thrips that have been identified as eusocial. Galls are initiated by a single foundress, who rears her brood and remains within the enclosed gall for life. The adults of both sexes of her first brood cohort are morphologically distinct from the second generation, comprising a nondispersing soldier caste. The foundress and sib‐mated soldiers jointly produce a second, dispersing generation, approximately 60–80% of which are produced by the soldiers. Mean per capita egg production of female soldiers is less than 33% that of the foundress.3. Adult eclosion of soldiers is protandrous but the overall sex ratio of the soldiers lacks bias (52% male). Protandry of soldiers increases the probability that female soldiers will be inseminated soon after their eclosion and therefore lay fertilised, female eggs. The lack of bias could be due to a balance between local resource competition and local mate competition. Gender‐specific defensive behaviour of soldiers with their enemies may also be important in explaining this unexpected sex ratio.4. The dispersing generation has an overall extreme female bias (5.6% male). Soldier incest increases relatedness between females more than between males, such that the foundress is more related to her granddaughters than her daughters, and female soldiers are more related to their daughters than their sons (assuming within‐gall relatedness < 1). A female bias in the offspring of soldiers should be preferred by both the foundress and soldiers as they are more related to soldier‐produced dispersing females than any other thrips in the gall. Female bias in the dispersing generation will also reduce local mate competition between males. Both soldier incest and local mate competition may therefore contribute to the extreme female bias in the dispersing generation.5. Selection pressures for sociality in gall‐inducing thrips appear to be more similar to those in gall‐inducing aphids and naked mole rats than to those in Hymenoptera.

Unmatedness Promotes the Evolution of Helping More in Diplodiploids than in Haplodiploids

“…Our analysis however suggests that haplodiploidy, together with unmatedness, could have contributed to the evolution of exclusive female help in outbreeding species like eusocial Hymenoptera by lowering the benefit threshold female helping. In contrast to Hymenoptera, in eusocial haplodiploid thrips both male and female offspring participate in nest defense (Crespi 1992;Kranz et al 1999). The evolution of both male and female helpers in eusocial thrips may be linked to lack of pre-adapations in either sex to soldiering, as suggested by Ross et al (2013), but also to the high degree of ancestral inbreeding in these species (McLeish et al 2006), which reduces the importance of relatedness asymmetries (Chapman et al 2000).…”

“…However, more recent analyses have shown that male workers should evolve as readily as female workers (Craig 1982;Pamilo 1991). Furthermore, eusocial haplodiploid thrips with both male and female helpers have been found (Crespi 1992;Kranz et al 1999). These findings and new analyses suggest that ecological circumstances and pre-adaptations like maternal care are more important in determining the sex of helpers than the genetics of sex determination (Queller and Strassmann 1998;Ross et al 2013).…”

High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips

“…In eusocial species, the first cohort to eclose are gall-bound soldiers, which are distinguished by robust forelimbs, reduced or absent wings, and self-sacrificing behavior exhibited in defense of the gall to the benefit of dispersing sisters and brothers (2,4,7). However, in at least one species, Kladothrips hamiltoni, it is suspected that soldiers could also be defending a few of their own offspring, as well as nieces and nephews, because soldiers are suspected of at least some egg laying within their natal gall (8). The foundress usually lives long enough to overlap with the adult soldiers, and she usually dies some time before the next group of individuals, the dispersive macropterae, reach the adult stage.…”

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

“…Correlation coefficients with an asterisk (*) are significant at less than the 0.05 level Sex ratios vary among species, and they also exhibit a temporal variation, as one sex can be produced before the other. Among the social species studied in detail thus far, there are notable associations between the order of eclosion by sex in soldiers and three variables: soldier sex ratios, offspring sex ratios, and the extent of reproductive skew between female soldiers and foundresses (Kranz et al 1999(Kranz et al , 2001a(Kranz et al , 2001bChapman et al 2002). Thus, K. habrus and K. waterhousei exhibit protogynous (females first) soldier production, strongly female-biased soldier sex ratios, an unbiased sex ratio of reproductive dispersers, and relatively high skew.…”