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

Abstract

A ustralian gall-inducing thrips gain food and shelter, in the form of a gall, from species of Acacia trees (1-6). The gall is formed as a female feeds on a developing phyllode (a petiole modified to serve as a stem and leaf) that encapsulates her and in some cases a male (4, 6). The foundress oviposits within the gall, and the developing thrips feed by sucking out the contents of plant cells on the gall's inner wall (1). 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. Two lifehistory observations indicate that relatedness of individuals within a gall may be high: (i) multiple founding by females, which would reduce relatedness among brood, is not observed for any of the gall-inducing species on Acacia (3, 4), and (ii) sex ratios of dispersing brood are markedly female-biased (3, 9), which suggests the presence of strong local mate competition and inbreeding.We developed microsatellite markers (10) for species of gall-inducing thrips with soldiers and used them to estimate genetic relatedness [refs. 11 and 12; RELATE 4.2c (http:// gsoft.smu.edu/GSoft.html) by K. R. Goodnight and D. C. Queller] and inbreeding in five of the species with soldiers ( Fig. 1; Table 1). In the four species for which multiple populations were sampled, the intraspecific similarity of relatedness and inbreeding estimates for populations that were up to 500 km apart indicates that these genetic parameters can be treated as speciesspecific values. These estimates of relatedness and inbreeding are among the highest ever recorded for social animals, and their magnitude is consistent with a high incidence of single-mating by foundresses, and brother-sister mating by both soldiers and dispersers (10). In addition, the strong relatedness asymmetries expected in outbred haplodiploid species (13) (e.g., a brood produced by a singly mated foundress is expected to exhibit relatedness among sisters of 0.75 whereas relatedness of sisters to brothers is expected to be 0.5) are not at a detectable level in the four species in which they can be estimated, as expected given their high levels of inbreeding (14). For example, from Table 1, K. hamiltoni population 3 exhibits among-sister relatedness of 0.85 and sister to brother relatedness of 0.82 (t ϭ 1.95, P Ͼ 0.05, n ϭ 12).Mapping of the relatedness and inbreeding estimates onto a phylogeny of Australian gall-inducing thrips on Acacia (15) i...

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

“…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). For diplodiploid species, our model predicts equal benefit thresholds for males and females.…”

Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis

“…Against this hypothesis, Hughes et al (2008) showed that monogamy-which maximizes relatedness of offspring-was ancestral in all eight Hymenopteran lineages that evolved eusociality. An important role for kin structure is also supported by the association of sociality with inbreeding in certain thrips (Chapman et al 2000) and spiders (Agnarsson et al 2006). Sponge-dwelling shrimp provide an independent test of the role of kin structure in the origin of eusociality.…”

“…Second, does group living indeed confer ecological advantages in enhancing ability to acquire and defend limited territories or other resources? Despite a long history of research, surprisingly few formal comparative studies have tested the importance of either genetic relatedness (but see Chapman et al 2000;Agnarsson et al 2006;Hughes et al 2008) or the hypothesized ecological benefits of social life in groups near the origin of eusociality. This is due in part to the generally ancient origins and phylogenetic conservatism of eusocial life in the major lineages of social insects, which obscure the conditions associated with the origins of eusociality (Crespi 1996).…”

Phylogenetics of Australian Acacia thrips: the evolution of behaviour and ecology

“…Crespi (1992b) suggested that the evolution of eusociality in thrips may have been associated with haplodiploidy, but phylogenetic studies show that high levels of inbreeding were present at the origin of eusociality in thrips, and the effect of inbreeding is likely to overwhelm the effect of haplodiploidy in lowering thresholds for altruistic behaviour (Chapman and Crespi, 1998;Chapman et al, 2000). Apart from eusociality, thrips have importance for evolutionary studies because of a number of other traits that are relevant to understanding the evolution of life history strategies (Kranz, 2000).…”