The evolution of soldier reproduction in social thrips

Abstract

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.

Lifetime monogamy and the evolution of eusociality

“…However, it is important to realize that many of them are lineages of recent origin with slight radiations at best and with close relatives that have lost or never gained eusocial traits (e.g. Stern & Foster 1997;Duffy 2003;Chapman et al 2002), so that they will not fit the strict obligate eusociality definition of Crespi & Yanega (1995) that I adhered to in Boomsma (2007) and the present review. I expect that even the naked mole-rat, with its social system based on sterile foragers and nurses rather than soldiers, will turn out not to be obligatorily eusocial, because its helpers are not sufficiently differentiated in lifespan (in captivity, Sherman & Jarvis 2002) and at least some of them can shift to a breeder phenotype when the dominant of the same gender disappears.…”

Beyond promiscuity: mate-choice commitments in social breeding

“…The fixed diameter of entrance tunnels would never select for soldier morphs because normal sized individuals can block tunnels. In the haplodiploid gall-forming thrips soldiers appear to be irreversible phenotypes, but remain able to reproduce [148,149]. In the gall-forming aphids, clonality makes direct/indirect fitness distinctions irrelevant, similar to germ-line and somatic cells in metazoan bodies having identical interests, and many alternative phenotypes already exist in the non-social aphid lineages that have produced social species [150].…”

Australian Thysanoptera – biological diversity and a diversity of studies

“…In contrast, other species induce small galls within which the foundress lays only a few eggs, and these give rise to wingless adults of both sexes with enlarged forelegs and prothorax. These wingless adults function as soldiers, fighting to protect their gall from invading caterpillars and kleptoparasitic thrips (Crespi & Abbot 1999;Perry et al 2002), and in some species the females have reduced reproductive capacity Chapman et al 2002).…”