Haplodiploidy and the Evolution of Eusociality: Split Sex Ratios

Abstract

It is generally accepted that from a theoretical perspective, haplodiploidy should facilitate the evolution of eusociality. However, the "haplodiploidy hypothesis" rests on theoretical arguments that were made before recent advances in our empirical understanding of sex allocation and the route by which eusociality evolved. Here we show that several possible promoters of the haplodiploidy effect would have been unimportant on the route to eusociality, because they involve traits that evolved only after eusociality had become established. We then focus on two biological mechanisms that could have played a role: split sex ratios as a result of either queen virginity or queen replacement. We find that these mechanisms can lead haplodiploidy to facilitating the evolution of helping but that their importance varies from appreciable to negligible, depending on the assumptions. Furthermore, under certain conditions, haplodiploidy can even inhibit the evolution of helping. In contrast, we find that the level of promiscuity has a strong and consistently negative influence on selection for helping. Consequently, from a relatedness perspective, monogamy is likely to have been a more important driver of eusociality than the haplodiploidy effect.

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

“…These ratios are the same as derived by Gardner et al (2012). For diplodiploids, the convergence stable sex ratios (z m and z p ) are 1/2, regardless of u (Fisher 1930).…”

“…However, the average sibling is valued more than the average offspring only when the individual reproductive value of males does not counter the benefits of high sister-sister relatedness, i.e., when the proportion of males in the population is more than 25 percent. Although several mechanisms for split sex ratios have been suggested in the literature, it seems that reproduction by unmated females is the only likely mechanism that could have been important at the origin of helping (reviewed in Gardner et al 2012). In haplodiploid species, unmated females have the option of laying unfertilized eggs, which develop to males.…”

“…This effect of unmatedness must be taken into account when comparing the conditions for the evolution of helping in haplodiploids and diplodiploids. A recent study by Gardner et al (2012) investigated how unmatedness influences the inclusive fitness valuations a female places on siblings and offspring, and how this affects the evolution of helping. Here we compare the effects of unmatedness on the evolution of helping by females and males in haplodiploids and diplodiploids, accounting for both the inclusive fitness valuations of relatives of different classes, and the number of offspring produced by mated and unmated females.…”

Sex ratio biases in termites provide evidence for kin selection

“…Class reproductive value describes the expected proportion of genes contributed by a class of individuals to a future generation 24,25 . When there are n types of mating that occur over the lifespan of the colony (for example, mating between parental founders, mother-son inbreeding, father-daughter inbreeding, so on.…”

Haplodiploidy and the Evolution of Eusociality: Worker Revolution

“…We consider the consequences of variation in biological details that could alter the association between helping and biased sex ratios, such as the underlying genetics, strength of selection, extent of worker reproduction, and rate of sex ratio evolution. We focus on the two Trivers and Hare (1976) scenarios because these have been so influential and because we have already examined the other factors that could lead to split sex ratios elsewhere, finding them unlikely to have played a major role in the evolution of eusociality (Gardner et al 2012a(Gardner et al , 2012bAlpedrinha et al 2013). In addition, they are different classes of scenarios, in that Trivers and Hare (1976) focused on how split sex ratios may arise transiently, as worker control spreads, whereas other scenarios involve split sex ratios being maintained at equilibrium, as evolutionarily stable strategies (reviewed by Gardner et al 2012a).…”