Sex investment ratios in eusocial Hymenoptera support inclusive fitness theory

Abstract

Inclusive fitness theory predicts that sex investment ratios in eusocial Hymenoptera are a function of the relatedness asymmetry (relative relatedness to females and males) of the individuals controlling sex allocation. In monogynous ants (with one queen per colony), assuming worker control, the theory therefore predicts female-biased sex investment ratios, as found in natural populations. Recently, E.O. Wilson and M.A. Nowak criticized this explanation and presented an alternative hypothesis. The WilsonNowak sex ratio hypothesis proposes that, in monogynous ants, there is selection for a 1 : 1 numerical sex ratio to avoid males remaining unmated, which, given queens exceed males in size, results in a female-biased sex investment ratio. The hypothesis also asserts that, contrary to inclusive fitness theory, queens not workers control sex allocation and queen-worker conflict over sex allocation is absent. Here, I argue that the Wilson-Nowak sex ratio hypothesis is flawed because it contradicts Fisher's sex ratio theory, which shows that selection on sex ratio does not maximize the number of mated offspring and that the sex ratio proposed by the hypothesis is not an equilibrium for the queen. In addition, the hypothesis is not supported by empirical evidence, as it fails to explain 'split' (bimodal) sex ratios or data showing queen and worker control and ongoing queen-worker conflict. By contrast, these phenomena match predictions of inclusive fitness theory. Hence, the Wilson-Nowak sex ratio hypothesis fails both as an alternative hypothesis for sex investment ratios in eusocial Hymenoptera and as a critique of inclusive fitness theory.

Sex allocation conflict between queens and workers inFormica pratensiswood ants predicts seasonal sex ratio variation

“…They have shown that we cannot fully understand precision of adaptation without knowledge of natural history and the mechanisms underlying facultative responses to environment. Our demonstration of seasonal sex ratio variation consistent with the predictions of differential power between conflict parties adds a novel angle to this literature, and adds to the evidence (Bourke ) against recent criticisms questioning the explanatory power of inclusive fitness theory in sex allocation research (Wilson and Nowak ).…”

“…Since Trivers and Hare () combined the theories of the evolution of sex ratios, sociality, and parent–offspring conflicts, sex allocation in social insects has been a celebrated test case of kin selection (Bourke and Franks ; Crozier and Pamilo , Bourke ). Sex allocation in general is one of the best‐studied cases of adaptation, both in terms of theoretically predicted optima and how precisely organisms are able to meet the predicted optima (West ).…”

Regression, least squares, and the general version of inclusive fitness

“…It equally strongly draws attention on selection against altruistic behaviors when . Errors that stem from ignoring such classic messages still recur, for example in the sex ratio theories criticized by Bourke ().…”

Ant collective behavior is heritable and shaped by selection

“…sex ratio). Social insect sex ratio and caste ratio have long served as important models for empirically testing predictions from inclusive fitness theory regarding predicted conflicts between queens and workers over sex ratio and caste ratio (Trivers & Hare 1976;Reuter & Keller 2001;Mehdiabadi et al 2003;Bourke 2015). However, despite this long-term intense interest in the evolution of colony-level traits, we still know empirically very little about the key parameters governing the evolution of these traits.…”