Extended haplodiploidy hypothesis

Abstract

Evolution of altruistic behavior was a hurdle for the logic of Darwinian evolution. Soon after Hamilton formalized the concept of inclusive fitness, which explains how altruism can evolve, he suggested that the high sororal relatedness brought by haplodiploidy could be why Hymenopterans have a high prevalence in eusocial species, and why helpers in Hymenoptera are always female. Later it was noted that in order to capitalize on the high sororal relatedness, helpers would need to direct help toward sisters, and this would bias the population sex ratio. Under a 1:3 males:females sex ratio, the inclusive fitness valuation a female places on her sister, brother, and an own offspring are equal—apparently removing the benefit of helping over independent reproduction. Based on this argumentation, haplodiploidy hypothesis has been considered a red herring. However, here we show that when population sex ratio, cost of altruism, and population growth rate are considered together, haplodiploidy does promote female helping even with female‐biased sex ratio, due the lowered cost of altruism in such populations. Our analysis highlights the need to re‐evaluate the role of haplodiploidy in the evolution of helping, and the importance of fully exploring the model assumptions when comparing interactions of population sex ratios and social behaviors.

The evolution of eusociality: no risk‐return tradeoff but the ecology matters

“…; Quinones & Pen ; Rautiala et al . ). It remains equivocal, however, whether relatedness really was unusually high in the ancestors of today's eusocial taxa (Nonacs ; Pernu & Helantera ), and the ecological parameters in Hamilton's Rule are potentially just as important determinants of whether helping or solitary nesting is the optimal strategy (Queller , ; Field et al .…”

“…Starting with Hamilton's (1964) famous threequarters relatedness hypothesis, theoretical attempts to understand why eusociality evolved in Hymenoptera have tended to focus on factors that can raise genetic relatedness such as haplodiploidy and more recently, lifetime queen monogamy (e.g. Trivers & Hare 1976;Seger 1983;Boomsma 2009;Fromhage & Kokko 2011;Nonacs 2011Nonacs , 2014Gardner et al 2012;Quinones & Pen 2017;Rautiala et al 2019). It remains equivocal, however, whether relatedness really was unusually high in the ancestors of today's eusocial taxa (Nonacs 2011;Pernu & Helantera 2019), and the ecological parameters in Hamilton's Rule are potentially just as important determinants of whether helping or solitary nesting is the optimal strategy (Queller 1994(Queller , 1996Field et al 2000;Korb & Heinze 2008;Avila & Fromhage 2015).…”

Sex ratio and sexual conflict in a collective action problem

“…In general, genetic relatedness promotes cooperation and increases contributions to collective action. For examples, both theoretical and empirical research on the evolution of cooperative breeding in haplodiploids suggest that cooperation is more likely to evolve under monogamy than when broods are the result of polyandrous matings (23–26); in theoretical work that specifically asks whether males or females should evolve into helpers, monogamous situations under haplodiploidy can favour females as helpers (9, 27). Our results add a collective action angle to these results: ours is not a model of cooperative breeding, as in our setting no individual foregoes own reproduction to help others, instead the collective good is group survival up to maturity.…”

Haplodiploidy

“…However, a very recent theoretical analysis has concluded that this logic is incomplete [11]. In this reanalysis, split sex ratios are unnecessary for the haplodiploidy hypothesis to work, as long as altruists preferentially rear sisters over brothers (i.e., through manipulating their nest's sex ratio), and altruism is still favored at a 3:1 population sex ratio.…”