Cooperative interactions among females and even more extraordinary sex ratios

Abstract

Hamilton's local mate competition theory provided an explanation for extraordinary female biased sex ratios in a range of organisms. When mating takes place locally, in structured populations, a female biased sex ratio is favoured to reduce competition between related males, and to provide more mates for males. However, there are a number of wasp species where the sex ratios appear to more female biased than predicted by Hamilton's theory. We investigated theoretically the extent to which cooperative interactions between related females can interact with local mate competition to favour even more female biased sex ratios. We found that: (i) cooperative interactions between females can lead to sex ratios that are more female biased than predicted by local competition theory alone; (ii) sex ratios can be more female biased when the cooperative interactions are offspring helping parents, rather than cooperation between siblings. Our results can be applied to a range of organisms, and provide an explanation for the extreme sex ratio biases that have been observed in Sclerodemus and Melittobia wasps.

Solving the sex ratio scandal inMelittobiawasps

“…5). One possible explanation for that is a cooperative interaction between related females 6,[51][52][53] . In Melittobia, females favor ovipositing on hosts parasitized by other females rather than intact hosts (J.…”

“…Cooperative interactions have previously been suggested to favour an increased proportion of female offspring in a range of organisms, including other parasitoids, bees, beetles, and birds 37,51,[56][57][58][59][60] . A complication here is that although limited dispersal increases relatedness between encountering individuals, it can also increase competition between the related individuals, and so reduce selection for female-biased sex ratios 32,33,46,53,61 .…”

“…Cooperative interactions have previously been suggested to favour an increased proportion of female offspring in a range of organisms, including other parasitoids, bees, beetles, and birds 37,51,56–60 . A complication here is that although limited dispersal increases relatedness between encountering individuals, it can also increase competition between the related individuals, and so reduce selection for female-biased sex ratios 32,33,46,53,61 . However, in the case of Melittobia species, overlapping generations, inelasticity, dispersing with relatives, and open sites could negate this increased competition 33,62–65 (Supplementary Information 3)…”

How many cooperators are too many? Foundress number, reproduction and sex ratio in a quasi‐social parasitoid

“…Its evolution requires that the actor also accrues fitness benefits, whether via kin selection (explaining altruistic cooperation that incurs a personal fitness cost to the actor, Hamilton, 1964), by‐products benefit (a direct consequence of a self‐interested act, Davies et al, 2012), reciprocity (preferentially helping individuals that have helped previously, Trivers, 1971; Dugatkin, 1997) or enforcement (rewarding cooperators and punishing non‐cooperators, Franks, 2003; Davies et al, 2012). Cooperative reproduction in social insects is often associated with biased offspring sex ratios (Bono & Crespi, 2008; Crozier & Pamilo, 1996; Iritani et al, 2021; West, 2009), often due to the indirect fitness benefits of cooperation being greater when an actor helps to rear offspring of one sex rather than the other.…”

“…Cooperative multi‐foundress reproduction in Sclerodermus appears to have evolved due to large hosts being very challenging for individual females to attack, with mean per capita reproductive output being higher among multi‐foundress groups (Tang et al, 2014). It has also been predicted that the mutual benefits of foundresses co‐exploiting hosts select for female‐biased sex ratios via local resource enhancement (LRE: Tang et al, 2014; Kapranas et al, 2016; Iritani et al, 2021) instead of, or in combination with, local mate competition (LMC: Hamilton, 1967), which is the more commonly applied explanation for female‐biased parasitoid sex ratios (Godfray, 1994; West, 2009). Local mate competition and local resource enhancement are two aspects of the same theoretical framework for explaining sex ratio bias (Taylor, 1981; West, 2009); LMC emphasises how mothers bias their sex allocation away from members of the sex that competes among itself for a resource (e.g., males competing for mating opportunities), and LRE emphasises how mothers bias allocation towards members of the sex that enhance each other's ability to exploit a resource (e.g., suppression of a common host by females).…”