Cooperative interactions among females can lead to 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 favored to reduce competition between related males, and to provide more mates for males. However, there are a number of wasp species in which the sex ratios appear to more female biased than predicted by Hamilton's theory. It has been hypothesized that the additional female bias in these wasp species results from cooperative interactions between females. We investigated theoretically the extent to which cooperation between related females can interact with local mate competition to favor even more female‐biased sex ratios. We found that (i) cooperation between females can lead to sex ratios that are more female biased than predicted by local competition theory alone, and (ii) sex ratios can be more female biased when the cooperation occurs from offspring to mothers before dispersal, rather than cooperation between siblings after dispersal. Our models formally confirm the verbal predictions made in previous experimental studies, which could be applied to a range of organisms. Specifically, cooperation can help explain sex ratio biases in Sclerodermus and Melittobia wasps, although quantitative comparisons between predictions and data suggest that some additional factors may be operating.

A solution to a sex ratio puzzle in Melittobia wasps

“…Cooperative female interactions have previously been suggested to favor an increased proportion of female offspring in a range of organisms, including other parasitoids, bees, beetles, and birds (38,54,(59)(60)(61)(62)(63). 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 (33,34,47,56,64). However, in the case of Melittobia species, overlapping generations, inelasticity, dispersing with relatives, and open sites could negate this increased competition (34,(65)(66)(67)(68) (SI Appendix, Supporting Information 3).…”

“…Variable clutch size increases average relatedness among interacting offspring and hence favors a more female-biased sex ratio (40)(41)(42). Another possible explanation is cooperative interactions between related females (6,(54)(55)(56). In Melittobia, females favor ovipositing on hosts parasitized by other females rather than intact hosts (56).…”

“…Another possible explanation is cooperative interactions between related females (6,(54)(55)(56). In Melittobia, females favor ovipositing on hosts parasitized by other females rather than intact hosts (56). In addition, a larger number of Melittobia females are likely to be advantageous to cooperatively make tunnels in host nests and to fight against mite species that live symbiotically with host species (57,58).…”

Individual- and group-level sex ratios under local mate competition: consequences of infanticide and reproductive dominance

“…A remaining puzzle is the extent of the sex ratio bias produced by species in the cooperatively brooding (“quasi-social”) parasitoid genus Sclerodermus (Hymenoptera [sub-clade Aculeata]: Bethylidae): sex ratios at offspring maturity are typically around 0.1 (10% offspring are males) and appear little influenced by the number of co-reproducing foundresses (e.g., Abdi et al, 2020b , 2021 ; Guo et al, 2022 ; Kapranas et al, 2016 ; Malabusini et al, 2022 ; Tang et al, 2014 ; Wang et al, 2016 ; Wei et al, 2017 ; Yang et al, 2018 ) or by the relatedness between foundresses ( Abdi et al, 2020a , b ; Guo et al, 2022 ). A proposed explanation ( Tang et al, 2014 ) is that mutually beneficial actions of co-foundress females during host attack and subsequent brood tending could select for the female bias via local resource enhancement (LRE: Taylor, 1981 ) but the size of the effect predicted by a recent formal model ( Iritani et al, 2021 ) is insufficient to explain the observed bias.…”

Comparing the effects of social environments and life history traits on sex allocation in a haplodiploid spider mite

“…Population size and density are two key socio-environmental factors that affect the offspring sex ratio in group-living animals. For example, in small populations founded by one or a few foundresses, females tend to produce femalebiased offspring to reduce the local mate competition between related males (Hamilton 1967;Krainacker & Carey 1991;Roeder 1992;Sato & Saito 2006;West 2009;Macke et al 2012Macke et al , 2014, whereas in dense populations mothers incline to produce more offspring of dispersive sex to reduce resource competition (Clark 1978;Mari et al 2008;Hjernquist et al 2009;Iritani et al 2021;Weerawansha et al 2022a, b). Social environments may affect offspring sex ratio directly by altering mothers' sex allocation strategies (Clark 1978;Iritani et al 2021;Weerawansha et al 2022a, b) or indirectly through mediating their other life history traits such as clutch size (West 2009) and egg size (West 2009;Macke et al 2011Macke et al , 2012.…”