Co‐foundress confinement elicits kinship effects in a naturally sub‐social parasitoid

Abstract

Kinship among interacting individuals is often associated with sociality and also with sex ratio effects. Parasitoids in the bethylid genus Goniozus are sub‐social, with single foundress females exhibiting post‐ovipositional maternal care via short‐term aggressive host and brood defence against conspecific females. Due to local mate competition (LMC) and broods normally being produced by a single foundress, sex ratios are female‐biased. Contests between adult females are, however, not normally fatal, and aggression is reduced when competing females are kin, raising the possibility of multi‐foundress reproduction on some hosts. Here, we screen for further life‐history effects of kinship by varying the numbers and relatedness of foundresses confined together with a host resource and also by varying the size of host. We confined groups of 1–8 Goniozus nephantidis females together with a host for 5+ days. Multi‐foundress groups were either all siblings or all nonsiblings. Our chief expectations included that competition for resources would be more intense among larger foundress groups but diminished by both larger host size and closer foundress relatedness, affecting both foundress mortality and reproductive output. From classical LMC theory, we expected that offspring group sex ratios would be less female‐biased when there were more foundresses, and from extended LMC theory, we expected that sex ratios would be more female‐biased when foundresses were close kin. We found that confinement led to the death of some females (11% overall) but only when host resources were most limiting. Mortality of foundresses was less common when foundresses were siblings. Developmental mortality among offspring was considerably higher in multi‐foundress clutches but was unaffected by foundress relatedness. Groups of sibling foundresses collectively produced similar numbers of offspring to nonsibling groups. There was little advantage for individual females to reproduce in multi‐foundress groups: single foundresses suppressed even the largest hosts presented and had the highest per capita production of adult offspring. Despite single foundress reproduction being the norm, G. nephantidis females in multi‐foundress groups appear to attune sex allocation according to both foundress number and foundress relatedness: broods produced by sibling foundresses had sex ratios similar to broods produced by single foundresses (ca. 11% males), whereas the sex ratios of broods produced by nonsibling females were approximately 20% higher and broadly increased with foundress number. We conclude that relatedness and host size may combine to reduce selection against communal reproduction on hosts and that, unlike other studied parasitoids, G. nephantidis sex ratios conform to predictions of both classical and extended LMC theories.

Solving the sex ratio scandal inMelittobiawasps

“…6). The direct assessment of kin via genetic cues appears to be rare in parasitoids, with most studies finding that females do not use genetic cues to assess relatedness to other females 16,25,[35][36][37]47 . An exception is provided by the bethylid Goniozus nephantidis, where females appear to be able to assess relatedness directly, and adjust their offspring sex ratio accordingly 34,36 .…”

“…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 lives symbiotically with host species 54,55 . 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 .…”

“…If females laying eggs on a host are related, then this increases the extent to which relatives are competing for mates, and so can favour an even more female-biased sex ratio 28,[31][32][33][34] . Although most parasitoid species appear unable to directly assess relatedness, dispersal behaviour could provide an indirect cue of whether females are with close relatives [35][36][37] .…”

“…Females could be assessing relatedness by either directly recognizing kin, or indirectly, by using whether or not they have dispersed as a cue of whether they are likely to be with non-relatives (dispersering females) or relatives (non-dispersering females) [34][35][36][37] . We conducted a laboratory experiment to test whether females directly recognize the relatedness of other females laying eggs on the same host, and adjust their sex ratio accordingly.…”

Cooperative interactions among females and even more extraordinary sex ratios

“…One example is provided by Melittobia wasps, where females of several species produce approximately 2 % male offspring when ovipositing alone ( n = 1), and hardly change their offspring sex ratio when more females lay eggs on a patch (larger; Fig 1A; Abe et al 2003, 2014). Another example is provided by Sclerodermus wasps, in which multiple females can lay eggs on a host but the females still only produce 7% males (Fig 1B; Tang et al 2014; Lupi et al 2017; Abdi et al 2020a,b,c). These cases therefore suggest that identifying additional factors that favour female-biased sex ratio is required.…”