Evolutionary stable sex ratios with non‐facultative male‐eggs first sex allocation in fig wasps

Abstract

Sex allocation theory has long generated insights into the nature of natural selection. Classical models have elucidated causal phenomena such as local mate competition and inbreeding on the degree of female bias exhibited by various invertebrates. Typically, these models assume mothers facultatively adjust sex allocation using predictive cues of future offspring mating conditions. Here we relax this assumption by developing a sex allocation model for haplodiploid mothers experiencing local mate competition that lay a fixed number of male eggs first. Female egg number is determined by remaining oviposition sites or remaining eggs of the mother, depending on which is exhausted first. Our model includes parameters for variation in foundress number, patch size, fecundity and offspring mortality that allow us to generate secondary sex ratio predictions based on specific parameterizations for natural populations. Simulations show that: 1) in line with classical models, factors that increase sib‐mating result in mothers laying relatively more female eggs; 2) high offspring mortality leads to relatively more males as fertilization insurance; 3) unlike classical model predictions, sub‐optimal predictions, such as more males than females are possible. In addition, our model provides the first quantitative predictions for the expected number of males and females in a patch where typically only one mother utilizes a given patch. We parameterized the model with data obtained from seven species of southern African fig wasps to predict expected means and variances for numbers of male and female offspring for typical numbers of mothers utilizing a patch. These predictions were compared to secondary sex ratio data from single foundress patches, the most commonly encountered situation for these species. Our predictions matched both the observed number and variance of male and female offspring with a high degree of accuracy suggesting that facultative adjustment is not required to produce evolutionary stable sex ratios.

Consequences of population structure for sex allocation and sexual conflict

“…First, inbreeding is probably confounded with dispersal type (with high inbreeding expected for the budding dispersal regime) and may be a factor impacting our results. Inbreeding can in itself select for more female-biased offspring sex ratios (Frank 1985; Herre 1985; Chung et al 2019). If coupled with high levels of juvenile mortality this could, in some cases, result in no males on a patch (West et al 2002b; Chung et al 2019), potentially explaining why we lost all 3 replicates of the ‘Local Budding’ and 1 replicate of the ‘Global Budding’ regimes.…”

“…Inbreeding can in itself select for more female-biased offspring sex ratios (Frank 1985; Herre 1985; Chung et al 2019). If coupled with high levels of juvenile mortality this could, in some cases, result in no males on a patch (West et al 2002b; Chung et al 2019), potentially explaining why we lost all 3 replicates of the ‘Local Budding’ and 1 replicate of the ‘Global Budding’ regimes. At the same time, the accrued costs of inbreeding may negate any benefit of female-biased sex ratios in the ‘Global Budding’ regime in the replicates that survived (Greeff 1996).…”

“…This might be because, in haplodiploids like spider mites, inbreeding costs are expressed mainly in female traits (Tien et al 2015). As such, there might be selection to augment the production of sons in environments, or patches, with low fecundity and/or high offspring mortality brought about by inbreeding, to ensure female fertilisation (West et al 2002b; Chung et al 2019). Thus, it is hard to predict the exact impact of inbreeding in our selection regimes, as we do not have accurate measures of offspring mortality during experimental evolution.…”

Egg load is a cue for offspring sex ratio adjustment in a fig‐pollinating wasp with male‐eggs‐first sex allocation

“…In Kradibia tentacularis , experimental introductions of either one, two or three foundresses into single figs, and when some wasps naturally re‐emerged from figs, re‐introduction into a second fig, resulted in brood sex ratios that mainly reflected clutch size; importantly, in single foundress second figs, clutch size reductions could only reflect individual egg loads with smaller egg loads resulting in less female‐biased sex ratios (relatively more males) (Raja et al, ). It is noteworthy that K. tentacularis exhibits ‘males‐first’ sex allocation (see also Hardy, ), whereby most male eggs are laid early during oviposition and mainly females thereafter (Chung, Pienaar, & Greeff, ; Raja et al, ; Wang et al, ). Variation in sex ratios according to clutch size/egg load may therefore also be influenced by a ‘males‐first’ sex allocation strategy, especially if foundresses on entering a second fig ‘reset to zero’ their sex allocation strategy (Raja et al ) and/or lay a fixed number of male eggs in each clutch (Kjellberg et al, ; Wang et al, ).…”

“…It is noteworthy that K. tentacularis exhibits 'males-first' sex allocation (see also Hardy, 1992), whereby most male eggs are laid early during oviposition and mainly females thereafter (Chung, Pienaar, & Greeff, 2019;Raja et al, 2008;Wang et al, 2015). Variation in sex ratios according to clutch size/egg load may therefore also be influenced by a 'males-first' sex allocation strategy, especially if foundresses on entering a second fig 'reset to zero' their sex allocation strategy (Raja et al 2008) and/or lay a fixed number of male eggs in each clutch (Kjellberg et al, 2005;Wang et al, 2015).…”