Why do males emerge before females? Sexual size dimorphism drives sexual bimaturism in insects

Abstract

Conspecific females and males often follow different development trajectories which leads to sex differences in age at maturity (sexual bimaturism, SBM). Whether SBM is typically selected for per se (direct selection hypothesis) or merely represents a side-effect of other sex-related adaptations (indirect selection hypothesis) is, however, still an open question. Substantial interspecific variation in the direction and degree of SBM, both in invertebrates and vertebrates, calls for multi-species studies to understand the relative importance of its evolutionary drivers. Here we use two complementary approaches to evaluate the evolutionary basis of SBM in insects. For this purpose, we assembled an extensive literaturederived data set of sex-specific development times and body sizes for a taxonomically and ecologically wide range of species. We use these data in a meta-analytic framework to evaluate support for the direct and indirect selection hypotheses. Our results confirm that protandrymales emerging as adults before femalesis the prevailing form of SBM in insects. Nevertheless, protandry is not as ubiquitous as often presumed: females emerged before males (= protogyny) in about 36% of the 192 species for which we had data. Moreover, in a considerable proportion of species, the sex difference in the timing of adult emergence was negligible. In search for the evolutionary basis of SBM, we found stronger support for the hypothesis that explains SBM by indirect selection. First, across species, the direction and degree of SBM appeared to be positively associated with the direction and degree of sexual size dimorphism (SSD). This is consistent with the view that SBM is a correlative by-product of evolution towards sexually dimorphic body sizes. Second, within protandrous species, the degree of protandry typically increased with plastic increase in development time, with females prolonging their development more than males in unfavourable conditions. This pattern is in conflict with the direct selection hypothesis, which predicts the degree of protandry to be insensitive to the quality of the juvenile environment. These converging lines of evidence support the idea that, in insects, SBM is generally a by-product of SSD rather than a result of selection on the two sexes to mature at different times. It appears plausible that selective pressures on maturation time per se generally cannot compete with viability-and fecundity-mediated selection on insect body sizes. Nevertheless, exceptions certainly exist: there are undeniable cases of SBM where this trait has evolved in response to direct selection. In such cases, either the advantage of sex difference in maturation time must have been particularly large, or fitness effects of body size have been unusually weak.

Temperature-modified density effects in the black soldier fly: low larval density leads to large size, short development time and high fat content

“…Regarding sex, female BSFs, in general, were significantly heavier than their male counterparts in almost all life-history traits except adult mass, but males matured and emerged before females. Males emerging before their female counterparts (protandry) has been confirmed as the dominant form of sexual bimaturism in insects (Teder et al, 2021). The study by Jones and Tomberlin (2019) on BSF larvae found similar results in all studied life-history traits, excluding adult mass, where the effect of sex was also found to be significant.…”

Limited sex differences in plastic responses suggest evolutionary conservatism of thermal reaction norms: A meta-analysis in insects

“…In particular, longer development confers a higher risk of succumbing to natural enemy attack and dying without leaving any progeny (Stearns 1992;Blanckenhorn 2000). Development time effects on fitness may also result from the trade-off between development time and body size: larger individuals are generally more fecund within species (Honek 1993), whereas-everything else being equal-attaining a larger size requires a longer (and riskier) juvenile development (Blanckenhorn 2000;Tammaru et al 2010;Teder et al 2021). Therefore, knowledge of sex-specific responses in development time can also shed further light on environmentally induced variation in sexual size dimorphism (Teder and Tammaru 2005;Hirst et al 2015).…”

“…To obtain a metric for comparing the thermal sensitivity of male and female development times, we calculated the reduced major axis (RMA) regression slope of male development times on female development times for each primary dataset. The RMA regression slope is a widely used quantitative measure to compare sex-specific plastic responses of various traits across environments (e.g., Fairbairn 1997;Hirst et al 2015;Teder et al 2021). The paired measurements of male and female average development times from each temperature treatment entered these regression models as individual data points.…”

Morphology and ultrastructure of antennal sensilla of the parasitic wasp Baryscapus dioryctriae (Hymenoptera: Eulophidae)

“…Therefore, the identification and functional study of antennal sensilla are essential to better understand the sensing system in the parasitic wasps and further study the interaction among host plant, pest, and their parasitoids. In general, sexual morphology dimorphism is considered to be a common phenomenon in insect, such as sexual size dimorphism (Teder et al, 2021), sexual wing dimorphism (Matsushima & Yokoi, 2022), and sexual antennae dimorphism (Mariette et al, 2021).…”