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 literature-derived 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 protandry – males emerging as adults before females – is 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.

中文翻译：

---

为什么男性先于女性出​​现？性大小二态性驱动昆虫的性双成熟

同种雌性和雄性通常遵循不同的发育轨迹，这导致成熟年龄的性别差异（性双成熟，SBM）。是否通常选择 SBM本身（直接选择假设）或仅代表其他与性别相关的适应的副作用（间接选择假设）仍然是一个悬而未决的问题。在无脊椎动物和脊椎动物中，SBM 的方向和程度存在大量种间差异，需要进行多物种研究以了解其进化驱动因素的相对重要性。在这里，我们使用两种互补的方法来评估昆虫 SBM 的进化基础。为此，我们为分类学和生态学范围广泛的物种收集了广泛的文献衍生数据集，其中包括性别特异性发育时间和体型。我们在元分析框架中使用这些数据来评估对直接和间接选择假设的支持。我们的研究结果证实，protandry（雄性先于雌性成年）是昆虫中 SBM 的主要形式。然而，protandry 并不像通常假设的那样普遍存在：在我们拥有数据的 192 个物种中，大约 36% 的物种在雄性之前出现了雌性（= protogyny）。此外，在相当大比例的物种中，成虫出现时间的性别差异可以忽略不计。在寻找 SBM 的进化基础时，我们发现对通过间接选择解释 SBM 的假设更有力的支持。首先，跨物种，SBM的方向和程度似乎与有性大小二态性（SSD）的方向和程度呈正相关。这与 SBM 是向两性体型进化的相关副产品的观点一致。其次，在原始物种中，protandry 的程度通常随着发育时间的延长而增加，在不利条件下，雌性比雄性延长其发育的时间更长。这种模式与直接选择假说相冲突，直接选择假说预测前生的程度对幼年环境的质量不敏感。这些趋同的证据支持这样一种观点，即在昆虫中，SBM 通常是 SSD 的副产品，而不是两种性别选择在不同时间成熟的结果。对成熟时间的选择压力似乎是合理的 它预测 protandry 的程度对少年环境的质量不敏感。这些趋同的证据支持这样一种观点，即在昆虫中，SBM 通常是 SSD 的副产品，而不是两种性别选择在不同时间成熟的结果。对成熟时间的选择压力似乎是合理的 它预测 protandry 的程度对少年环境的质量不敏感。这些趋同的证据支持这样一种观点，即在昆虫中，SBM 通常是 SSD 的副产品，而不是两种性别选择在不同时间成熟的结果。对成熟时间的选择压力似乎是合理的本身通常无法与生存力和繁殖力介导的昆虫体型选择竞争。然而，例外情况肯定存在：不可否认的 SBM 案例中，这种性状是为了响应直接选择而进化的。在这种情况下，要么成熟时间的性别差异优势特别大，要么体型对健康的影响异常微弱。