Male development tracks rapidly shifting sexual versus natural selection pressures

Theory predicts that interplay between sexual and natural selection shapes phenotypic distributions over evolutionary time [1–3]. We show that this also significantly affects individual development. Developmental plasticity, whereby individuals vary their ontogeny in response to variation in the selection to be encountered upon maturity [4–6], has previously been demonstrated in response to single selective pressures, such as predation and sperm competition [7,8]. We show that the relative magnitude of opposing natural and sexual selection can trigger developmental shifts and rapidly change the distribution of phenotypic traits critical to reproductive success. Males of the sexually cannibalistic redback spider (Latrodectus hasselti) show a tactical, condition-dependent shift between conflicting developmental strategies favoured by scramble competition or surviving mate search. Male condition, developmental rate and body size changed with the relative importance of these selective pressures, which naturally fluctuate throughout a breeding season [9–11]. This has important implications for studies comparing fitness values of fixed traits without regard for plasticity. We exposed penultimate-instar redback spider males to noncontact, pheromonal cues [12,13] simulating dense (females present) or sparse (females absent) populations. This treatment was combined with high, intermediate or low diet levels, respectively. When females are sparse, natural selection for provisioning to survive mate searching, during which 80% of males perish [14], will be more intense than sexual selection for scramble competition for virgin females (90% median paternity for the first male to mate) [15]. As multiple males commonly settle on females’ webs [16], male density will also affect competitive success. We, therefore, examined male growth, development time, and body condition as a function of diet, female treatment and male density. We also assessed male phenotypes as a function of female proximity in the field (Supplemental Data). Our laboratory and field results collectively show that redback males adjust their development in response to pheromonal cues of female and male density. When females are absent, males trade-off rapid development for increased body size and condition (Table 1; Figure 1) as larger males in better condition are more likely to survive mate searching and direct competition when females are sparse. In contrast, males trade-off size and body condition for rapid development when females are present (Table 1; Figure 1), which would ensure that they can reach virgin females first [15]. Similarly, in the field, as female proximity increases, male size (Two-way ANCOVA, F = 8.96, p = 0.004) and body condition (Two-way ANCOVA, F = 5.14, p = 0.028) decrease. Sexual selection for scramble competition has been proposed to contribute to sexual size dimorphism as a side-effect of rapid development of males [17]. These results show that the degree of dimorphism could change within seasons as selection fluctuates. Although increased female density resulted in smaller males of poorer condition that developed rapidly, increased male density led to the development of smaller males in better condition (Table 1). This independent effect of neighbouring males suggests a trade-off between size and body condition. Thus, the relative importance of these traits to male fitness apparently changes as a function of both female and male density. Although conflicting selection usually results in non-optimal phenotypes with moderate fitness [18,19], in redback spiders, conflicting pressures acting on phenotypic plasticity yield phenotypes optimized for specific competitive challenges [6]. This is critical because redback males are under strong selection to succeed in their single mating opportunity [16,20]. Similar plasticity may be important in cases where males have few mating opportunities that occur over small spatial or temporal scales, where juveniles can detect cues reliably predicting adult challenges and/or where allocation of limited resources -0.06 -0.04 -0.02 0.00 0.02 0.04 0.06