Sex differences in phenotypic plasticity of a mechanism that controls body size: implications for sexual size dimorphism

R. Craig Stillwell 0 Goggy Davidowitz 0 0 Department of Entomology, University of Arizona , Tucson, AZ 85721-0036 , USA The degree and/or direction of sexual size dimorphism (SSD) varies considerably among species and among populations within species. Although this variation is in part genetically based, much of it is probably due to the sexes exhibiting differences in body size plasticity. Here, we use the hawkmoth, Manduca sexta, to test the hypothesis that moths reared on different diet qualities and at different temperatures will exhibit sex-specific body size plasticity. In addition, we explore the proximate mechanisms that potentially create sex-specific plasticity by examining three physiological variables known to regulate body size in this insect: the growth rate, the critical weight (which measures the cessation of juvenile hormone secretion from the corpora allata) and the interval to cessation of growth (ICG; which measures the time interval between the critical weight and the secretion of the ecdysteroids that regulate pupation and metamorphosis). We found that peak larval mass of males and females did not exhibit sex-specific plasticity in response to diet or temperature. However, the sexes did exhibit sex-specific plasticity in the mechanism that controls size; males and females exhibited sex-specific plasticity in the growth rate and the critical weight in response to both diet and temperature, whereas the ICG only exhibited sex-specific plasticity in response to diet. Our results suggest it is important for the sexes to maintain the same degree of SSD across environments and that this is accomplished by the sexes exhibiting differential sensitivity of the physiological factors that determine body size to environmental variation. 1. INTRODUCTION Males and females of most animals differ in their size, a phenomenon known as sexual size dimorphism (SSD; Fairbairn 1997, 2007). The direction and magnitude of SSD varies considerably among the major taxa and among species due to variation in the sources of selection acting in concert to create SSD: variation among taxa/species in the magnitude of sexual selection favouring large size in males (owing to male male competition or female choice), variation in fecundity selection favouring large size in females (larger females produce more eggs) and variation in a variety of sources of selection favouring small size in both sexes (Stillwell et al. 2010). In addition, recent studies have shown that the magnitude of SSD, but often not the direction, changes considerably among populations within species (Blanckenhorn et al. 2006, 2007; Stillwell et al. 2007a). Although much of this intraspecific variation in SSD is partly genetically based and hence due to selection, some of this variation is also probably due to a sex difference in phenotypic plasticity in body size (Fairbairn 2005; Stillwell et al. 2010). However, how such sex differences in body size plasticity are generated is puzzling because males and females share the same genes that control growth and development (Badyaev 2002). Consequently, how the sexes grow to different sizes and how the sexes exhibit sex-specific plasticity in response to environmental variability is poorly understood, particularly in invertebrates such as insects (Stillwell et al. 2010). Although many environmental and ecological variables induce plasticity in body size and other traits of ectothermic animals (Stillwell et al. 2007a; Teder et al. 2008; Blanckenhorn 2009), two are particularly important in inducing plasticity in growth and life-history traits: diet quantity/quality and temperature (Davidowitz et al. 2004; Stillwell et al. 2007b). Insects typically mature at larger sizes when raised at lower temperatures and when raised on higher quality diets (Atkinson 1994; Berrigan & Charnov 1994; Davidowitz et al. 2004; Stillwell & Fox 2005; Stillwell et al. 2007b; Kingsolver & Huey 2008). Insects also generally exhibit sex-specific plasticity in body mass in response to diet quality/quantity (Stillwell et al. 2010). For example, Bonduriansky (2007) found that in the Australian fly, Telostylinus angusticollis, males were generally more sensitive to rearing diet (lowquality versus high-quality diet) than were females; on the low-quality diet, males and females were nearly identical in size, whereas males were considerably larger than females on the high-quality diet. However, studies that have investigated whether temperature creates sex-specific plasticity in size are inconsistent (Stillwell et al. 2010); for instance, Stillwell & Fox (2007) found that males of the seed-feeding beetle, Callosobruchus maculatus, were generally more sensitive to rearing temperature than were females, creating temperature-induced variation in SSD. However, other studies have found that temperature produced no sex-specific plasticity in body size (Stillwell et al. 2010; this study). Despite a recent increase in interest on studying sex differences in body size plasticity, the mechanisms that produce these sex differences in plasticity are still poorly understood. Understanding both the ultimate (evolutionary/ecological) and proximate (developmental/ physiological) mechanisms that generate these patterns are essential to understanding the evolution of intraspecific variation in SSD in animals. Although the proximate mechanisms responsible for sex-specific plasticity in body size remain largely unknown, there are only four ways the sexes could differ in their plasticity in size: males and females must exhibit differences in plasticity in (i) size at hatching, (ii) growth rate, (iii) the duration of the growth period and/or (iv) size-dependent survival (Blanckenhorn 1997; Badyaev 2002; Esperk et al. 2007; Stillwell & Fox 2007; Stillwell et al. 2010). Few studies have examined these variables in the context of sex-specific plasticity, but of those that have, the results are not consistent (Stillwell et al. 2010). Alternatively, such sex differences in body size plasticity could be generated through sex differences in physiological mechanisms. The regulation of body size and plasticity in body size are known to be under physiological control in insects (Stern & Emlen 1999; Davidowitz & Nijhout 2004; Davidowitz et al. 2004; Nijhout & Davidowitz 2009). However, the physiological mechanisms that potentially generate sex-specific plasticity in body size have not previously been explored. Here we use the hawkmoth, Manduca sexta (Lepidoptera: Sphingidae), a model system in insect physiology, to investigate sex differences in plasticity of the underlying physiological mechanisms that potentially create sexspecific norms of reaction in body size. In insects, growth is typically exponential, such that most growth occurs in the last larval instar (Nijhout et al. 2006). In M. sexta, 90 per cent of the accumulation of mass occurs in the final (fifth) instar (Davidowitz et al. 2004). During the last instar, a comple (...truncated)