In insects and many other animals, diet quality is a key environmental determinant of individual body size, which often reflects condition (Blanckenhorn, 2000). Environmental variation in diet may select for environment-dependent maternal or paternal effects (as opposed to potentially environment-independent parent-of-origin effects, such as genomic imprinting, e.g. see Fitch et al., 1998; Lloyd, 2000), for two nonexclusive reasons. First, individuals that acquire high condition from a resource-rich environment may benefit by transferring their condition to their offspring, thus enhancing offspring fitness (Mousseau & Fox, 1998; Pál & Miklós, 1999; Qvarnström & Price, 2001). This predicts that offspring of high-condition parents will do better in any environment, but especially in a poor-quality environment where enhanced condition is most beneficial. Second, if the environment (e.g. diet) that the parents experience predicts the environment that their offspring will encounter, parents may be selected to optimize offspring phenotype for that environment (Mousseau & Dingle, 1991; Rossiter, 1996; Mousseau & Fox, 1998; Fox & Czesak, 2000; Gilchrist & Huey, 2001; Rotem et al., 2003; Holbrook & Schal, 2004). This predicts that offspring will do best in an environment similar to that experienced by their parents.
Environment-dependent maternal effects, reflecting variation in maternal provisioning, have been reported in many insects and other animals (Rossiter, 1996; Mousseau & Fox, 1998). Similarly, environment-dependent paternal effects have been reported in species where males provision their offspring through gifts of nutrients or other important substances transferred to females (Zeh & Smith, 1985; Dussourd et al., 1988; Gwynne, 1988; Smedley & Eisner, 1996; Vahed, 1998), or through direct contributions to offspring feeding (Griffith et al., 1999; Hunt & Simmons, 2000; Rauter & Moore, 2002). However, paternal effects are generally assumed to be absent, or much less important than maternal effects, in animals that lack paternal provisioning (Falconer & Mackay, 1996).
Nonetheless, several recent studies suggest that environment-dependent paternal effects can occur in the absence of paternal provisioning in the conventional sense. In Drosophila, the ambient temperature experienced by males affects life-history traits in their offspring (Huey et al., 1995; Watson & Hoffmann, 1995; Magiafoglou & Hoffmann, 2003) and, in locusts, paternal social environment influences offspring colour and behaviour (Islam et al., 1994). Such paternal effects could be mediated by small doses of accessory gland products (García-González & Simmons, 2007; Ivy, 2007). Moreover, there is mounting evidence that environment can induce epigenetic modifications (e.g. changes in methylation patterns or chromatin structure) in the germ line, resulting in epigenetic ‘reprogramming’ of sperm (Jablonka & Lamb, 1995, 2005; Fitch et al., 1998; Pembrey, 2002; Chang et al., 2006; Pembrey et al., 2006). In mice, paternal and maternal diets can affect offspring phenotype (Anderson et al., 2006; Cooney, 2006; Cropley et al., 2006). In rats, an environmentally induced low-fertility male phenotype was transmitted through the male line for four generations (Anway et al., 2005; Anway & Skinner, 2006). However, very few studies have tested for environment-dependent paternal effects in species lacking conventional forms of paternal provisioning, and the ecological and evolutionary importance of such effects remains uncertain in such species.
The possibility of such paternal effects has interesting implications for theory. In species lacking paternal provisioning, environmental variation is assumed to diminish heritability (i.e. offspring–paternal resemblance) for male quality, and thus reduce the indirect benefits of choice for females (Hunt et al., 2004). Nonetheless, environmental variation could play an important role in evolution if it could be transmitted to offspring through paternal effects. If environmental variation augments offspring–paternal resemblance through the transfer of paternal condition to offspring, it may contribute to indirect selection on female preferences (see Discussion).
In the fly Telostylinus angusticollis (Neriidae), larval diet quality affects a suite of condition-dependent traits, including larval survival, development rate, and adult body size and shape, and these effects are particularly strong in males (Bonduriansky, 2007). Similar phenotypic variation is observed in the wild (Fig. 1), and probably reflects natural variation in larval diet quality. Thus, environmental variation in body size (and, presumably, condition) appears to be an ecologically important parameter in natural populations. Females may be capable of transmitting environmental variation to offspring through maternal effects (e.g. via variation in egg provisioning). However, it is not clear whether environment-dependent paternal effects are possible in this species, because there is no evidence of any conventional form of paternal provisioning: mean copulation duration is only 43 s; there is no external or internal spermatophore, no visible insemination reaction and mean ejaculate size is < 0.01% of male body volume (R. Bonduriansky, unpublished data). By contrast, nuptial gifts of nutrients or other diet-derived substances are typically manifested in large ejaculates that constitute at least 1% (and often > 5%) of male body mass (Dussourd et al., 1988; Wedell, 1993; Smedley & Eisner, 1996; Vahed, 1998; Bonduriansky, 2001), and produce an insemination reaction (Markow & Ankney, 1988; Pitnick et al., 1997). The tiny ejaculate and lack of insemination reaction in T. angusticollis thus suggest that ejaculates are unlikely to function as nuptial gifts in this species.
We investigated the effects of environmental variation in maternal and paternal condition on four offspring traits in T. angusticollis: egg size, larval survival rate, development time and adult body size. To do this, we manipulated larval diet quality over two generations, and tested for effects of maternal, paternal and offspring diets and their interactions on offspring. We found that both mothers and fathers transfer their condition to offspring, but that maternal and paternal effects influence different aspects of offspring phenotype. Moreover, we observed a paternal diet effect on offspring body size and, through follow-up assays, found that this effect is probably sufficient to enhance offspring fitness. The paternal diet effect may be mediated by a cryptic form of paternal investment.