AN EVOLUTIONARY ARGUMENT FOR EGG LIMITATION

Insect parasitoids and insect herbivores with parasitoidlike biologies (e.g., some fruit flies and seed beetles) deposit eggs in or upon hosts that represent a discrete resource for the development of offspring. As a result, there is an unusually direct link between oviposition behavior and fitness gains for these insects, making them particularly suitable for the development and testing of theory for reproductive behavior, including clutch size (Godfray 1994), sex allocation (Charnov 1982; Wrensch and Ebbert 1993), and evolutionary conflicts between siblings or between parents and offspring (Godfray 1987a; Godfray and Parker 1992; Grbic et al. 1992; Rosenheim 1993; Ode and Strand 1995). A central question that has arisen during the course of this work is: what is the nature of the trade-off between current and future reproduction? The existence of such a trade-off has been suggested by the observation of clutch sizes smaller than the "Lack clutch size," which is the optimal clutch size when there is no cost of reproduction (Godfray 1987b; Vet et al. 1994). Early theoretical work postulated that the realized lifetime reproductive success of parasitoids was limited by the time available to locate hosts and oviposit. Thus, the tradeoff was mediated by the time required to deposit each additional egg within a clutch (Charnov and Skinner 1984, 1985; Skinner 1985). This approach was widely adopted, in large part because a rate-maximizing strategy is amenable to mathematically tractable analyses that yield simple analytical solutions. This approach also had the advantage of familiarity, as it was directly analogous to optimal foraging theory developed for predators (Stephens and Krebs 1986). For many parasitoids, however, the time required to deposit eggs is very small compared with the time required to locate hosts; thus, oviposition time can make only a small and often negligible contribution to the cost of reproduction (Godfray 1994). Other workers have argued, therefore, that the trade-off is unlikely to involve only time (Weis et al. 1983; Iwasa et al. 1984; Parker and Courtney 1984; Begon and Parker 1986; Parker and Begon 1986; Godfray 1987b; Mangel 1987, 1989; Charnov and Skinner 1988; Charnov and Stephens 1988). An alternate factor that could mediate a cost of reproduction is the cost of the eggs themselves. This cost can take two forms. First, there may be a physiological cost if the energetic outlay required to mature oocytes accelerates senescence (Roitberg 1989; Kirkwood and Rose 1991; Lessells 1991; Tatar et al. 1993). Second, there may be an opportunity cost, because an egg laid on one host cannot be laid on a subsequently encountered (and potentially higher quality) host. Empirical studies have shown that insect oviposition behavior may change in response to changing egg load, supporting the idea that eggs mediate at least part of the cost of reproduction (Rosenheim and Rosen 1991; Minkenberg et al. 1992; Fletcher et al. 1994; Prokopy et al. 1994; Heimpel and Rosenheim 1995). Nevertheless, many workers continue to argue that egg limitation (defined as the temporary or permanent exhaustion of the supply of mature oocytes) is either extremely rare or completely absent in some parasitoids (Godfray 1987b; Janssen 1989; van Dijken et al. 1991, 1993; Hardy et al. 1992; van Alphen et al. 1992; Visser et al. 1992), and the question has become the focus of debate (Driessen and Hemerik 1992). One question that has not been posed, but which is central to understanding insect life histories, is whether egg limitation is a plausible outcome of the evolutionary process. Here I construct simple models that predict that egg limitation will be a common component of parasitoid life histories. The prediction of egg limitation is derived from simple assumptions of trade-offs between (1) egg size versus egg number; and (2) resource allocations to somatic maintenance versus reproduction.