INTRODUCTION
Resource availability and acquisition are central to life history investment (Williams, 1966; Gadgil and Bossert, 1970; Stearns, 1992; Roff, 1992). Due to competition for resources, negative associations (i.e., physiological trade-offs) between traits often arise when organisms are resource limited (Gadgil and Bossert, 1970; van Noordwijk and de Jong, 1986; Perrin and Sibly, 1993; Zera et al., 1998; Zera and Harshman, 2001). Allocation of resources to reproduction versus immune function represents one such key physiological trade-off (Sheldon and Verhulst, 1996; Lochmiller and Deerenberg, 2000; Norris and Evans, 2000; Partridge et al., 2005; Martin et al., 2008; McKean et al., 2008; Schwenke et al., 2016), and numerous negative associations between these traits have been reported in food-limited organisms including nematodes (Klass, 1977), insects (Chippindale et al., 1993; Chapman et al., 1994; Tatar and Carey, 1995), birds (Gustafsson et al., 1994; Ilmonen et al., 2000; Bonneaud et al., 2004; Ardia, 2005), lizards (French et al., 2007; Cox et al., 2010), and mammals (Koivula et al., 2003).
Beyond the consequences for trade-offs dictated by the number of total calories consumed, only recently have investigators begun to consider the independent effects of macronutrients (i.e., carbohydrates, protein, and fat) on an individual’s life history strategy. This was largely driven by the development of nutritional geometry (Simpson and Raubenheimer, 1995; Simpson et al., 2017), a multidimensional framework for disentangling the effects of energy consumption from those of particular nutrient combinations. The application of this framework has revealed that the amount of macronutrients consumed often mediate life history trade-offs, including those between lifespan and reproduction (Lee et al., 2008; Maklakov et al., 2008; Jensen et al., 2015; Solon-Biet et al., 2015; Rapkin et al., 2017b) and growth and immune function (Cotter et al., 2011).
A recent application of nutritional geometry has illuminated the nutritional landscape underlying the trade-off between immune function (i.e., mounting an encapsulation response) and reproductive effort (i.e., time spent broadcasting a long-range acoustic call for mate attraction) in male crickets, Gryllodes sigillatus (Rapkin et al. , 2018). In this study, crickets were maintained on one of 24 holidic diets varying in protein:carbohydrate (P:C) ratio and total nutritional content that yielded a nutritional landscape with six nutritional rails, along which P:C ratio was held constant but total calories differed. Nutrient intake was measured during sexual maturation, and calling effort and encapsulation ability were subsequently quantified. Rapkin et al. (2018) found that immune function in males was maximized at a P:C ratio of approximately 5:1, whereas calling effort was maximized at a carbohydrate-biased P:C ratio of approximately 1:8. Because optimal expression of each trait occurred at distinct P:C ratios, this study provides important evidence that macronutrient intake, independent of total calories, directs the trade-off between reproduction and immune function.
The ratio of macronutrients available to an individual and the influence on reproduction and immunity may alter the life history investment strategy employed following a pathogenic infection. On one hand, the cost of immunity trade-off hypothesis predicts an increased investment in immunity to fight infection, at a cost to current reproduction (Festa-Bianchet 1988; Gustafsson et al. 1994; Norris et al. 1994; Svensson et al. 1998; Adamo 1999; Jacot et al. 2004; Ahtiainen et al. 2005; Stahlschmidt et al. 2013). Alternatively, individuals may increase their investment in reproduction in response to the threat of infection to their immediate survival, in a life history strategy known as terminal investment (Williams, 1966; Clutton‐Brock, 1984). A recent refinement of this idea, the dynamic terminal investment threshold model, proposes that the tendency of an individual to terminally invest depends on other intrinsic and extrinsic factors, such as age or diet, that alter an individual’s residual reproductive value (i.e., expectation for future offspring) (Duffield et al., 2017). In support of this possibility, Hudson et al. (2019) recently demonstrated that the propensity to terminally invest in female Drosophila melanogasterwas contingent on the amount of protein consumed. Specifically, female flies only expressed terminal investment (i.e., increased egg laying following an infection of Pseudomonas aeruginosa ) when they were fed a high protein diet, whereas infected females fed a diet of lower total protein did not increase egg production relative to uninfected females. This study highlights how nutrition-dependent condition, based on the amount of protein consumed in this example, may interact with infection status to determine an individual’s investment in key life history traits, including reproduction.
Here, we explore how macronutrient intake interacts with simulated infection cue intensity, achieved through a spectrum of immune challenge treatments, to influence expression of life history traits in male decorated crickets, G. sigillatus . Specifically, we quantified reproductive effort (calling effort) and immune function (circulating hemocytes, presence of hemocyte microaggregations, and antibacterial activity of the hemolymph) of males maintained on diets previously shown to maximize calling effort (P:C = 1:8, “high carbohydrate diet”) or a component of immune function, specifically via encapsulation ability (P:C = 5:1, “high protein diet”) (Rapkin et al., 2018). Due to the divergent nutritional demands of calling effort and immune function, we predicted that males would exhibit significantly different life history strategies depending on their macronutrient intake, infection cue intensity, or the interaction between these factors.