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.