Trade-off 3: Energy allocation between stressors and life-history traits
Stressors can not only directly reduce growth and reproduction of organisms (e.g. by disrupting endocrine systems (Rattan & Flaws 2019) or by shortening telomeres (Chatelain et al. 2020)), but they can also indirectly reduce fitness by demanding energy that could otherwise be allocated to growth and reproduction (Rohr et al. 2004; Portner & Knust 2007; Correa-Araneda et al. 2017). A fundamental tenet of basic life history theory is that adaptive allocation to competing demands depends on the marginal benefits versus costs of additional investment in each demand (Roff 2002). Nonlinearities involving accelerating costs or benefits of increased investment can also produce aforementioned fitness cliffs (threshold effects), where here, even a small reduction in investment in a given demand results in a large decrease in fitness. Life history studies suggest that, although there are exceptions, these nonlinearities are often associated with strong competition, or size/condition-dependent safety (Einum & Fleming 1999; Luttbeg & Sih 2010). Being near such a threshold could constrain organisms to allocate sufficient energy to a given demand to prevent falling over a fitness cliff. We next discuss some implications of this basic concept for how organisms might allocate energy to physiological responses to stressors versus competing life history demands. Intriguing insights come from acknowledging that adaptive allocation strategies involving multiple stressors can shift in non-intuitive ways that can be predicted by life history theory.
When energetic requirements for competing demands (e.g., for growth, reproduction, or other survival needs beyond coping with the focal stressors) are close to a fitness cliff, multiple stressors can have synergistic negative impacts through the combined energetic loads they place on an organism. That is, it is clear, through the lens of life-history theory, that stressors need not interact directly to drive strong synergistic effects on the organism; these can manifest through the co-occurrence of independent stressors at a sensitive level along the continuum of an organism’s energetic state.
When physiological demands of stressors and life history demands are both near fitness cliffs, the need to divert energy to cope with stressors is particularly likely to produce strong indirect, negative impacts on fitness through reduced growth, development or reproduction. Life history stages that suffer higher marginal costs of reduced energy investment should be particularly vulnerable to suffering indirect costs of physiological demands of stressors. Life stages vary in their vulnerability to different combinations of stressors, and this varies across taxa (Stoks 2001; Rohr et al. 2011; Przeslawski et al. 2015; Watson et al. 2018; Tran et al. 2020). Yet, for many taxa, when juveniles divert energy to dealing with multiple stressors rather than development, this results in particularly strong negative effects, involving both increased sublethal effects and higher mortality (Byrne & Przeslawski 2013; Przeslawski et al. 2015; Lange et al. 2018; Miler et al. 2020). For example, echinoderm larvae can show elevated mortality, impaired development and signs of metabolic depression following exposure to heightened temperature and p CO2 (Byrne & Przeslawski 2013; Przeslawski et al. 2015). Such costs of reduced growth and development can be particularly strong in systems with seasonal time horizons, where growing to a threshold size or stage or accumulating sufficient energy reserves in a given time period is crucial for survival (e.g., for migration, overwintering or metamorphosis when ephemeral habitats disappear).
Similarly, when reproduction requires an abundance of energy, females can suffer higher costs of coping with stressors during reproductive periods than during non-reproductive periods. French et al. (2007) experimentally manipulated reproductive investment in female tree lizards (Urosaurus ornatus ) by stimulating vitellogenesis and found that lizards that had higher reproductive investment also had suppressed immune systems when resources were limited. In particular, if offspring fitness is a strongly nonlinear (e.g., sigmoidal) function of female parental investment, this can cause females to invest more into reproduction and less in coping with stressors, thus yielding larger direct costs of stressors. Alternatively, animals exposed to stress sometimes reduce their investment per offspring (Domis et al.2013; Jager et al. 2013). If this substantially reduces average offspring survival (e.g., if offspring survival falls over a fitness cliff), then adult exposure to stressors can result in a large indirect cost in terms of both offspring and adult fitness. For example, blue orchard bees (Osmia lignaria ) exposed to resource limitation and the pesticide imidacloprid suffered an additive reduction in reproductive fitness via a lowered probability of successful nesting and a reduced number of offspring produced (Stuligross & Williams 2020). Additionally, offspring sex ratios became male biased, increasing the likelihood of further reductions in reproductive fitness in the future (Stuligross & Williams 2020).
For males, mating success often depends heavily on possessing either large relative size or ornaments (Andersson 1994); in these cases, males can suffer a fitness cliff where reduced investment in sexually selected traits can result in little or no mating success. Strong sexual selection can then favor males diverting their limited energy into sexually selected traits, even at the cost of reduced investment in physiological responses to stressors. Such scenarios would result in a strong direct cost (e.g. mortality due to the stressors) of exposure to stressors. Alternatively, if some sites have abundant food but high risk, sexual selection can favor taking greater risks (e.g., increasing exposure to predators or other stressors) to bring in the energy required to invest in both ornaments and in physiological responses to stressors to maintain condition; the increased exposure to predators would represent a large indirect cost of exposure to stressors.