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.