Life history theory is based on the assumption that resources are finite so that traits competing for this common pool of resources will experience a trade-off. The shared resource most commonly studied is food and studies typically manipulate resource acquisition by varying diet quantity or quality without considering the specific nutrients involved. Recent studies using the Geometric Framework (GF), however, suggest that life-history trade-offs are often regulated by the intake of specific nutrients. Despite this, a robust framework documenting the existence and quantifying the strength of nutritionally based trade-offs currently does not exist for studies using the GF. Here, we provide a conceptual framework showing that such trade-offs occur when life-history traits are maximised in different regions of nutrient space and that this divergence can be quantified by the overlap in the 95% confidence region (CR) of the global maxima, the angle (θ) between the linear nutritional vectors and the Euclidean distance (d) between the global maxima for each trait. We then empirically tested this framework by examining the effects of protein (P) and carbohydrate (C) intake on the trade-off between reproduction and immune function in male and female decorated crickets (Gryllodes sigillatus). Encapsulation ability and egg production in females increased with the intake of both nutrients, being maximised at a P:C ratio of 1.04:1 and 1:1.17, respectively. In contrast, encapsulation ability in males only increased with the intake of P being maximised at a P:C ratio of 5.14:1, whereas calling effort increased with the intake of C but decreased with the intake of P and was maximized at a P:C ratio of 1:7.08. Consequently, the trade-off between reproduction and encapsulation ability is much larger in males than females, a view supported by the non-overlapping 95% CRs on the global maxima for these traits in males and the larger estimates of θ and d. The sexes regulated their intake of nutrients in a similar way under dietary choice, at a P:C ratio of 1:2 and 1:1.84 in males and females, respectively. Although this ratio was more closely aligned with the optima for immune function and reproduction in females than males, neither sex optimally regulated their nutrient intake. Collectively, our study highlights that greater consideration should be given to the intake of specific nutrients when examining nutritionally based life-history trade-offs and how this varies across the sexes.
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Intralocus sexual conflict over optimal nutrient intake and the evolution of sex differences in life span and reproduction
Despite widespread variation in life span across species, three clear patterns exist: sex differences in life span are ubiquitous, life span is commonly traded against reproduction, and nutrition has a major influence on these traits and how they trade‐off. One process that potentially unites these patterns is intralocus sexual conflict over the optimal intake of nutrients for life span and reproduction. If nutrient intake has sex‐specific effects on life span and reproduction but nutrient choice is genetically linked across the sexes, intralocus sexual conflict will occur and may prevent one or both sexes from feeding to their nutritional optima. Here we determine the potential for this process to operate in the decorated cricket We show that protein and carbohydrate intake have contrasting effects on life span and reproduction in the sexes and that there are strong positive intersexual genetic correlations for the intake of these nutrients under dietary choice. This is predicted to accelerate the evolutionary response of nutrient intake in males but constrain it in females, suggesting they are losing the conflict. Supporting this view, males and females regulate nutrient intake to a common nutrient ratio that was not perfectly optimal for life span or reproduction in either sex, especially in females. Our findings show that intralocus sexual conflict over the optimal intake of nutrients is likely to be an important process generating sex differences in life span and reproduction and may help explain why females age faster and live shorter than males in
A free
- Award ID(s):
- 1654028
- PAR ID:
- 10445879
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Functional Ecology
- Volume:
- 36
- Issue:
- 4
- ISSN:
- 0269-8463
- Page Range / eLocation ID:
- p. 865-881
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Life-history theory assumes that resources are finite and that there may be trade-offs between traits competing for this common resource pool. The limiting resource most commonly studied is food and studies typically manipulate resource acquisition by varying diet quantity or quality without considering the specific nutrients involved. Recent studies using the Geometric Framework (GF) however, suggest that life-history trade-offs are often regulated by the intake of specific nutrients. Despite this, we lack a robust framework identifying and quantifying the strength of nutritionally based trade-offs using the GF. Here, we provide a conceptual framework showing that such trade-offs occur when life-history traits are maximised in different regions of nutrient space and that this divergence can be quantified by the overlap in the 95% confidence region (CR) of the global maxima, the angle (θ) between the linear nutritional vectors, and the Euclidean distance (d) between the global maximum for each trait. We then empirically test this framework by examining the effects of protein (P) and carbohydrate (C) intake on the trade-off between reproduction and immune function in male and female decorated crickets (Gryllodes sigillatus). Encapsulation ability and egg production in females increased with the intake of both nutrients, being maximised at a P:C ratio of 1.04:1 and 1:1.17, respectively. In contrast, encapsulation ability in males only increased with the intake of P being maximised at a P:C ratio of 5.14:1, whereas calling effort increased with C intake but decreased with P intake and was maximized at a P:C ratio of 1:7.08. Consequently, the trade-off between reproduction and encapsulation ability is much larger in males than females, a view supported by the non-overlapping 95% CRs on the global maxima for these traits in males but not females and the larger estimates of θ and d. When given dietary choice, the sexes regulated their nutrient intake in a similar way, at a P:C ratio of 1:2 and 1:1.84 in males and females, respectively. Although this ratio was more closely aligned with the optima for immune function and reproduction in females than males, neither sex optimally regulated their nutrient intake to maximise the expression of reproductive effort or immune function or, in the case of males, allow for moderate expression of both traits. Collectively, our study highlights that greater consideration should be given to the intake of specific nutrients when examining nutritionally based life-history trade-offs and how this varies between the sexes.more » « less
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Abstract Sex differences in animal coloration often result from sex‐dependent regulatory mechanisms. Still, some species exhibit incomplete sexual dimorphism as females carry a rudimentary version of a costly male trait, leading to intralocus sexual conflict. The underlying physiology and condition dependence of these traits can inform why such conflicts remain unresolved. In eastern fence lizards (
Sceloporus undulatus ), blue iridophore badges are found in males and females, but melanin pigmentation underneath and surrounding badges is male‐exclusive. We track color saturation and area of badges across sexual maturity, and their relationship to individual quality (body condition and immunocompetence) and relevant hormones (testosterone and corticosterone). Saturation and testosterone were positively correlated in both sexes, but hormone and trait had little overlap between males and females. Saturation was correlated with body condition and immunocompetence in males but not in females. Co‐regulation by androgens may have released females from resource allocation costs of color saturation, even when in high condition. Badge area was independent of testosterone, but associated with low corticosterone in females, indicating that a nonsex hormone underlies incomplete sexual dimorphism. Given the evidence in this species for female reproductive costs associated with ornamentation, this sex‐nonspecific regulation of an honest signal may underlie intralocus sexual conflict. -
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Abstract Dietary macronutrients regulate life span and aging, yet little is known about their evolutionary effects. Here, we examine the evolutionary response of these traits in decorated crickets (Gryllodes sigillatus) maintained on diets varying in caloric content and protein-to-carbohydrate ratio. After 37 generations, each population was split: half remained on the evolution diet, and half switched to a standardized diet. Crickets lived longer and aged slower when evolving on high-calorie (both sexes) and carbohydrate-biased (females only) diets and had lower baseline mortality on high-calorie (females only) diets. However, on the standardized diet, crickets lived longer when evolving on high-calorie diets (both sexes), aged slower on high-calorie (females only) and carbohydrate-biased (both sexes) diets, and had lower baseline mortality on high-calorie (males only) and protein-biased (both sexes) diets. Life span was longer, and baseline mortality was lower when provided with the evolution vs. the standardized diet, but the aging rate was comparable. Moreover, life span was longer, aging slower (females only), and baseline mortality was lower (males only) compared to our evolved baseline, suggesting varying degrees of dietary adaptation. Collectively, we show dietary components influence the evolution of life span and aging in different ways and highlight the value of combining experimental evolution with nutritional geometry.
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Abstract Under life‐history theories of ageing, increased senescence should follow relatively high reproductive effort. This expectation has rarely been tested against senescence varying between and within the two sexes, although such an approach may clarify the origins of sex‐specific ageing in the context of a given mating system.
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Sula granti ; a seabird) practise serial monogamy and biparental care. A male‐biased population sex ratio results in earlier and more frequent breeding by females. Based on sex‐specific reproductive schedules, females were expected to show faster age‐related decline for survival and reproduction. Within each sex, high reproductive effort in early life was expected to reduce late‐life performance and accelerate senescence.Longitudinal data were used to (a) evaluate the sex specificity of reproductive and actuarial senescence and then (b) test for early‐/late‐life fitness trade‐offs within each sex. Within‐sex analyses inform an interpretation of sex differences in senescence based on costs of reproduction. Analyses incorporated individual heterogeneity in breeding performance and cohort‐level differences in early‐adult environments.
Females showed marginally more intense actuarial senescence and stronger age‐related declines for fledging success. The opposite pattern (earlier and faster male senescence) was found for breeding probability. Individual reproductive effort in early life positively predicted late‐life reproductive performance in both sexes and thus did not support a causal link between early‐reproduction/late‐life fitness trade‐offs and sex differences in ageing. A high‐quality diet in early adulthood reduced late‐life survival (females) and accelerated senescence for fledging success (males).
This study documents clear variation in ageing patterns—by sex, early‐adult environment and early‐adult reproductive effort—with implications for the role mating systems and early‐life environments play in determining ageing patterns. Absent evidence for a disposable soma mechanism, patterns of sex differences in senescence may result from age‐ and condition‐dependent mate choice interacting with this population's male‐biased sex ratio and mate rotation.
