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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The Geometry of Nutrient Space–Based Life-History Trade-Offs: Sex-Specific Effects of Macronutrient Intake on the Trade- Off between Encapsulation Ability and Reproductive Effort in Decorated Crickets
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.
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- Award ID(s):
- 1634878
- PAR ID:
- 10065062
- Date Published:
- Journal Name:
- The American naturalist
- Volume:
- 191
- Issue:
- 4
- ISSN:
- 0003-0147
- Page Range / eLocation ID:
- 452-474
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract 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
Gryllodes sigillatus . Using the Geometric Framework for Nutrition, we restrict male and female crickets to diets varying in the ratio of protein to carbohydrates and total nutrient content to quantify the effects on life span and daily reproductive effort in the sexes. We then use inbred lines to estimate the quantitative genetic basis of nutrient choice in males and females. We combine the nutrient effects and genetic estimates to predict the magnitude of evolutionary constraint for these traits in each sex. Finally, we present male and female crickets with a much broader range of diet pairs to determine how the sexes actively regulate their intake of nutrients.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
G. sigillatus .A free
Plain Language Summary can be found within the Supporting Information of this article. -
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Abstract Nutritional geometry has advanced our understanding of how macronutrients (e.g., proteins and carbohydrates) influence the expression of life history traits and their corresponding trade‐offs. For example, recent work has revealed that reproduction and immune function in male decorated crickets are optimized at very different protein:carbohydrate (P:C) dietary ratios. However, it is unclear how an individual's macronutrient intake interacts with its perceived infection status to determine investment in reproduction or other key life history traits. Here, we employed a fully factorial design in which calling effort and immune function were quantified for male crickets fed either diets previously demonstrated to maximize calling effort (P:C = 1:8) or immune function (P:C = 5:1), and then administered a treatment from a spectrum of increasing infection cue intensity using heat‐killed bacteria. Both diet and a simulated infection threat independently influenced the survival, immunity, and reproductive effort of males. If they called, males increased calling effort at the low infection cue dose, consistent with the terminal investment hypothesis, but interpretation of responses at the higher threat levels was hampered by the differential mortality of males across infection cue and diet treatments. A high protein, low carbohydrate diet severely reduced the health, survival, and overall fitness of male crickets. There was, however, no evidence of an interaction between diet and infection cue dose on calling effort, suggesting that the threshold for terminal investment was not contingent on diet as investigated here.
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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.
Nazca boobies (
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.
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