Abstract
Dietary restriction (DR) is one of the main experimental paradigms to investigate the mechanisms that determine lifespan and aging. Yet, the exact nutritional parameters responsible for DR remain unclear. Recently, the advent of the geometric framework of nutrition (GF) has refocussed interest from calories to dietary macronutrients. However, GF experiments focus on invertebrates, with the importance of macronutrients in vertebrates still widely debated. This has led to the suggestion of a fundamental difference in the mode of action of DR between vertebrates and invertebrates, questioning the suggestion of an evolutionarily conserved mechanism. The use of dietary dilution rather than restriction in GF studies makes comparison with traditional DR studies difficult. Here, using a novel nonmodel vertebrate system (the stickleback fish, Gasterosteus aculeatus), we test the effect of macronutrient versus calorie intake on key fitness‐related traits, both using the GF and avoiding dietary dilution. We find that the intake of macronutrients rather than calories determines both mortality risk and reproduction. Male mortality risk was lowest on intermediate lipid intakes, and female risk was generally reduced by low protein intakes. The effect of macronutrient intake on reproduction was similar between the sexes, with high protein intakes maximizing reproduction. Our results provide, to our knowledge, the first evidence that macronutrient, not caloric, intake predicts changes in mortality and reproduction in the absence of dietary dilution. This supports the suggestion of evolutionary conservation in the effect of diet on lifespan, but via variation in macronutrient intake rather than calories.
Highlights
Understanding how diet influences traits such as aging, survival and reproduction is a fundamental question in biology with clear application to human health (Fontana & Partridge, 2015)
In a rare application of the geometric framework of nutrition (GF) to a vertebrate species, it was the intake of protein and carbohydrate that determined lifespan in mice rather than overall calorie intake (Solon‐Biet et al, 2014), suggesting that the same patterns are true in vertebrates as well as invertebrates
We address the following questions: (a) Is calorie or macronutrient intake the key determinant of mortality risk in a nonmodel vertebrate species? (b) Are survival and reproduction maximized at different macronutrient intakes suggesting a diet‐mediated trade‐off? and (c) Are there sex differences in the effect of macronutrient intake and calories on survival and reproduction when males experience more reproductive costs? We explore other key fitness and health‐related traits, such as growth and body condition (e.g., Solon‐Biet et al, 2014; Moatt et al, 2017)
Summary
Understanding how diet influences traits such as aging, survival and reproduction is a fundamental question in biology with clear application to human health (Fontana & Partridge, 2015). A comprehensive series of studies varying dietary protein content, but not using the GF, found that protein restriction could not produce the same effects as caloric restriction (e.g., Mitchell, Delville, et al, 2015; Mitchell, Tang, et al, 2015) The disparity between these studies and those of Solon‐Biet et al (2014) has been suggested to result from key methodological differences (Speakman et al, 2016). High protein intakes increased reproductive effort, providing evidence for a macronutrient mediated trade‐off between reproduction and mortality in sticklebacks
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