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Journal ArticleDOI

Lifespan and reproduction in Drosophila: New insights from nutritional geometry

TL;DR: The use of recent techniques in nutrition research to quantify the detailed relationship between diet, nutrient intake, lifespan, and reproduction in Drosophila melanogaster indicates a role for both direct costs of reproduction and other deleterious consequences of ingesting high levels of protein.
Abstract: Modest dietary restriction (DR) prolongs life in a wide range of organisms, spanning single-celled yeast to mammals. Here, we report the use of recent techniques in nutrition research to quantify the detailed relationship between diet, nutrient intake, lifespan, and reproduction in Drosophila melanogaster. Caloric restriction (CR) was not responsible for extending lifespan in our experimental flies. Response surfaces for lifespan and fecundity were maximized at different protein–carbohydrate intakes, with longevity highest at a protein-to-carbohydrate ratio of 1:16 and egg-laying rate maximized at 1:2. Lifetime egg production, the measure closest to fitness, was maximized at an intermediate P:C ratio of 1:4. Flies offered a choice of complementary foods regulated intake to maximize lifetime egg production. The results indicate a role for both direct costs of reproduction and other deleterious consequences of ingesting high levels of protein. We unite a body of apparently conflicting work within a common framework and provide a platform for studying aging in all organisms.

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Citations
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Journal ArticleDOI
TL;DR: The Geometric Framework, a state-space nutritional modeling method, was used to measure interactive effects of dietary energy, protein, fat, and carbohydrate on food intake, cardiometabolic phenotype, and longevity in mice fed one of 25 diets ad libitum, suggesting that longevity can be extended in ad Libitum-fed animals by manipulating the ratio of macronutrients.

732 citations


Cites background or result from "Lifespan and reproduction in Drosop..."

  • ...The results are consistent with recent reports in invertebrates showing that the ratio of protein to carbohydrate in the diet influences lifespan (Lee et al., 2008; Piper et al., 2011)....

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  • ...…the susceptibility to obesity and metabolic disease, immune function, and resistance to infectious diseases (Blumfield et al., 2012; Gosby et al., 2011; Huang et al., 2013; Lee et al., 2008; Mayntz et al., 2009; Piper et al., 2011; Ponton et al., 2011; Simpson and Raubenheimer, 2009, 2012)....

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  • ...In particular, it has emerged that the balance of protein to nonprotein energy in the diet is especially significant, influencing total energy intake, growth and development, body composition, reproduction, aging, gut microbial ecology, the susceptibility to obesity and metabolic disease, immune function, and resistance to infectious diseases (Blumfield et al., 2012; Gosby et al., 2011; Huang et al., 2013; Lee et al., 2008; Mayntz et al., 2009; Piper et al., 2011; Ponton et al., 2011; Simpson and Raubenheimer, 2009, 2012)....

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  • ...The development of the Geometric Framework for nutrition (GF) now provides a platform for taming this complexity (Lee et al., 2008; Mayntz et al., 2005; Piper et al., 2011; Simpson and Raubenheimer, 2009, 2012)....

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  • ...Thus, we relate macronutrient intakes to longevity, in particular testing the extent to which lifespan in ad libitum-fed mice is determined by calorie intake per se or by the balance of protein to carbohydrate, as recently proposed from GF studies of insects (Fanson et al., 2009; Lee et al., 2008)....

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Journal ArticleDOI
24 Dec 2009-Nature
TL;DR: Reduced activity of the insulin/insulin-like growth factor signalling pathway extends lifespan in diverse organisms, and it is found that it also protects against the shortening of lifespan with full feeding.
Abstract: Dietary restriction extends healthy lifespan in diverse organisms and reduces fecundity. It is widely assumed to induce adaptive reallocation of nutrients from reproduction to somatic maintenance, aiding survival of food shortages in nature. If this were the case, long life under dietary restriction and high fecundity under full feeding would be mutually exclusive, through competition for the same limiting nutrients. Here we report a test of this idea in which we identified the nutrients producing the responses of lifespan and fecundity to dietary restriction in Drosophila. Adding essential amino acids to the dietary restriction condition increased fecundity and decreased lifespan, similar to the effects of full feeding, with other nutrients having little or no effect. However, methionine alone was necessary and sufficient to increase fecundity as much as did full feeding, but without reducing lifespan. Reallocation of nutrients therefore does not explain the responses to dietary restriction. Lifespan was decreased by the addition of amino acids, with an interaction between methionine and other essential amino acids having a key role. Hence, an imbalance in dietary amino acids away from the ratio optimal for reproduction shortens lifespan during full feeding and limits fecundity during dietary restriction. Reduced activity of the insulin/insulin-like growth factor signalling pathway extends lifespan in diverse organisms, and we find that it also protects against the shortening of lifespan with full feeding. In other organisms, including mammals, it may be possible to obtain the benefits to lifespan of dietary restriction without incurring a reduction in fecundity, through a suitable balance of nutrients in the diet.

680 citations

Journal ArticleDOI
TL;DR: Comparative studies of nutrient regulation suggest coexisting generalist herbivores occupy unique nutritional feeding niches, and work with pathogens and parasitoids has revealed the manner in which top-down pressures influence patterns of nutrient intake.
Abstract: The primary reason animals, including insect herbivores, eat is to acquire a mix of nutrients needed to fuel the processes of growth, development, and reproduction. Most insect herbivores strongly regulate their nutrient intake when given the opportunity. When they are restricted to imbalanced diets, they employ regulatory rules that govern the extent to which nutrients occurring in excess or deficit are eaten. Insect herbivores also regularly encounter allelochemicals as they eat, and recent work indicates the effect an allelochemical has on nutrient regulation, and insect herbivore performance, is modified depending on a food's nutrient composition. Comparative studies of nutrient regulation suggest coexisting generalist herbivores occupy unique nutritional feeding niches, and work with pathogens and parasitoids has revealed the manner in which top-down pressures influence patterns of nutrient intake. Insect herbivores regulate their nutrient intake using pre- and postingestive mechanisms, plus learning, and there is evidence that some of these mechanisms are shaped by natural selection.

656 citations

Journal ArticleDOI
TL;DR: This review reviews the evidence in support of the contention that ROS production will constitute a primary and universal constraint in life-history evolution, and integrates the above suggestions into one life- history framework.
Abstract: Evolutionary theory is firmly grounded on the existence of trade-offs between life-history traits, and recent interest has centred on the physiological mechanisms underlying such trade-offs. Several branches of evolutionary biology, particularly those focusing on ageing, immunological and sexual selection theory, have implicated reactive oxygen species (ROS) as profound evolutionary players. ROS are a highly reactive group of oxygen-containing molecules, generated as common by-products of vital oxidative enzyme complexes. Both animals and plants appear to intentionally harness ROS for use as molecular messengers to fulfil a wide range of essential biological processes. However, at high levels, ROS are known to exert very damaging effects through oxidative stress. For these reasons, ROS have been suggested to be important mediators of the cost of reproduction, and of trade-offs between metabolic rate and lifespan, and between immunity, sexual ornamentation and sperm quality. In this review, we integrate the above suggestions into one life-history framework, and review the evidence in support of the contention that ROS production will constitute a primary and universal constraint in life-history evolution.

615 citations


Cites background or result from "Lifespan and reproduction in Drosop..."

  • ...to carbohydrate that correspond to the longest lifespans differ from the ratios that correspond to highest reproductive success (Lee et al. 2008; Maklakov et al. 2008),...

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  • ...Yet, recent studies in Drosophila (Mair et al. 2005; Lee et al. 2008; Skorupa et al. 2008) and Teleogryllus crickets (Maklakov et al. 2008) have clearly indicated that in these systems, it is nutrient, rather than caloric, restriction that plays the major role in modulating lifespan....

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  • ...Two complementary studies experimentally increased the costs of reproduction in female Drosophila melanogaster by stimulating egg production through supplementation with either yeast (Wang et al. 2001) or a juvenile hormone analogue— methoprene (Salmon et al. 2001)....

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  • ...Yet, recent studies in Drosophila (Mair et al. 2005; Lee et al. 2008; Skorupa et al. 2008) and Teleogryllus crickets (Maklakov et al....

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  • ...For instance, in both species, the ratios of protein to carbohydrate that correspond to the longest lifespans differ from the ratios that correspond to highest reproductive success (Lee et al. 2008; Maklakov et al. 2008), consistent with the idea that a trade-off exists between lifespan and fitness....

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Journal ArticleDOI
TL;DR: This work synthesizes ideas and evidence linking sex and ageing, and makes the case that a focus on this fascinating problem will ultimately lead to a more complete understanding of both the evolution of ageing and the Evolution of sexual strategies.
Abstract: Summary 1Classic evolutionary models interpret ageing as a cost of reproduction, but evolutionary research has thus far largely neglected the conceptual links between the evolution of ageing and a key mode of selection on male and female reproductive strategies – sexual selection and sexual conflict. 2We synthesize ideas and evidence linking sex and ageing, and make the case that a focus on this fascinating problem will ultimately lead to a more complete understanding of both the evolution of ageing and the evolution of sexual strategies. 3The primary and secondary differentiation of male and female reproductive strategies is expected to produce sex-specific optima for traits that affect longevity and ageing rate, often favouring a ‘live fast, die young’ strategy in males, relative to females, although numerous exceptions to this pattern are observed and sex-differences in ageing rate, in particular, remain poorly understood. 4Conversely, environmental factors that influence life expectancy or ageing rate can thereby determine the magnitude or even sign of sexual selection. 5Sexual conflict is expected to displace the sexes from their sex-specific life-history optima through sexually antagonistic interactions, as well as sex-specific selection on loci expressed in both sexes. 6Despite the availability of interesting and testable hypotheses linking sexual selection and ageing, relevant empirical studies are remarkably sparse, and the complex relation between sex, mortality rate and ageing remains poorly understood.

469 citations

References
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Journal ArticleDOI
09 Nov 2000-Nature
TL;DR: Genetic studies in genetically tractable model organisms established that ageing is indeed regulated by specific genes, and allowed an analysis of the pathways involved, linking physiology, signal transduction and gene regulation.
Abstract: Searches for genes involved in the ageing process have been made in genetically tractable model organisms such as yeast, the nematode Caenorhabditis elegans, Drosophila melanogaster fruitflies and mice. These genetic studies have established that ageing is indeed regulated by specific genes, and have allowed an analysis of the pathways involved, linking physiology, signal transduction and gene regulation. Intriguing similarities in the phenotypes of many of these mutants indicate that the mutations may also perturb regulatory systems that control ageing in higher organisms.

1,306 citations

Journal ArticleDOI
TL;DR: It is shown that inhibition of TOR signaling pathway by alteration of the expression of genes in this nutrient-sensing pathway, which is conserved from yeast to human, extends lifespan in a manner that may overlap with known effects of dietary restriction on longevity.

1,205 citations


"Lifespan and reproduction in Drosop..." refers background in this paper

  • ..., TOR) pathways (30), and damage to organs arising from nitrogenous breakdown products....

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Journal ArticleDOI
TL;DR: Recent findings that are beginning to clarify the mechanisms by which CR results in longevity and robust health, which might open new avenues of therapy for diseases of ageing are summarized.
Abstract: Calorie restriction (CR) is the only experimental manipulation that is known to extend the lifespan of a number of organisms including yeast, worms, flies, rodents and perhaps non-human primates. In addition, CR has been shown to reduce the incidence of age-related disorders (for example, diabetes, cancer and cardiovascular disorders) in mammals. The mechanisms through which this occurs have been unclear. CR induces metabolic changes, improves insulin sensitivity and alters neuroendocrine function in animals. In this review, we summarize recent findings that are beginning to clarify the mechanisms by which CR results in longevity and robust health, which might open new avenues of therapy for diseases of ageing.

954 citations


"Lifespan and reproduction in Drosop..." refers background in this paper

  • ...It is widely held that the life-extending effects of dietary restriction (DR) are due to caloric restriction (CR) (1, 8, 9), but recently this view has been challenged by experiments suggesting that specific nutrients (proteins and certain amino acids) rather than energy are responsible (10–12)....

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Journal ArticleDOI
TL;DR: The absence of adequate information on the effects of good-quality, calorie-restricted diets in nonobese humans reflects the difficulties involved in conducting long-term studies in an environment so conducive to overfeeding.

647 citations


"Lifespan and reproduction in Drosop..." refers background in this paper

  • ...There is growing interest in the relationship between dietary restriction and quality and length of life in humans, although experimental data are lacking and difficult to obtain (7)....

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