Abstract
Nutritional variation across the lifetime can have significant and sex-specific impacts on fitness. Using Drosophila melanogaster, we measured these impacts by testing the effects on life span and reproductive success of high or low yeast content in developmental versus adult diets, separately for each sex. We tested two hypotheses: that dietary mismatches between development and adulthood are costly and that any such costs are sex-specific. Overall, the results revealed the rich and complex responses of each sex to dietary variation across the lifetime. Contrary to the first hypothesis, dietary mismatches between developmental and adult life stages were not universally costly. Where costs of nutritional variation across the life course did occur, they were sex-, context-, and trait-specific, consistent with hypothesis 2. We found effects of mismatches between developmental and adult diets on reproductive success in females but not males. Adult diet was the main determinant of survival, and life span was significantly longer on high yeast adult food, in comparison to low, in both sexes. Developing on a high yeast diet also benefited adult female life span and reproductive success, regardless of adult diet. In contrast, a high yeast developmental diet was only beneficial for male life span when it was followed by low yeast adult food. Adult diet affected mating frequency in opposing directions, with males having higher mating frequency on high and females on low, with no interaction with developmental diet for either sex. The results emphasize the importance of sex differences and of the directionality of dietary mismatches in the responses to nutritional variation.
Highlights
Nutritional variation across the lifetime can have significant and sex-specific impacts on fitness
Mismatches in the quality or quantity of diets between developmental and adult stages could be crucial determinants of fitness, if the anticipated nutritional environment set during development is not subsequently encountered [9,10,11]. This is the basis of the thrifty phenotype (TP) hypothesis discussed later [9] and, in principle, applies to any type of dietary mismatch encountered across the lifetime
Costs of dietary mismatching can be minimized by: (i) a switch from a poor developmental to good adult nutrition leading to compensatory feeding and catch-up growth after the dietary switch, reducing the costs from the “poor start” [2,4,18]; (ii) carry-through benefits accrued from a nutritionally rich developmental diet to ameliorate a poor adult diet [13]; (iii) a harsh developmental environment acting as a filter for developmental viability, selecting only the most resilient individuals, with higher average fitness (reviewed by May and colleagues [5])
Summary
Nutritional variation across the lifetime can have significant and sex-specific impacts on fitness. Mismatches in the quality or quantity of diets between developmental and adult stages could be crucial determinants of fitness, if the anticipated nutritional environment set during development is not subsequently encountered [9,10,11] This is the basis of the thrifty phenotype (TP) hypothesis discussed later [9] and, in principle, applies to any type of dietary mismatch encountered across the lifetime. In addition to any dietary mismatching, it is predicted the responses of individuals of each sex will depend on whether a poor versus good diet is initially encountered during development, and how these interact with whatever dietary environment experienced during adulthood Such effects will depend on the variation in diet quality, the nutritional sensitivity of each sex and the duration of any nutritional stress or surfeit in each life stage [12,13], reviewed by Flatt and Schmidt [14]. Costs of dietary mismatching can be minimized by: (i) a switch from a poor developmental to good adult nutrition leading to compensatory feeding and catch-up growth after the dietary switch, reducing the costs from the “poor start” [2,4,18]; (ii) carry-through (silver spoon) benefits (eg, fat reserves) accrued from a nutritionally rich developmental diet to ameliorate a poor adult diet [13]; (iii) a harsh developmental environment acting as a filter for developmental viability, selecting only the most resilient individuals, with higher average fitness (reviewed by May and colleagues [5])
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