Thermal and nutritional environments during development exert different effects on adult reproductive success in...

Environments experienced during development have long-lasting consequences for adult performance and fitness. The "environmental matching" hypothesis predicts that individuals perform best when adult and developmental environments match whereas the "silver spoon" hypothesis expects that fitness is higher in individuals developed under favorable environments regardless of adult environments. Temperature and nutrition are the two most influential determinants of environmental quality, but it remains to be elucidated which of these hypotheses better explains the long-term effects of thermal and nutritional histories on adult fitness traits. Here we compared how the temperature and nutrition of larval environment would affect adult survivorship and reproductive success in the fruit fly, Drosophila melanogaster. The aspect of nutrition focused on in this study was the dietary protein-to-carbohydrate (P:C) ratio. The impact of low developmental and adult temperature was to improve adult survivorship. High P:C diet had a negative effect on adult survivorship when ingested during the adult stage, but had a positive effect when ingested during development. No matter whether adult and developmental environments matched or not, females raised in warm and protein-enriched environments produced more eggs than those raised in cool and protein-limiting environments, suggesting the presence of a significant silver spoon effect of larval temperature and nutrition. The effect of larval temperature on adult egg production was weak but persisted across the early adult stage whereas that of larval nutrition was initially strong but diminished rapidly after day 5 posteclosion. Egg production after day 5 was strongly influenced by the P:C ratio of the adult diet, indicating that the diet contributing mainly to reproduction had shifted from larval to adult diet. Our results highlight the importance of thermal and nutritional histories in shaping organismal performance and fitness and also demonstrate how the silver spoon effects of these aspects of environmental histories differ fundamentally in their nature, strength, and persistence.