Drosophila melanogaster larvae make nutritional choices that minimize developmental time

Abstract

Organisms from slime moulds to humans carefully regulate their macronutrient intake to optimize a wide range of life history characters including survival, stress resistance, and reproductive success. However, life history characters often differ in their response to nutrition, forcing organisms to make foraging decisions while balancing the trade-offs between these effects. To date, we have a limited understanding of how the nutritional environment shapes the relationship between life history characters and foraging decisions. To gain insight into the problem, we used a geometric framework for nutrition to assess how the protein and carbohydrate content of the larval diet affected key life history traits in the fruit fly, Drosophila melanogaster. In no-choice assays, survival from egg to pupae, female and male body size, and ovariole number - a proxy for female fecundity - were maximized at the highest protein to carbohydrate (P:C) ratio (1.5:1). In contrast, development time was minimized at intermediate P:C ratios, around 1:2. Next, we subjected larvae to two-choice tests to determine how they regulated their protein and carbohydrate intake in relation to these life history traits. Our results show that larvae targeted their consumption to P:C ratios that minimized development time. Finally, we examined whether adult females also chose to lay their eggs in the P:C ratios that minimized developmental time. Using a three-choice assay, we found that adult females preferentially laid their eggs in food P:C ratios that were suboptimal for all larval life history traits. Our results demonstrate that D. melanogaster larvae make foraging decisions that trade-off developmental time with body size, ovariole number, and survival. In addition, adult females make oviposition decisions that do not appear to benefit the larvae. We propose that these decisions may reflect the living nature of the larval nutritional environment in rotting fruit. These studies illustrate the interaction between the nutritional environment, life history traits, and foraging choices in D. melanogaster, and lend insight into the ecology of their foraging decisions.

Fitness traits of Drosophila melanogaster (Diptera: Drosophilidae) after long-term laboratory rearing on different diets

“…Quality and amount of nutritive resources, as well as the balance of macronutrients in food, have a strong effect on the life-history traits of D. melanogaster (Lee et al, 2008;Kolss et al, 2009;Kristensen et al, 2011;Schwarz et al, 2014;May et al, 2015;Rodrigues et al, 2015;Simpson et al, 2015;AbedVieillard & Cortot, 2016). Nutritive demands may change during the course of life and may be sex-specifi c, if the sexes maximize fi tness in different ways (Lee et al, 2008;Maklakov et al, 2008;Lihoreau et al, 2016).…”

“…It is recorded that D. melanogaster reared on a protein rich diet are more viable, heavier and larger, and have more ovarioles (Rodrigues et al, 2015). On the other hand, a low level of protein in the diet results in prolonged development, delay in emergence and decrease in egg-to-adult survival, fecundity and growth in D. melanogaster (Wang & Clark, 1995;Tu & Tatar, 2003;Kolss et al, 2009;Rodrigues et al, 2015). Results obtained in this study confi rm the results of the above mentioned studies.…”

“…Certain amounts of protein, carbohydrate, lipid, vitamins and minerals are essential for growth and survival of juveniles (Simpson & Raubenheimer, 1993;Simpson et al, 2004). The amount of protein and carbohydrate in the larval food of D. melanogaster affects their developmental time, egg-to-adult survival and lifespan Heilbronn & Ravussin, 2005;Fanson et al, 2009;Andersen et al, 2010;Kristensen et al, 2011;Merkey et al, 2011;Rodrigues et al, 2015;Reis, 2016). However, it is only protein that determines body and tissue growth in larvae (Britton & Edgar, 1998;Colombani et al, 2003).…”

“…Effects of nutrition can be sex specifi c (Lee & Micchelli, 2013;Reddiex et al, 2013;Nazario-Yepiz et al, 2017). Thus, for females of D. melanogaster the protein to carbohydrate (P : C) ratio affects longevity, egg laying rate and lifetime egg production (Lee et al, 2008;Fanson et al, 2009;Rodrigues et al, 2015).…”

“…However, in nature animals are often exposed to changes in the quality and quantity of food, and in its availability. Consequently, there are changes in their resistance to stress, life-history traits and reproduction (Djawdan et al, 1998;Bross et al, 2005;Broughton et al, 2005;Carsten et al, 2005;Burger et al, 2007;Sisodia & Singh, 2012;Reddiex et al, 2013;AbedVieillard et al, 2014;Rodrigues et al, 2015;Kristensen et al, 2016).…”