LIFE-HISTORY CONSEQUENCES OF ADAPTATION TO LARVAL NUTRITIONAL STRESS IN DROSOPHILA

Many animal species face periods of chronic nutritional stress during which the individuals must continue to develop, grow, and/or reproduce despite low quantity or quality of food. Here, we use experimental evolution to study adaptation to such chronic nutritional stress in six replicate Drosophila melanogaster populations selected for the ability to survive and develop within a limited time on a very poor larval food. In unselected control populations, this poor food resulted in 20% lower egg‐to‐adult viability, 70% longer egg‐to‐adult development, and 50% lower adult body weight (compared to the standard food on which the flies were normally maintained). The evolutionary changes associated with adaptation to the poor food were assayed by comparing the selected and control lines in a common environment for different traits after 29–64 generations of selection. The selected populations evolved improved egg‐to‐adult viability and faster development on poor food. Even though the adult dry weight of selected flies when raised on the poor food was lower than that of controls, their average larval growth rate was higher. No differences in proportional pupal lipid content were observed. When raised on the standard food, the selected flies showed the same egg‐to‐adult viability and the same resistance to larval heat and cold shock as the controls and a slightly shorter developmental time. However, despite only 4% shorter development time, the adults of selected populations raised on the standard food were 13% smaller and showed 20% lower early‐life fecundity than the controls, with no differences in life span. The selected flies also turned out less tolerant to adult malnutrition. Thus, fruit flies have the genetic potential to adapt to poor larval food, with no detectable loss of larval performance on the standard food. However, adaptation to larval nutritional stress is associated with trade‐offs with adult fitness components, including adult tolerance to nutritional stress.     

Maternal effects increase survival probability in Drosophila subobscura larvae

Drosophilid flies breeding on ephemeral resource patches (e.g., decaying fruits) are assumed to transfer yeasts to their oviposition sites, presumably in order to positively affect offspring development. We tested this hypothesis with Drosophila subobscura Collin (Diptera: Drosophilidae) by manipulating their nutritional (yeast‐fed vs. non‐yeast‐fed) and reproductive status (mated vs. non‐mated). Flies were then released into vials containing decaying fruits (either sloes, crab apples, or Syrian plums). After a constant residence time in the vials, the flies were removed, 16 first‐instar larvae were transferred to the fruits and their survival probability to the adult stage was recorded. Whereas previous exposure of the larval substrate to yeast‐fed males and virgin females (yeast‐fed and non‐yeast‐fed) had no effect on survivorship, exposure to yeast‐fed and mated females that deposited eggs on the fruits (subsequently removed) led to a significant increase in the survival probability of the transferred larvae to the adult stage. Although the exact mechanism of yeast transmission remains to be determined, we suggest an active inoculation of the breeding substrates with yeast by ovipositing females. In agreement with previous studies, we found a negative effect of mould growth on larval survival, which, however, depended on the fruit type. We discuss various scenarios of yeast involvement in benefits to the insect larvae and suggest that insect–mould interactions should be examined in detail in order to better understand the behavioural and life‐history traits of insects that depend on ephemeral resources.     

Drosophila melanogaster larvae make nutritional choices that minimize developmental time

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.     

Impacts of diet quality on life‐history and reproductive traits in male and female armed beetle,Gnatocerus cornutus

1. The energy available for reproduction is usually limited by resource acquisition (i.e. condition). Because condition is known to be strongly affected by environmental factors, reproductive investments also vary across heterogeneous environments. 2. Although the condition dependence of reproductive investment is common to both sexes, reproductive traits may exhibit sexually different responses to environmental fluctuation due to sex‐specific life‐history strategies. However, few direct experimental studies have investigated the condition dependence of reproductive investments in both sexes. 3. We investigated the condition dependence of life‐history and reproductive traits of males and females in the beetle Gnatocerus cornutus Fabricus by manipulating larval and adult diet quality. We found that male and female life‐history traits exhibited similar responses to environmental fluctuations. 4. By contrast, the sexes exhibit different patterns of condition dependence in reproductive traits (i.e. the adult nutritional environment has a strong impact on the female lifetime reproductive success, whereas larval nutritional environment strongly affects the secondary sexual trait in males). 5. This difference in the plasticity of reproductive traits may lead to different selection pressures for each sex, even if both sexes develop and/or live in the same environment.     

The plastic fly: the effect of sustained fluctuations in adult food supply on life‐history traits

Many adult traits in Drosophila melanogaster show phenotypic plasticity, and the effects of diet on traits such as lifespan and reproduction are well explored. Although plasticity in response to food is still present in older flies, it is unknown how sustained environmental variation affects life‐history traits. Here, we explore how such life‐long fluctuations of food supply affect weight and survival in groups of flies and affect weight, survival and reproduction in individual flies. In both experiments, we kept adults on constant high or low food and compared these to flies that experienced fluctuations of food either once or twice a week. For these ‘yoyo’ groups, the initial food level and the duration of the dietary variation differed during adulthood, creating four ‘yoyo’ fly groups. In groups of flies, survival and weight were affected by adult food. However, for individuals, survival and reproduction, but not weight, were affected by adult food, indicating that single and group housing of female flies affects life‐history trajectories. Remarkably, both the manner and extent to which life‐history traits varied in relation to food depended on whether flies initially experienced high or low food after eclosion. We therefore conclude that the expression of life‐history traits in adult life is affected not only by adult plasticity, but also by early adult life experiences. This is an important but often overlooked factor in studies of life‐history evolution and may explain variation in life‐history experiments.     

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

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.     

Effects of resource variation during early life and adult social environment on contest outcomes in burying beetles: a context-dependent silver spoon strategy?

Good early nutritional conditions may confer a lasting fitness advantage over individuals suffering poor early conditions (a ‘silver spoon’ effect). Alternatively, if early conditions predict the likely adult environment, adaptive plastic responses might maximize individual performance when developmental and adult conditions match (environmental-matching effect). Here, we test for silver spoon and environmental-matching effects by manipulating the early nutritional environment of Nicrophorus vespilloides burying beetles. We manipulated nutrition during two specific early developmental windows: the larval environment and the post-eclosion environment. We then tested contest success in relation to variation in adult social environmental quality experienced (defined according to whether contest opponents were smaller (good environment) or larger (poor environment) than the focal individual). Variation in the larval environment influenced adult body size but not contest success per se for a given adult social environment experienced (an ‘indirect’ silver spoon effect). Variation in post-eclosion environment affected contest success dependent on the quality of the adult environment experienced (a context-dependent ‘direct’ silver spoon effect). By contrast, there was no evidence for environmental-matching. The results demonstrate the importance of social environmental context in determining how variation in nutrition in early life affects success as an adult.     

Effects of food variability on growth and reproduction of Aedes aegypti

Despite a large body of knowledge about the evolution of life histories, we know little about how variable food availability during an individual's development affects its life history. We measured the effects of manipulating food levels during early and late larval development of the mosquito Aedes aegypti on its growth rate, life history and reproductive success. Switching from low to high food led to compensatory growth: individuals grew more rapidly during late larval development and emerged at a size close to that of mosquitoes consistently reared at high food. However, switching to high food had very little effect on longevity, and fecundity and reproductive success were considerably lower than in consistently well‐fed mosquitoes. Changing from high to low food led to adults with similar size as in consistently badly nourished mosquitoes, but even lower fecundity and reproductive success. A rapid response of growth to changing resources can thus have unexpected effects in later life and in lifetime reproductive success. More generally, our study emphasizes the importance of varying developmental conditions for the evolutionary pressures underlying life‐history evolution.     

Effects of larval density and food stress on life‐history traits of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae)

High population density and nutrition restriction can lead to phase variation in morphology and development, and subsequently induce changes in the reaction norms of adult flight in migrant insects. However, response of migratory propensity to such stress in Endopterygote insects, especially in several species of Lepidoptera, remains unclear. In this study, larval and adult developmental responses to crowding and food stress were investigated in the migratory moth, Cnaphalocrocis medinalis (Guenée). A high larval rearing density significantly reduced pupal mass, survival rate and female fecundity. Larvae developed rapidly under crowding conditions, and time to pupation was 2 days earlier than individuals reared alone. By contrast, short‐term starvation and associated compensatory growth prolonged larval duration by 3–4 days and pupal duration by 1–2 days. It also reduced the pupal mass, but showed no detectable effects on female reproductive performance. Both sexes had similar development strategies; however, females seemed to be more sensitive to crowding and food shortage than males. A positive effect was expected if such stress factors acted as cues that triggering a behavioural or physiological shift to a distinct migratory phase. To the contrary, we found no proof that crowding and starvation caused maturation delay in female reproductive development. All treatments did not significantly increase female pre‐oviposition period. Therefore, we concluded that life developmental responses to crowding and food shortage in this species were different. Adult migration propensity was not enhanced under such stress conditions during the larval phase.     

Sex differences in nutrient intake can reduce the potential for sexual conflict over fitness maximization by female and male crickets

As females and males have different roles in reproduction, they are expected to require different nutrients for the expression of reproductive traits. However, due to their shared genome, both sexes may be constrained in the regulation of nutrient intake that maximizes sex‐specific fitness. Here, we used the Geometric Framework for nutrition to examine the effect of macronutrient and micronutrient intakes on lifespan, fecundity and cuticular hydrocarbons (CHCs) that signal mate quality to prospective mates in female field crickets, Teleogryllus oceanicus. In addition, we contrasted nutritional effects on life‐history traits between males and females to determine how sex differences influence nutrient regulation. We found that carbohydrate intake maximized female lifespan and protein intake influenced CHC expression, while early life fecundity (cumulative fecundity at day 21) and lifetime fecundity were dependent on both macronutrient and micronutrient intakes. Fecundity required different nutrient blends to those required to optimize sperm viability in males, generating the potential for sexual conflict over macronutrient intake. The regulation of protein (P) and carbohydrate (C) intakes by virgin and mated females initially matched that of males, but females adjusted their intake to a higher P:C ratio, 1P:2C, that maximized fecundity as they aged. This suggests that a sex‐specific, age‐dependent change in intake target for sexually mature females, regardless of their mating status, adjusts protein consumption in preparation for oviposition. Sex differences in the regulation of nutrient intake to optimize critical reproductive traits in female and male T. oceanicus provide an example of how sexual conflict over nutrition can shape differences in foraging between the sexes.     

Changes in genetic architecture during relaxation in Drosophila melanogaster selected on divergent virgin life span

Artificial selection experiments often confer important information on the genetic correlations constraining the evolution of life history. After artificial selection has ceased however, selection pressures in the culture environment can change the correlation matrix again. Here, we reinvestigate direct and correlated responses in a set of lines of Drosophila melanogaster that were selected on virgin life span and for which selection has been relaxed for 10 years. The decrease in progeny production in long-lived lines, a strong indication of antagonistic pleiotropy, had disappeared during relaxation. This was associated with a higher cost of reproduction to long-lived flies in mated, but not in virgin life span. These data strongly suggest that genetic mechanisms of mated and virgin life span determination are partly independent. Furthermore, data on body weight, developmental time and viability indicated deleterious effects of longevity selection in either direction, giving rise to a nonlinear relationship with life span for these characters. In order to reclaim original patterns, we founded a new set of derived lines by resuming selection in mixed replicate lines of the original set. Although selection was successful, most patterns in correlated characters remained, showing that these new patterns are resistant to new episodes of selection.     

Sexual development of wild and mass‐reared male Queensland fruit flies in response to natural food sources

Diet has a profound influence on the fitness of adult tephritid flies. Mass‐reared flies are provided yeast hydrolysate as a rich source of nutrition that supports rapid sexual development and mating success. In contrast, wild tephritid flies often live in environments where food may be hard to find, and these are the conditions that sexually immature mass‐reared sterile males encounter when released into the field during sterile insect technique campaigns. The effect of natural food sources (bat guano, bird droppings, citrus pollen, and wheat pollen) on the sexual development of adult mass‐reared fertile, mass‐reared sterile, and wild male Queensland fruit flies, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), was determined by measuring ejaculatory apodeme size. Inclusion of yeast hydrolysate in the adult diet was associated with faster growth of the ejaculatory apodeme in comparison with all other diets. Effects of diet were far less pronounced in mass‐reared males, which may indicate reduced nutritional requirements, whereas the ejaculatory apodeme of wild males fed on natural sources of food or sucrose alone did not increase in size over the first 20 days of adult life.     

Poor Nutritional Conditions During the Early Larval Stage Reduce Risk‐Taking Activities of Fire Salamander Larvae (Salamandra salamandra)

Environmental conditions experienced early in life have been shown to significantly affect growth trajectories at later stages in many vertebrate species. Amphibians typically have a biphasic life history, with an aquatic larval phase during early development and a subsequent terrestrial adult phase after completed metamorphosis. Thus, the early conditions have an especially strong impact on the future survival and fitness of amphibians. We studied whether early nutritional conditions affect the behavioural reaction of fire salamander larvae (Salamandra salamandra) before completion of metamorphosis. Fire salamander larvae reared under rich nutritional conditions were heavier and larger, displayed better body condition overall throughout the first three month of life and metamorphosed earlier compared with larvae raised under poor nutritional conditions. Specifically, we tested whether larvae reared under these different conditions differed with respect to their risk‐taking behaviour and activity. We found no differences in the activity of larvae with respect to their experienced early food conditions. However, larvae reared under poor nutritional conditions hid significantly more often in a risk‐taking test than larvae reared under rich food conditions. This increase in shelter‐seeking behaviour might be an adaptation to reduce the risk of larval drift or an adaptation to compensate for physiological deficits in part by appropriate behavioural reactions. Our results indicate that environmental conditions, such as food availability, may lead to different behavioural strategies.     

The effects of larval nutrition on reproductive performance in a food-limited adult environment

It is often assumed that larval food stress reduces lifetime fitness regardless of the conditions subsequently faced by adults. However, according to the environment-matching hypothesis, a plastic developmental response to poor nutrition results in an adult phenotype that is better adapted to restricted food conditions than one having developed in high food conditions. Such a strategy might evolve when current conditions are a reliable predictor of future conditions. To test this hypothesis, we assessed the effects of larval food conditions (low, improving and high food) on reproductive fitness in both low and high food adults environments. Contrary to this hypothesis, we found no evidence that food restriction in larval ladybird beetles produced adults that were better suited to continuing food stress. In fact, reproductive rate was invariably lower in females that were reared at low food, regardless of whether adults were well fed or food stressed. Juveniles that encountered improving conditions during the larval stage compensated for delayed growth by accelerating subsequent growth, and thus showed no evidence of a reduced reproductive rate. However, these same individuals lost more mass during the period of starvation in adults, which indicates that accelerated growth results in an increased risk of starvation during subsequent periods of food stress.     

Sex‐specific compensatory growth in the larvae of the greater wax moth Galleria mellonella

Deficiency of food resources in ontogeny is known to prolong an organism's developmental time and affect body size in adulthood. Yet life‐history traits are plastic: an organism can increase its growth rate to compensate for a period of slow growth, a phenomenon known as ‘compensatory growth’. We tested whether larvae of the greater wax moth Galleria mellonella can accelerate their growth after a fast of 12, 24 or 72 h. We found that a subgroup of female larvae showed compensatory growth when starved for 12 h. Food deficiency lasting more than 12 h resulted in longer development and lower mass gain. Strength of encapsulation reactions against a foreign body inserted in haemocoel was the weakest in females that showed compensatory growth, whereas the strongest encapsulation was recorded in the males and females that fasted for 24 and 72 h. More specifically, we found sex‐biased immune reactions so that females had stronger encapsulation rates than males in one group that fasted for 72 h. Overall, rapidly growing females had a short larval development period and the shortest adult lifespan. These results suggest that highly dynamic trade‐offs between the environment, life‐history traits and sex lead to plasticity in developmental strategies/growth rates in the greater wax moth.     

Energy beyond the pupal stage: larval nutrition and its long-time consequences for male mating performance in a scorpionfly

The basic requirement for selection to take effect is variation in fitness relevant traits among individuals of a population. This study is concerned with the question whether environmental conditions met during an early phase of life history that is dominated by the natural component of selection will affect traits and behaviour in a sexual selection context after metamorphosis in a holometabolous insect species. We examined the effects of nutrition as a proximate factor responsible for intrasexual phenotypic variation in the mating performance of male Panorpa vulgaris (Mecoptera: Panorpidae). For this purpose, we manipulated food availability during larval development as well as during adulthood. To obtain matings and to increase their reproductive success males must secrete salivary masses which are then consumed by the females during copulation. The results of the present study are consistent with those of previous studies demonstrating a strong effect of nutrition during adulthood on various fitness relevant traits (salivary gland development, saliva investment in copulations, etc.). But moreover, we could show that food availability during larval development affected male body weight and that there was an interaction between larval and adult diet affecting salivary gland weight relative to body weight. Therefore, food availability during the larval stage can become an important and limiting factor for salivary gland development (and mating success) depending on food availability during adulthood. Several other variables (number of salivary masses, copulation duration, salivary mass weight and saliva investment) seemed not to be associated with larval nutrition.     

Chronic malnutrition favours smaller critical size for metamorphosis initiation in Drosophila melanogaster

Critical size at which metamorphosis is initiated represents an important checkpoint in insect development. Here, we use experimental evolution in Drosophila melanogaster to test the long-standing hypothesis that larval malnutrition should favour a smaller critical size. We report that six fly populations subject to 112 generations of laboratory natural selection on an extremely poor larval food evolved an 18% smaller critical size (compared to six unselected control populations). Thus, even though critical size is not plastic with respect to nutrition, smaller critical size can evolve as an adaptation to nutritional stress. We also demonstrate that this reduction in critical size (rather than differences in growth rate) mediates a trade-off in body weight that the selected populations experience on standard food, on which they show a 15-17% smaller adult body weight. This illustrates how developmental mechanisms that control life history may shape constraints and trade-offs in life history evolution.     

Yeast hydrolysate supplement increases starvation vulnerability of Queensland fruit fly

Post‐teneral diets containing yeast hydrolysate are reported to increase longevity, reproductive development and sexual performance of Queensland fruit fly (‘Q‐fly’) Bactrocera tryoni Froggatt (Diptera: Tephritidae). Consequently, diets including yeast hydrolysate are recommended for sterile Q‐flies before release in sterile insect technique (SIT) programmes. However, in some tephritids, diets including yeast hydrolysate are associated with an increased vulnerability to starvation. In the present study, the effects of yeast hydrolysate supplementation before release are considered with respect to the longevity of released Q‐fly when food becomes scarce. Experiments are carried out in three settings of varying resemblance to field conditions: 5‐L laboratory cages, 107‐L outdoor cages and 14 140‐L field cages containing potted citrus trees. In all experimental settings, compared with flies that received only sucrose, male and female Q‐flies that are provided with yeast hydrolysate during the first 2 days of adult life have a significantly shorter survival when subsequently deprived of food. Yeast supplementation appears to commit Q‐flies to a developmental trajectory that renders them more vulnerable to starvation. The practical significance of these findings for SIT depends on how often the releases are carried out under conditions in which Q‐flies experience extreme food shortages in the field.     

A survival cost to mating in a polyandrous butterfly, Colias eurytheme

Adaptations that enhance fitness in one sex may be harmful to members of the opposite sex and lead to antagonistic coevolution between the sexes. In fruit flies, for example, selection for fertilization success has rendered the male ejaculate slightly toxic to females. Here we investigated whether mating imposes a cost upon female fitness in a polyandrous pierid butterfly ( Colias eurytheme ) by comparing life history traits between once-mated females and virgins. Mated females laid relatively more eggs early in their adult life, but suffered a reduction in longevity relative to virgins held under identical experimental conditions. The effect of mating on female survivorship was statistically independent of lifetime and early life fecundity. Moreover, lifetime fecundity co-varied positively with longevity across all females, and across females within each treatment group, hence there was no phenotypic trade-off between survival and reproduction. These results suggest that the observed longevity difference between virgin and mated females represents a true cost of mating, possibly arising from a toxic side effect of the male ejaculate. However, irrespective of this cost, virgin and mated females laid an equivalent lifetime number of eggs. Female C. eurytheme are also known to use nutrients from the male ejaculate to supplement their reproductive output, hence it is presently unclear how the observed longevity cost may have influenced the evolution of lifetime mating schedules in this polyandrous species.