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.     

The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster

Both developmental nutrition and adult nutrition affect life‐history traits; however, little is known about whether the effect of developmental nutrition depends on the adult environment experienced. We used the fruit fly to determine whether life‐history traits, particularly life span and fecundity, are affected by developmental nutrition, and whether this depends on the extent to which the adult environment allows females to realize their full reproductive potential. We raised flies on three different developmental food levels containing increasing amounts of yeast and sugar: poor, control, and rich. We found that development on poor or rich larval food resulted in several life‐history phenotypes indicative of suboptimal conditions, including increased developmental time, and, for poor food, decreased adult weight. However, development on poor larval food actually increased adult virgin life span. In addition, we manipulated the reproductive potential of the adult environment by adding yeast or yeast and a male. This manipulation interacted with larval food to determine adult fecundity. Specifically, under two adult conditions, flies raised on poor larval food had higher reproduction at certain ages – when singly mated this occurred early in life and when continuously mated with yeast this occurred during midlife. We show that poor larval food is not necessarily detrimental to key adult life‐history traits, but does exert an adult environment‐dependent effect, especially by affecting virgin life span and altering adult patterns of reproductive investment. Our findings are relevant because (1) they may explain differences between published studies on nutritional effects on life‐history traits; (2) they indicate that optimal nutritional conditions are likely to be different for larvae and adults, potentially reflecting evolutionary history; and (3) they urge for the incorporation of developmental nutritional conditions into the central life‐history concept of resource acquisition and allocation.     

Contribution of maternal effects to dietary selection in Mediterranean fruit flies

Individual responses to dietary variation represent a fundamental component of fitness, and nutritional adaptation can occur over just a few generations. Maternal effects can show marked proximate responses to nutrition, but whether they contribute to longer term dietary adaptation is unclear. Here, we tested the hypotheses that maternal effects: (i) contribute to dietary adaptation, (ii) diminish when dietary conditions are constant between generations, (iii) are trait‐specific and (iv) interact with high‐ and low‐quality food. We used experimental evolution regimes in the medfly (Ceratitis capitata) to test these predictions by subjecting an outbred laboratory‐adapted population to replicated experimental evolution on either constant high calorie sugar (‘A’) or low‐calorie starch (‘S’) larval diets, with a standard adult diet across both regimes. We measured the contribution of maternal effects by comparing developmental and adult phenotypes of individuals reared on their own diet with those swapped onto the opposite diet for either one or two generations (high and low maternal effect conditions, respectively), both at the start and after 30 generations of selection. Initially, there were strong maternal effects on female body mass and male mating success but not larval survival. Interestingly, the initial maternal effects observed in female body mass and male mating success showed sex‐specific interactions when individuals from high calorie regimes were tested on low calorie diets. However, as populations responded to selection, the effects of maternal provisioning on all traits diminished. The results broadly supported the predictions. They show how the contribution of maternal effects to dietary responses evolves in a context‐dependent manner, with significant variation across different fitness‐related traits. We conclude that maternal effects can evolve during nutritional adaptation and hence may be an important life history trait to measure, rather than to routinely minimize.     

Antagonistic, stage-specific selection on defensive chemical sequestration in a toxic butterfly

Larvae of the pipevine swallowtail ( Battus philenor ) sequester toxic alkaloids called aristolochic acids from their Aristolochia host plants, rendering both larvae and adults chemically defended against most predators. Using a chemically controlled artificial diet, we observed substantial among-family variation in sequestration ability and larval developmental rate in a population occurring in central Texas. Early instar larvae from families that sequester greater amounts of aristolochic acid showed increased survivorship in a field experiment in which cohorts from each family were exposed to natural predators, whereas among-family variation in growth rate did not predict survivorship. Conversely, the aristolochic acid content of adult butterflies was negatively correlated with adult fat content, a fitness correlate. Sequestration ability positively affects the probability of larval survivorship, but at the cost of adult fat content. The costs and benefits of aristolochic acid sequestration vary during the course of the butterfly's development, and these antagonistic selection pressures may explain why variation in sequestration ability persists in wild populations.     

Interactions between ecological factors in the developmental environment modulate pupal and adult traits in a polyphagous fly

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Larval and nurse worker control of developmental plasticity and the evolution of honey bee queen-worker dimorphism

Social evolution in honey bees has produced strong queen-worker dimorphism for plastic traits that depend on larval nutrition. The honey bee developmental programme includes both larval components that determine plastic growth responses to larval nutrition and nurse components that regulate larval nutrition. We studied how these two components contribute to variation in worker and queen body size and ovary size for two pairs of honey bee lineages that show similar differences in worker body-ovary size allometry but have diverged over different evolutionary timescales. Our results indicate that the lineages have diverged for both nurse and larval developmental components, that rapid changes in worker body-ovary size allometry may disrupt queen development and that queen-worker dimorphism arises mainly from discrete nurse-provided nutritional environments, not from a developmental switch that converts variable nutritional environments into discrete phenotypes. Both larval and nurse components have likely contributed to the evolution of queen-worker dimorphism.     

Effects of nutrition and density in Culex pipiens

Mosquito larvae face numerous biotic and abiotic challenges that affect their development and survivorship, as well as adult fitness. We conducted two experiments under semi‐natural conditions to evaluate the effects of intraspecific competition, nutrient limitation and sub‐lethal doses of malathion on individual life history traits in adult Culex pipiens (Diptera: Culicidae). In the first experiment, larvae of Cx. pipiens were reared at different intraspecific densities and exposed to sub‐lethal doses of malathion. In the second experiment, different intraspecific densities of Cx. pipiens larvae were reared under conditions of low or high larval nutrients, and subsequent adults were fed on either water or 10% sucrose solution. Malathion treatment had relatively minor effects compared with density, which had significant negative effects on development rate, survivorship to adulthood, body size (wing length) and longevity. As larval density increased, a sex ratio distortion in survivorship to adulthood emerged, in which a bias towards males was apparent. Nutrient‐rich larval environments alleviated, in part, the effects of increasing density and extended the lifespan of mosquitoes fed on water and 10% sucrose. Density‐dependent alterations in adult longevity attributable to the larval environment are complex and show contrasting results depending on interactions with other environmental factors. This study suggests that larval resource availability and competition influence Cx. pipiens population growth correlates and have lasting effects on traits that relate to a mosquito's ability to vector pathogens.     

Development time mediates the effect of larval diet on ageing and mating success of male antler flies in the wild

High-quality developmental environments often improve individual performance into adulthood, but allocating toward early life traits, such as growth, development rate and reproduction, may lead to trade-offs with late-life performance. It is, therefore, uncertain how a rich developmental environment will affect the ageing process (senescence), particularly in wild insects. To investigate the effects of early life environmental quality on insect life-history traits, including senescence, we reared larval antler flies (Protopiophila litigata) on four diets of varying nutrient concentration, then recorded survival and mating success of adult males released in the wild. Declining diet quality was associated with slower development, but had no effect on other life-history traits once development time was accounted for. Fast-developing males were larger and lived longer, but experienced more rapid senescence in survival and lower average mating rate compared to slow developers. Ultimately, larval diet, development time and body size did not predict lifetime mating success. Thus, a rich environment led to a mixture of apparent benefits and costs, mediated by development time. Our results indicate that ‘silver spoon'' effects can be complex and that development time mediates the response of adult life-history traits to early life environmental quality.     

Carryover effects of larval environment on individual variation in a facultatively diadromous fish

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Diet and a developmental time constraint alter life‐history trade‐offs in a caddis fly (Trichoptera: Limnephilidae)

Environmental factors influence variation in life histories by affecting growth, development, and reproduction. We conducted an experiment in outdoor mesocosms to examine how diet and a time constraint on juvenile development (pond‐drying) influence life‐history trade‐offs (growth, development, adult body mass) in the caddis fly Limnephilus externus (Trichoptera: Limnephilidae). We predicted that: (1) diet supplementation would accelerate larval growth and development, and enhance survival to adulthood; (2) pond‐drying would accelerate development and increase larval mortality; and (3) the relationship between adult mass and age at maturity would be negative. Diet supplementation did lead to larger adult mass under nondrying conditions, but did not significantly alter growth or development rates. Contrary to predictions, pond‐drying reduced growth rates and delayed development. The slope (positive or negative) of the female mass–age at maturity relationship depended on interactions with diet or pond‐drying, but the male mass–age relationship was negative and independent of treatment. Our results suggest that pond‐drying can have negative effects on the future fitness of individuals by increasing the risk of desiccation‐induced, pre‐reproductive mortality and decreasing adult body size at maturity. These negative effects on life history cannot be overcome with additional nutritional resources in this species. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 495–504.     

Effects of larval energetic resources on life history and adult allocation patterns in a caddisfly (Trichoptera: Phryganeidae)

Abstract 1. How populations respond to environmental change depends, in part, on the connection between environmental variance during early life stages and its effect on subsequent life‐history traits. For example, environmental variation during the larval stage can influence the life histories of organisms with complex life cycles by altering the amount of time spent in each stage of the life cycle as well as by altering allocation to life‐history traits during metamorphosis. 2. The effects of larval energetic resources on developmental timing, adult mass, fecundity, mating success, and allocation to adult body structures (thorax, abdomen, wings) were examined in an aquatic caddisfly (Agrypnia deflata Milne, Trichoptera: Phryganeidae). Larval energetic reserves were manipulated by removing larval cases just prior to pupation. In the first experiment, cases of all individuals were removed just prior to pupation; experimental individuals were required to build a new case whereas control individuals were allowed to re‐enter their case without building. In the second experiment, energy differences were maximised between the two treatments by supplementing the larval diet of the control group and removing cases and not supplementing the diet of the experimental group. 3. Male and female development time, adult mass, and female fecundity were not influenced by case removal or diet supplementation. In contrast, allocation to adult body parts indicated a trade‐off between abdominal and thoracic mass among case‐removal females, suggesting that, under larval resource stress, females adjust resource allocation during metamorphosis to alleviate potential negative impacts on clutch size. In addition, latency to copulation increased when cases were removed, indicating larval resource stress could influence male mating success. 4. This study suggests that, under larval energetic stress, the negative impacts on female reproduction might be mitigated by re‐allocating resources during metamorphosis, whereas male allocation strategies might not be as flexible as female strategies.     

ECOLOGICAL HISTORY AND EVOLUTION IN A NOVEL ENVIRONMENT: HABITAT HETEROGENEITY AND INSECT ADAPTATION TO A NEW HOST PLANT

Environmental heterogeneity has often been implicated in the maintenance of genetic variation. However, previous research has not considered how environmental heterogeneity might affect the rate of adaptation to a novel environment. In this study, I used an insect-plant system to test the hypothesis that heterogeneous environments maintain more genetic variation in fitness components in a novel environment than do uniform environments. To manipulate recent ecological history, replicate populations of the dipteran leafminer Liriomyza trifolii were maintained for 20 generations in one of three treatments: a heterogeneous environment that contained five species of host plant, and two uniform environments that contained either a susceptible chrysanthemum or tomato. The hypothesis that greater genetic variance for survivorship and developmental time on a new host plant (a leafminer-resistant chrysanthemum) would be maintained in the heterogeneous treatment relative to the uniform environments was then tested with a sib-analysis and a natural selection experiment. Populations from the heterogeneous host plant treatment had no greater genetic variance in either larval survivorship or developmental time on the new host than did populations from either of the other treatments. Moreover, the rate of adaptation to the new host did not differ between the ecological history treatments, although the populations from the uniform chrysanthemum treatment had higher mean survivorship throughout the selection experiment. The estimates of the heritability of larval survivorship from the sib-analysis and selection experiment were quite similar. These results imply that ecologically realistic levels of environmental heterogeneity will not necessarily maintain more genetic variance than uniform environments when traits expressed in a particular novel environment are considered.     

Adult beetles compensate for poor larval food conditions

Life history traits of herbivores are highly influenced by the quality of their hosts, i.e., the composition of primary and secondary plant metabolites. In holometabolous insects, larvae and adults may face different host plants, which differ in quality. It has been hypothesised that adult fitness is either highest when larval and adult environmental conditions match (environmental matching) or it may be mainly determined by optimal larval conditions (silver spoon effect). Alternatively, the adult stage may be most decisive for the actual fitness, independent of larval food exposure, due to adult compensation ability. To determine the influence of constant versus changing larval and adult host plant experiences on growth performance, fitness and feeding preferences, we carried out a match–mismatch experiment using the mustard leaf beetle, Phaedon cochleariae. Larvae and adults were either constantly reared on watercress (natural host) or cabbage (crop plant) or were switched after metamorphosis to the other host. Growth, reproductive traits and feeding preferences were determined repeatedly over lifetime and host plant quality traits analysed. Differences in the host quality led to differences in the development time and female reproduction. Egg numbers were significantly influenced by the host plant species experienced by the adults. Thus, adults were able to compensate for poor larval conditions. Likewise, the current host experience was most decisive for feeding preferences; in adult beetles a feeding preference was shaped regardless of the larval host plant. Larvae or adults reared on the more nutritious host, cabbage, showed a higher preference for this host. Hence, beetles most likely develop a preference when gaining a direct positive feedback in terms of an improved performance, whereby the current experience matters the most. Highly nutritious crop plants may be, in consequence, all the more exploited by potential pests that may show a high plasticity in reproduction and feeding preferences.     

Genetic and nutritional effects on male traits and reproductive performance in Tribolium flour beetles

In Tribolium flour beetles and other organisms, individuals migrate between heterogeneous environments where they often encounter markedly different nutritional conditions. Under these circumstances, theory suggests that genotype-by-environment interactions (GEI) may be important in facilitating adaptation to new environments and maintaining genetic variation for male traits subject to directional selection. Here, we used a nested half-sib breeding design with Tribolium castaneum to partition the separate and joint effects of male genotype and nutritional environment on phenotypic variation in a comprehensive suite of life-history traits, reproductive performance measures across three sequential sexual selection episodes, and fitness. When male genotypes were tested across three nutritional environments, considerable phenotypic plasticity was found for male mating and insemination success, longevity and traits related to larval development. Our results also revealed significant additive genetic variation for male mating rate, sperm offence ability (P(2)), longevity and total fitness and for several traits reflecting both larval and adult resource use. In addition, we found evidence supporting GEI for sperm defence ability (P(1)), adult longevity and larval development; thus, no single male genotype outperforms others in every nutritional environment. These results provide insight into the potential roles of phenotypic plasticity and GEI in facilitating Tribolium adaptation to new environments in ecological and evolutionary time.     

Life‐history trade‐offs under different larval diets in Drosophila suzukii (Diptera: Drosophilidae)

Most larval drosophilids eat the microorganisms that develop in rotting fruit, a relatively protein‐rich resource. By contrast, the spotted‐wing Drosophila suzukii Matsumara (Diptera: Drosophilidae) uniquely develops in ripening fruit, a protein‐poor, carbohydrate‐rich resource. This shift in larval nutritional niche has led to D. suzukii being a significant agricultural pest in the U.S.A. and Europe. Although occupying a new niche may benefit a species by reducing competition, adaptation in host use may generate trade‐offs affecting fitness. To test the hypothesis that fitness trade‐offs will change with adaptation to novel larval diets, D. suzukii larval development on either a diet of a fresh, ripe blueberry (a natural host) or standard artificial Drosophila media (protein‐rich) is compared and the effect of diet on development time from egg to adult, adult body size and male wing spot area, and female fecundity is assessed. Larval development time differs, with larvae on the blueberry emerging as adults earlier than those on the artificial medium, although other fitness measures do not vary between the two diets. In addition, the faster development time on a blueberry does not trade off with body size as expected, although early fecundity is delayed in females that develop on blueberries. Thus, adaptation to a novel larval diet environment does not come at a cost to the ability to develop in protein‐rich resources.     

Adaptation to divergent larval diets in the medfly,Ceratitis capitata

Variation in diet can influence the timing of major life‐history events and can drive population diversification and ultimately speciation. Proximate responses of life histories to diet have been well studied. However, there are scant experimental data on how organisms adapt to divergent diets over the longer term. We focused on this omission by testing the responses of a global pest, the Mediterranean fruitfly, to divergent selection on larval diets of different nutritional profiles. Tests conducted before and after 30 generations of nutritional selection revealed a complex interplay between the effects of novel larval dietary conditions on both plastic and evolved responses. There were proximate‐only responses to the larval diet in adult male courtship and the frequency of copulation. Males on higher calorie larval diets consistently engaged in more bouts of energetic courtship. In contrast, following selection, larval development time, and egg to adult survival showed evidence of evolved divergence between diet regimes. Adult body size showed evidence for adaptation, with flies being significantly heavier when reared on their “own” diet. The results show the multifaceted responses of individuals to dietary selection and are important in understanding the extreme generalism exhibited by the medfly.     

Temperature‐by‐nutrient interactions affecting growth rate in an insect ectotherm

Temperature and nutrition are two prominent environmental variables influencing juvenile growth rate in ectotherms. These two factors interact in complex ways. Here, we present a comprehensive analysis of the interactive effects of temperature and nutrition on various components of fitness (growth rate, survival), food intake, and level of energy storage in an insect herbivore, caterpillars of Spodoptera exigua Hübner (Lepidoptera: Noctuidae). In a factorial experimental design, final‐instar caterpillars (i.e., fifth instars) were individually reared at one of three constant temperatures (18, 26, and 34 °C), in which they received one of six diets differing in their ratio of protein and digestible carbohydrate [P:C mixture, expressed as the percentage of diet by dry mass: protein 42%:carbohydrate 0% (42:0), 35:7, 28:14, 21:21, 14:28, and 7:35]. Within the range of test temperatures, larval growth rate increased with rising temperature and was strongly affected by P:C mixture, reaching a maximum on moderate P:C diets at each temperature and falling at very high and low P:C mixtures. There was a significant temperature*diet interaction, such that the difference in growth rates between temperatures was greatest on moderate P:C diets and least on the most extreme diets (42:0 and 7:35). Food intake rate patterns followed a similar trend to growth rate. Rapidly growing animals at high ambient temperature suffered high mortality across all dietary P:C mixtures, but to a greater extent on the extremely unbalanced diets. This suggests that there are developmental and physiological costs associated with fast growth at high temperature, as indicated by high rate of pupation failure and reduced lipid storage efficiency. Our study shows how temperature and nutrition interplay to mediate phenotypic variations in growth rates and energy utilization in an insect ectotherm.     

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.     

Estimation of fitness from energetics and life‐history data: An example using mussels

Changing environments have the potential to alter the fitness of organisms through effects on components of fitness such as energy acquisition, metabolic cost, growth rate, survivorship, and reproductive output. Organisms, on the other hand, can alter aspects of their physiology and life histories through phenotypic plasticity as well as through genetic change in populations (selection). Researchers examining the effects of environmental variables frequently concentrate on individual components of fitness, although methods exist to combine these into a population level estimate of average fitness, as the per capita rate of population growth for a set of identical individuals with a particular set of traits. Recent advances in energetic modeling have provided excellent data on energy intake and costs leading to growth, reproduction, and other life‐history parameters; these in turn have consequences for survivorship at all life‐history stages, and thus for fitness. Components of fitness alone (performance measures) are useful in determining organism response to changing conditions, but are often not good predictors of fitness; they can differ in both form and magnitude, as demonstrated in our model. Here, we combine an energetics model for growth and allocation with a matrix model that calculates population growth rate for a group of individuals with a particular set of traits. We use intertidal mussels as an example, because data exist for some of the important energetic and life‐history parameters, and because there is a hypothesized energetic trade‐off between byssus production (affecting survivorship), and energy used for growth and reproduction. The model shows exactly how strong this trade‐off is in terms of overall fitness, and it illustrates conditions where fitness components are good predictors of actual fitness, and cases where they are not. In addition, the model is used to examine the effects of environmental change on this trade‐off and on both fitness and on individual fitness components.