Adult Starvation Resistance Research Articles

Starvation selection reduces and delays larval ecdysone production and signaling.

Previous studies have shown that selection for starvation resistance in Drosophila melanogaster results in delayed eclosion and increased adult fat stores. It is assumed that these traits are caused by the starvation selection pressure, but its mechanism is unknown. We found that our starvation-selected (SS) population stores more fat during larval development and has extended larval development and pupal development time. Developmental checkpoints in the third instar associated with ecdysteroid hormone pulses are increasingly delayed. The delay in the late larval period seen in the SS population is indicative of reduced and delayed ecdysone signaling. An enzyme immunoassay for ecdysteroids (with greatest affinity to the metabolically active 20-hydroxyecdysone and the α-ecdysone precursor) confirmed that the SS population had reduced and delayed hormone production compared with that of fed control (FC) flies. Feeding third instar larvae on food supplemented with α-ecdysone partially rescued the developmental delay and reduced subsequent adult starvation resistance. This work suggests that starvation selection causes reduced and delayed production of ecdysteroids in the larval stage and affects the developmental delay phenotype that contributes to subsequent adult fat storage and starvation resistance.

Nutritional phenotype underlines the performance trade-offs of Drosophila suzukii on different fruit diets

Animals confined to different dietary conditions often exhibit distinct, sometimes contrasting, nutritional phenotypes and performance outcomes. This is especially true for many oviparous insects whose developmental diets can vary depending on the mother's egg-laying site selection. Much research on the relationship between preference and performance in insects has focused on larval success, which overlooks the complexities of dietary effects on diverse performance parameters across life stages and potential trade-offs between those parameters. Furthermore, the connection between diet-induced nutritional phenotype and performance trade-offs is not well understood. Here, using Drosophila suzukii, we quantify multiple performance indices of larvae and adults reared on five host fruits of different protein-to-sugar ratios (P:S) which have previously been shown to differ in attractiveness to fly foraging and oviposition. Our results demonstrate robust diet-specific performance trade-offs, with fly fecundity, larval development time, pupal size, and adult weight superior in flies reared on the high P:S raspberry diet, in contrast to the low P:S grape diet; but the reverse was found in terms of adult starvation resistance. Notably, the contrasting performance trade-offs are readily explained by the fly nutritional phenotype, reflected in the protein and energy (glucose and lipid) contents of flies reared on the two fruits. Together, our results provide experimental evidence for metabolic plasticity of D. suzukii reared on different fruits and the possibility of using adult nutritional phenotype as a marker for diet and performance outcomes.

Activation of innate immunity during development induces unresolved dysbiotic inflammatory gut and shortens lifespan.

ABSTRACTAn early-life inflammatory response is associated with risks of age-related pathologies. How transient immune signalling activity during animal development influences life-long fitness is not well understood. Using Drosophila as a model, we find that activation of innate immune pathway Immune deficiency (Imd) signalling in the developing larvae increases adult starvation resistance, decreases food intake and shortens organismal lifespan. Interestingly, lifespan is shortened by Imd activation in the larval gut and fat body, whereas starvation resistance and food intake are altered by that in neurons. The adult flies that developed with Imd activation show sustained Imd activity in the gut, despite complete tissue renewal during metamorphosis. The larval Imd activation increases an immunostimulative bacterial species, Gluconobacter sp., in the gut microbiome, and this dysbiosis is persistent to adulthood. Removal of gut microbiota by antibiotics in the adult fly mitigates intestinal immune activation and rescues the shortened lifespan. This study demonstrates that early-life immune activation triggers long-term physiological changes, highlighted as an irreversible alteration in gut microbiota, prolonged inflammatory intestine and concomitant shortening of the organismal lifespan.

The Genomic Architecture of Adaptation to Larval Malnutrition Points to a Trade-off with Adult Starvation Resistance in Drosophila.

Periods of nutrient shortage impose strong selection on animal populations. Experimental studies of genetic adaptation to nutrient shortage largely focus on resistance to acute starvation at adult stage; it is not clear how conclusions drawn from these studies extrapolate to other forms of nutritional stress. We studied the genomic signature of adaptation to chronic juvenile malnutrition in six populations of Drosophila melanogaster evolved for 150 generations on an extremely nutrient-poor larval diet. Comparison with control populations evolved on standard food revealed repeatable genomic differentiation between the two set of population, involving >3,000 candidate SNPs forming >100 independently evolving clusters. The candidate genomic regions were enriched in genes implicated in hormone, carbohydrate, and lipid metabolism, including some with known effects on fitness-related life-history traits. Rather than being close to fixation, a substantial fraction of candidate SNPs segregated at intermediate allele frequencies in all malnutrition-adapted populations. This, together with patterns of among-population variation in allele frequencies and estimates of Tajima’s D, suggests that the poor diet results in balancing selection on some genomic regions. Our candidate genes for tolerance to larval malnutrition showed a high overlap with genes previously implicated in acute starvation resistance. However, adaptation to larval malnutrition in our study was associated with reduced tolerance to acute adult starvation. Thus, rather than reflecting synergy, the shared genomic architecture appears to mediate an evolutionary trade-off between tolerances to these two forms of nutritional stress.

Testing the plant stress hypothesis: stressed plants offer better food to an insect herbivore

AbstractTemperature and nutrition are among the most important environmental factors affecting ectotherm growth. As temperature and host‐plant quality often co‐vary in nature, the interaction between the two is of potentially high ecological importance for herbivorous insects. We here use the temperate‐zone butterfly Pieris napi L. (Lepidoptera: Pieridae) to investigate interactive effects of larval rearing temperature and host‐plant quality (by manipulating water availability) on larval growth. As growth rates have been hypothesized to govern stress tolerance, we additionally assessed adult starvation resistance. Butterflies followed the ‘temperature‐size rule’, which states that body size increases at lower developmental temperatures, proximately caused by differences in growth increment, which resulted from increased consumption at the lower temperature. Larvae benefitted from feeding on stressed plants from the low‐water regime by having higher body mass, growth rate, and food conversion efficiency, thus supporting the plant stress hypothesis, which predicts that plant quality for herbivores should increase if stress is imposed on plants. Some effects of host‐plant quality on larval growth parameters were as strong as or even stronger than effects of temperature, whereas interactive effects between temperature and food quality were scarce. At the low temperature, adult starvation resistance was higher than at the higher temperature and females were more resistant than males, whereas plant water regime had no clear impact. No evidence was found for a trade‐off between growth rate and starvation resistance. This study illustrates the importance of considering effects of host‐plant quality along with variation in other environmental factors for estimating the impact of environmental changes on herbivorous species.

The costs of phenotypic adaptation to repeatedly fluctuating temperatures in a soil arthropod

Costs of phenotypic adaptation to changing environments have often been studied in morphological structures. Such structures typically are irreversible for at least some stage in the organism's life. In this study we investigated whether recurrent and reversible adaptation to changes in the thermal environment incurs a cost in terms of some key life-history traits in the collembolan Orchesella cincta. We exposed juvenile O. cincta to two treatments differing in the frequency of temperature fluctuation but with equal total temperature sums. In the high frequency treatment temperature fluctuated daily between 10 and 20 °C, while in the low frequency treatment temperature fluctuated on a weekly schedule. During the treatments we measured juvenile growth rate and juvenile mortality, and after six weeks the animals were transferred to constant 15 °C and adult starvation resistance was assessed. We found no significant differences between the treatments in juvenile growth rate or juvenile survival. Also, adults that had grown up under high frequency temperature fluctuations did not suffer from reduced starvation resistance compared to animals growing under low frequency temperature fluctuations. This finding supports the hypothesis that selection minimizes the production costs of inducible phenotypes and suggests that the development of optimal phenotypes and evolution of temperature reaction norms are not constrained by such costs.

Changed gene expression for candidate ageing genes in long-lived Bicyclus anynana butterflies

Candidate genes for the regulation of lifespan have emerged from studies that use mutants and genetically manipulated model organisms. However, it is rarely addressed whether these genes contribute to lifespan variation in populations of these species that capture natural standing genetic variation. Here, we explore expression variation in three candidate ageing genes, Indy, sod2, and catalase, in Bicyclus anynana, a butterfly with well understood ecology. We used lines established from natural populations and artificially selected for increased adult starvation resistance. They show a considerable increase in adult lifespan under both starvation and optimal food conditions. We measured adult butterflies of various ages, under a range of optimal and starvation diets, from two selected populations and one unselected control population. In all lines, Indy and catalase are up-regulated in response to starvation while this is not evident for sod2. Under starvation, Indy and catalase are up-regulated in, while this is not evident for sod2. Under optimal food conditions, Indy is down-regulated at a later age, with Indy expression showing relatively high inter-individual variation. We find differences between the selected lines and the unselected line. Under starvation conditions, expression is higher for catalase in one, and for sod2 in both selected lines. Importantly, sod2 expression is also higher in the selected populations under optimal food conditions. We conclude that sod2, but not Indy, is involved in the response to artificial selection for increased starvation resistance. The role of catalase is less clear because of the differences between the two selected lines. Moreover, sod2 appears to be a candidate gene that underpins the genetic correlation between starvation resistance and longevity. Our study indicates that some, but not all, genes identified through mutant screens in other organisms may underpin standing genetic variation for ageing-related traits in stocks of Bicyclus butterflies established from natural populations. Clearly, this needs to be investigated in other organisms as well, especially in the organisms to which mutants screens were applied. This information will narrow down the list of genes that underpin variation in lifespan and ageing in extant populations of organisms, and which may serve as candidate genes in humans.

Phenotypic plasticity of starvation resistance in the butterfly Bicyclus anynana

Starvation resistance is an important trait related to survival in many species and often involves dramatic changes in physiology and homeostasis. The tropical African butterfly Bicyclus anynana lives in two seasonal environments and has evolved phenotypic plasticity. The contrasting demands of the favourable, wet season and the harsh, dry season have shaped a remarkable life history, which makes this species particularly interesting for investigating the relationship between starvation resistance, metabolism, and its environmental modulation. This study reports on two laboratory experiments to investigate the effects of pre-adult and adult temperatures that mimic the seasonal environments, on starvation resistance and resting metabolic rate (RMR) in adult B. anynana. In addition, we investigate starvation resistance in wet and dry seasonal form genotypes; artificial selection on eyespot size has yielded lines that only produce one or the other of the seasonal forms across all rearing environments. As expected, the results show a large effect of adult temperature. More relevant, we show here that both pre-adult temperature and genetic background also influence adult starvation resistance, showing that phenotypic plasticity in this species includes starvation resistance. The dry season form genotype has a higher starvation resistance when developed at dry season temperatures, indicating a genetic modulation of starvation resistance in relation to temperature. Paradoxically, dry season pre-adult temperatures reduce starvation resistance and raise RMR. The high overall association of RMR and starvation resistance in our experiments suggests that energy expenditure and survival are linked, but that they may counteract each other in their influence on fitness in the dry season. We hypothesize that metabolism is moderating a trade-off between pre-adult (larval) survival and adult survival in the dry season.

Evolutionary domestication in Drosophila subobscura

The domestication of plants and animals is historically one of the most important topics in evolutionary biology. The evolutionary genetic changes arising from human cultivation are complex because of the effects of such varied processes as continuing natural selection, artificial selection, deliberate inbreeding, genetic drift and hybridization of different lineages. Despite the interest of domestication as an evolutionary process, few studies of multicellular sexual species have approached this topic using well-replicated experiments. Here we present a comprehensive study in which replicated evolutionary trajectories from several Drosophila subobscura populations provide a detailed view of the evolutionary dynamics of domestication in an outbreeding animal species. Our results show a clear evolutionary response in fecundity traits, but no clear pattern for adult starvation resistance and juvenile traits such as development time and viability. These results supply new perspectives on the confounding of adaptation with other evolutionary mechanisms in the process of domestication.

Wolbachia effects in Drosophila melanogaster: in search of fitness benefits

Insect endosymbionts often influence host nutrition but these effects have not been comprehensively investigated in Wolbachia endosymbionts that are widespread in insects. Using strains of Drosophila melanogaster with the wMel Wolbachia infection, we showed that Wolbachia did not influence adult starvation resistance. Wolbachia also had no effect on larval development time or the size of emerging adults from a low nutrition medium. While Wolbachia may influence the expression of heat shock proteins, we found that there was no effect on adult heat resistance when tested in terms of survival or virility following heat stress. The absence of nutrition or stress effects suggests that other processes maintain wMel frequencies in natural populations of Drosophila melanogaster.

Correlated response of autogeny to selection for adult starvation resistance in the blowfly, Lucilia cuprina

We withheld sucrose from adults in three lineages of Lucilia cuprina, producing a four-fold greater mortality than in control lineages, in order to impose direct selection for carbohydrate starvation resistance. The frequency of autogeny (maturation of eggs in the absence of adult protein feeding) increased as a correlated response by an average of 4.9 to 9.2% per generation in three lineages subjected to starvation over five generations. The frequency of autogeny fluctuated but did not display a significant net change in three control lineages. Autogeny in L. cuprina seems to behave as a threshold trait, with a continuous, genetically-based underlying disposition producing discrete phenotypes. The heritability of autogeny in our laboratory lineages was estimated to be 0.09 to 0.39, 0.04 to 0.36, and -0.08 to 0.30 (95% confidence intervals). Despite the potential for autogeny to evolve and despite protein limitation of female fecundity in Australian populations of L. cuprina, the trait is rare or absent in the field. Genetic variation for autogeny may be maintained, but at sub-threshold levels, by nutrient availability in the field, while trade-offs associated with autogeny probably limit the net fitness benefit of the trait and prevent the evolution of a noticeable frequency of autogenous females.

Correlated response of autogeny to selection for adult starvation resistance in the blowfly, Lucilia cuprina

We withheld sucrose from adults in three lineages of Lucilia cuprina, producing a four-fold greater mortality than in control lineages, in order to impose direct selection for carbohydrate starvation resistance. The frequency of autogeny (maturation of eggs in the absence of adult protein feeding) increased as a correlated response by an average of 4.9 to 9.2% per generation in three lineages subjected to starvation over five generations. The frequency of autogeny fluctuated but did not display a significant net change in three control lineages. Autogeny in L. cuprina seems to behave as a threshold trait, with a continuous, genetically-based underlying disposition producing discrete phenotypes. The heritability of autogeny in our laboratory lineages was estimated to be 0.09 to 0.39, 0.04 to 0.36, and −0.08 to 0.30 (95% confidence intervals). Despite the potential for autogeny to evolve and despite protein limitation of female fecundity in Australian populations of L. cuprina, the trait is rare or absent in the field. Genetic variation for autogeny may be maintained, but at sub-threshold levels, by nutrient availability in the field, while trade-offs associated with autogeny probably limit the net fitness benefit of the trait and prevent the evolution of a noticeable frequency of autogenous females.

Life-History Traits Related to Host Selection in Mycophagous Drosophilids

1. Mycophagous drosophilids in Hokkaido, northern Japan, differ in fungal host selection from each other. Differences in life-history traits among them are explained by 'habitat' characteristics influential to the demography of adults and larvae. 2. Pleurotus fungi, to which three Hirtodrosophila species are specialized, produce fruiting bodies, usually in large clumps, intermittently throughout the fly breeding season on the large, dead logs or stumps of elms. On the other hand, the appearance of fruiting bodies is temporally unpredictable in fungi other than Pleurotus, being restricted, respectively, to particular seasons and influenced greatly by weather conditions. Newly emerging adults of polyphagous species have higher abilities to withstand starvation than those of the stenophagous Hirtodrosophila species, in order to cope with their temporally unpredictable habitats. However, habitat unpredictability for mature adults that have already found a fungal patch and fed and/or bred on it is reversed between the stenophagous and polyphagous species. The three Hirtodrosophila species specialized to Pleurotus fungi show significantly higher ratios of reproductive allocation than the other polyphagous species. There will be no chance for mature adult flies of the Hirtodrosophila species to find another breeding site. They are, therefore, regarded as living in spatially unpredictable habitats and to allocate more energy to current reproduction. On the other hand, mature adults of polyphagous species are expected to find another site more easily owing to their polyphagous nature, and invest some energy for residual reproductive value. 3. Five species preferring decayed fungi allocate nearly equal proportions of energy to reproduction, but partition is differently allocated to either large clutches or to large eggs. This differentiation of strategies is related to the difference in larval habitats. Larval habitats are regarded as more unstable for species utilizing fungi of shorter duration. In short-lasting habitats, larvae growing up within a short period would be favoured by natural selection. Larval developmental time is negatively correlated with relative egg size. Drosophila brachynephros and D. curvispina, which are somewhat specialized to soft, deliquescent Coprinus fungi, take the large-egg strategy to cope with their short-lasting larval habitats. On the other hand, H. histrioides, frequently using Polyporellus fungi with large, long-lasting fruiting bodies, take the opposite strategy, producing many small eggs. The same positive correlation between the developmental time and the duration of fungi preferred is also seen among species breeding on fresh fungi. However, the developmental time is always shorter in species preferring decayed fungi than in species preferring fresh ones if the relative egg size is the same. 4. The positive correlation between larval developmental time and adult survival, which is the basis for Sevenster & van Alphen's hypothesis that the difference in life histories promotes the co-existence of competing species in temporally variable environments, is tested for mycophagous drosophilids. It is demonstrated that there is a negative rather than positive correlation between larval developmental time and adult survival time under starvation. Adult starvation resistance is directly correlated with adult body size, and larval developmental time with relative egg size. This study suggests that the relations between larval developmental time and adult survival can be reversed according to the combinations of adult and larval habitats.

COMPLEX TRADE-OFFS AND THE EVOLUTION OF STARVATION RESISTANCE IN DROSOPHILA MELANOGASTER.

The measurement of trade-offs may be complicated when selection exploits multiple avenues of adaptation or multiple life-cycle stages. We surveyed 10 populations of Drosophila melanogaster selected for increased resistance to starvation for 60 generations, their paired controls, and their mutual ancestors (a total of 30 outbred populations) for evidence of physiological and life-history trade-offs that span life-cycle stages. The directly selected lines showed an impressive response to starvation selection, with mature adult females resisting starvation death 4-6 times longer than unselected controls or ancestors-up to a maximum of almost 20 days. Starvation-selected flies are already 80% more resistant to starvation death than their controls immediately upon eclosion, suggesting that a significant portion of their selection response was owing to preadult growth and acquisition of metabolites relevant to the stress. These same lines exhibited significantly longer development and lower viability in the larval and pupal stages. Weight and lipid measurements on one of the starvation-selected treatments (SB1-5 ), its control populations (CB1-5 ), and their ancestor populations (B1-5 ) revealed three important findings. First, starvation resistance and lipid content were linearly correlated; second, larval lipid acquisition played a major role in the evolution of adult starvation resistance; finally, increased larval growth rate and lipid acquisition had a fitness cost exacted in reduced viability and slower development. This study implicates multiple life-cycle stages in the response to selection for the stress resistance of only one stage. Our starvation-selected populations illustrate a case that may be common in nature. Patterns of genetic correlation may prove misleading unless multiple pleiotropic interconnections are resolved.