Adult Starvation 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.

Consistent heat tolerance under starvation across seasonal morphs in Mycalesis mineus (Lepidoptera: Nymphalidae)

Heat tolerance is a key trait for understanding insect responses to extreme heat events, but tolerance may be modulated by changes in food availability and seasonal variability in temperature. Differences in sensitivity and resistance across life stages are also important determinants of species responses. Using a full-factorial experimental design, we here investigated the effects of larval starvation, adult starvation, and seasonal morph (developmental temperature) on heat tolerance of a seasonally polyphenic butterfly, Mycalesis mineus, in both larval and adult stages. While starvation and rearing temperature profoundly influenced various life history traits in the insect, none of the treatments affected adult heat tolerance. There was also no evidence of reduced heat tolerance in larvae under starvation stress, though larval thermal tolerance was higher by ~1 °C at the higher developmental temperature. The lack of a starvation effect was unexpected given the general physiological cost of heat tolerance mechanisms. This might be attributed to the ability to tolerate heat being preserved under resource-based trade-offs due to its critical role in ensuring insect survival. Invariant heat tolerance in M. mineus shows that some insects may have thermal capacity to cope with extreme heat under short-term starvation and seasonality disruptions, though more prolonged changes may have greater consequences. The capacity to maintain key physiological function under multiple stressors will be crucial for species resilience in future novel environments.

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 effects of adaptation to urea on feeding rates and growth in Drosophila larvae.

A collection of forty populations were used to study the phenotypic adaptation of Drosophila melanogaster larvae to urea‐laced food. A long‐term goal of this research is to map genes responsible for these phenotypes. This mapping requires large numbers of populations. Thus, we studied fifteen populations subjected to direct selection for urea tolerance and five controls. In addition, we studied another twenty populations which had not been exposed to urea but were subjected to stress or demographic selection. In this study, we describe the differentiation in these population for six phenotypes: (1) larval feeding rates, (2) larval viability in urea‐laced food, (3) larval development time in urea‐laced food, (4) adult starvation times, (5) adult desiccation times, and (6) larval growth rates. No significant differences were observed for desiccation resistance. The demographically/stress‐selected populations had longer times to starvation than urea‐selected populations. The urea‐adapted populations showed elevated survival and reduced development time in urea‐laced food relative to the control and nonadapted populations. The urea‐adapted populations also showed reduced larval feeding rates relative to controls. We show that there is a strong linear relationship between feeding rates and growth rates at the same larval ages feeding rates were measured. This suggests that feeding rates are correlated with food intake and growth. This relationship between larval feeding rates, food consumption, and efficiency has been postulated to involve important trade‐offs that govern larval evolution in stressful environments. Our results support the idea that energy allocation is a central organizing theme in adaptive evolution.

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.

A Mutation of lips-6 in C. elegans.

The lips-6 gene encodes a putative lipase that plays a role in adult starvation response through a pathway that is parallel to the dauer pathway in larval Caenorhabditis elegans worms. We created a mutation of lips-6 to study its effects on lifespan and the ascaroside profile. We found that lips-6 had a wild-type lifespan and a wild-type ascaroside profile. These results suggest that the lips-6 gene plays a minimal role in C. elegans lifespan biology and does not affect the ascaroside profile until it is specifically activated by starvation in adult worms.

Cross-Generational Effects of Heat Stress on Fitness and Wolbachia Density in Aedes aegypti Mosquitoes.

Aedes aegypti mosquitoes infected with Wolbachia symbionts are now being released into the field to control the spread of pathogenic human arboviruses. Wolbachia can spread throughout vector populations by inducing cytoplasmic incompatibility and can reduce disease transmission by interfering with virus replication. The success of this strategy depends on the effects of Wolbachia on mosquito fitness and the stability of Wolbachia infections across generations. Wolbachia infections are vulnerable to heat stress, and sustained periods of hot weather in the field may influence their utility as disease control agents, particularly if temperature effects persist across generations. To investigate the cross-generational effects of heat stress on Wolbachia density and mosquito fitness, we subjected Ae. aegypti with two different Wolbachia infection types (wMel, wAlbB) and uninfected controls to cyclical heat stress during larval development over two generations. We then tested adult starvation tolerance and wing length as measures of fitness and measured the density of wMel in adults. Both heat stress and Wolbachia infection reduced adult starvation tolerance. wMel Wolbachia density in female offspring was lower when mothers experienced heat stress, but male Wolbachia density did not depend on the rearing temperature of the previous generation. We also found cross-generational effects of heat stress on female starvation tolerance, but there was no cross-generational effect on wing length. Fitness costs of Wolbachia infections and cross-generational effects of heat stress on Wolbachia density may reduce the ability of Wolbachia to invade populations and control arbovirus transmission under specific environmental conditions.

Larval starvation improves metabolic response to adult starvation in honey bees (Apis mellifera L.).

Environmental changes during development have long-term effects on adult phenotypes in diverse organisms. Some of the effects play important roles in helping organisms adapt to different environments, such as insect polymorphism. Others, especially those resulting from an adverse developmental environment, have a negative effect on adult health and fitness. However, recent studies have shown that those phenotypes influenced by early environmental adversity have adaptive value under certain (anticipatory) conditions that are similar to the developmental environment, though evidence is mostly from morphological and behavioral observations and it is still rare at physiological and molecular levels. In the companion study, we applied a short-term starvation treatment to fifth instar honey bee larvae and measured changes in adult morphology, starvation resistance, hormonal and metabolic physiology and gene expression. Our results suggest that honey bees can adaptively respond to the predicted nutritional stress. In the present study, we further hypothesized that developmental starvation specifically improves the metabolic response of adult bees to starvation instead of globally affecting metabolism under well-fed conditions. Here, we produced adult honey bees that had experienced a short-term larval starvation, then we starved them for 12 h and monitored metabolic rate, blood sugar concentrations and metabolic reserves. We found that the bees that experienced larval starvation were able to shift to other fuels faster and better maintain stable blood sugar levels during starvation. However, developmental nutritional stress did not change metabolic rates or blood sugar levels in adult bees under normal conditions. Overall, our study provides further evidence that early larval starvation specifically improves the metabolic responses to adult starvation in honey bees.

Changes in the biting activity of a dengue vector relative to larval and adult nutritional histories: Implications for preventive measures

The magnitude of dengue transmission depends largely on the level of human–vector contact. Therefore, knowledge regarding the biting periodicity of mosquitoes is crucial to determine transmission periods' risk, and in planning personal protection measures. Dengue vectors are day-active and endure transitory periods of starvation overnight. However, it is unclear how their blood feeding activity pattern is related to body size when temporarily deprived of their main source of energy — sugar. We examined the changes in Aedes albopictus diurnal biting activity, taking into account larval nutritional history and adult starvation. Overall, large body size and non-starvation conditions were associated with better blood feeding success, but these parameters did not significantly modify the timing of first blood feeding attempt. Females of both sizes showed significant temporal variations in their blood feeding activities. Under conditions of starvation, blood meal uptake was much greater in large females from morning to evening. Similar variations of feeding activity were observed in small females, except in the morning. Under non-starvation conditions, the blood feeding activity of small mosquitoes tended to decrease over time, whereas blood meal uptake activity was high and remained almost constant from morning to evening for larger mosquitoes. This work emphasizes the importance of body size and hunger on the dynamics of vector–host interaction and has important implications for the development of novel strategies for the prevention of disease transmission. Knowing when dengue vectors actively bite during the day can help in timing effective personal protective measures.

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.

Adult Starvation and Disease‐Related Malnutrition

Multiple definitions for malnutrition syndromes are found in the literature resulting in confusion. Recent evidence suggests that varying degrees of acute or chronic inflammation are key contributing factors in the pathophysiology of malnutrition that is associated with disease or injury. An International Guideline Committee was constituted to develop a consensus approach to defining malnutrition syndromes for adults in the clinical setting. Consensus was achieved through a series of meetings held at the A.S.P.E.N. and ESPEN Congresses. It was agreed that an etiology-based approach that incorporates a current understanding of inflammatory response would be most appropriate. The Committee proposes the following nomenclature for nutrition diagnosis in adults in the clinical practice setting. "Starvation-related malnutrition", when there is chronic starvation without inflammation, "chronic disease-related malnutrition", when inflammation is chronic and of mild to moderate degree, and "acute disease or injury-related malnutrition", when inflammation is acute and of severe degree. This commentary is intended to present a simple etiology-based construct for the diagnosis of adult malnutrition in the clinical setting. Development of associated laboratory, functional, food intake, and body weight criteria and their application to routine clinical practice will require validation.

Neonatal Maternal Deprivation Response and Developmental Changes in Gene Expression Revealed by Hypothalamic Gene Expression Profiling in Mice

Neonatal feeding problems are observed in several genetic diseases including Prader-Willi syndrome (PWS). Later in life, individuals with PWS develop hyperphagia and obesity due to lack of appetite control. We hypothesized that failure to thrive in infancy and later-onset hyperphagia are related and could be due to a defect in the hypothalamus. In this study, we performed gene expression microarray analysis of the hypothalamic response to maternal deprivation in neonatal wild-type and Snord116del mice, a mouse model for PWS in which a cluster of imprinted C/D box snoRNAs is deleted. The neonatal starvation response in both strains was dramatically different from that reported in adult rodents. Genes that are affected by adult starvation showed no expression change in the hypothalamus of 5 day-old pups after 6 hours of maternal deprivation. Unlike in adult rodents, expression levels of Nanos2 and Pdk4 were increased, and those of Pgpep1, Ndp, Brms1l, Mett10d, and Snx1 were decreased after neonatal deprivation. In addition, we compared hypothalamic gene expression profiles at postnatal days 5 and 13 and observed significant developmental changes. Notably, the gene expression profiles of Snord116del deletion mice and wild-type littermates were very similar at all time points and conditions, arguing against a role of Snord116 in feeding regulation in the neonatal period.

Adult starvation and disease-related malnutrition: A proposal for etiology-based diagnosis in the clinical practice setting from the International Consensus Guideline Committee

Multiple definitions for malnutrition syndromes are found in the literature resulting in confusion. Recent evidence suggests that varying degrees of acute or chronic inflammation are key contributing factors in the pathophysiology of malnutrition that is associated with disease or injury. An International Guideline Committee was constituted to develop a consensus approach to defining malnutrition syndromes for adults in the clinical setting. Consensus was achieved through a series of meetings held at the ASPEN and ESPEN Congresses. It was agreed that an etiology-based approach that incorporates a current understanding of inflammatory response would be most appropriate. The Committee proposes the following nomenclature for nutrition diagnosis in adults in the clinical practice setting. "Starvation-related malnutrition", when there is chronic starvation without inflammation, "chronic disease-related malnutrition", when inflammation is chronic and of mild to moderate degree, and "acute disease or injury-related malnutrition", when inflammation is acute and of severe degree. This commentary is intended to present a simple etiology-based construct for the diagnosis of adult malnutrition in the clinical setting. Development of associated laboratory, functional, food intake, and body weight criteria and their application to routine clinical practice will require validation.

Increased Life Span in a Polyphenic Butterfly Artificially Selected for Starvation Resistance

Starvation resistance is closely associated with fitness in natural populations of many organisms. It often co-varies with longevity and is a relevant target for understanding the evolution of aging. We selected for increased starvation resistance in the seasonally polyphenic butterfly Bicyclus anynana in a warm, wet-seasonal environment over 17 generations. We measured the response to selection for two selected lines compared to that of an unselected stock. Results show an increase in survival under adult starvation of 50%-100%. In addition, selection lines showed an increase in life span under normal adult feeding of 30%-50%. Female reproduction was changed toward laying fewer but larger eggs. The results indicate a sex-specific response to selection: females reallocated resources toward a more durable body, whereas males appeared to increase starvation resistance through changed metabolic rate. The phenotype produced by artificial selection resembles the form that occurs in the cool, dry-season environment, which suggests that selection has targeted the regulatory mechanisms for survival that are also involved in the suite of traits (including starvation resistance) central to the adaptive plastic response of this butterfly to seasonal conditions. In general, these results imply that the regulation of life span involves mechanisms of phenotypic plasticity.

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.