Selection for rapid and slow recovery from chill‐ and heat‐coma in Drosophila melanogaster

To assess the trade‐offs associated with cold and heat tolerance, selection experiments were conducted on the rate of recovery from chill‐ and heat‐coma using Drosophila melanogaster. Flies were treated with cold and heat to induce coma, and those that showed rapid or slow recovery from coma were selected. The lines selected for rapid (or slow) recovery from chill‐coma also showed rapid (slow) recovery from heat‐coma, although such a correlation was not observed in the lines selected for the rate of recovery from heat‐coma. On the other hand, survival after cold was enhanced in both lines selected for rapid and slow recovery from chill‐coma, and survival after heat was enhanced in both lines selected for rapid and slow recovery from heat‐coma. It was assumed that cold and heat treatments to induce coma caused some damages to flies and those that were tolerant to cold or heat were unintentionally selected in the present coma‐based selection. Only a weak trade‐off was observed between survival‐based cold and heat tolerance. On the other hand, developmental time was prolonged and desiccation resistance, walking speed, and longevity were reduced in the lines selected for rapid and slow recovery from chill‐ and/or heat‐coma, suggesting that these resistance and life‐history traits are under trade‐offs with cold and/or heat tolerance. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 72–80.     

Idiosyncratic evolution of maternal effects in response to juvenile malnutrition in Drosophila

Maternal effects often affect fitness traits, but there is little experimental evidence pertaining to their contribution to response to selection imposed by novel environments. We studied the evolution of maternal effects in Drosophila populations selected for tolerance to chronic larval malnutrition. To this end, we performed pairwise reciprocal F₁ crosses between six selected (malnutrition tolerant) populations and six unselected control populations and assessed the effect of cross direction on larval growth and developmental rate, adult weight and egg‐to‐adult viability expressed under the malnutrition regime. Each pair of reciprocal crosses revealed large maternal effects (possibly including cytoplasmic genetic effects) on at least one trait, but the magnitude, sign and which traits were affected varied among populations. Thus, maternal effects contributed significantly to the response to selection imposed by the malnutrition regime, but these changes were idiosyncratic, suggesting a rugged adaptive landscape. Furthermore, although the selected populations evolved both faster growth and higher viability, the maternal effects on growth rate and viability were negatively correlated across populations. Thus, genes mediating maternal effects can evolve to partially counteract the response to selection mediated by the effects of alleles on their own carriers’ phenotype, and maternal effects may contribute to evolutionary trade‐offs between components of offspring fitness.     

No apparent cost of evolved immune response in Drosophila melanogaster

Maintenance and deployment of the immune system are costly and are hence predicted to trade‐off with other resource‐demanding traits, such as reproduction. We subjected this longstanding idea to test using laboratory experimental evolution approach. In the present study, replicate populations of Drosophila melanogaster were subjected to three selection regimes—I (Infection with Pseudomonas entomophila), S (Sham‐infection with MgSO₄), and U (Unhandled Control). After 30 generations of selection flies from the I regime had evolved better survivorship upon infection with P. entomophila compared to flies from U and S regimes. However, contrary to expectations and previous reports, we did not find any evidence of trade‐offs between immunity and other life history related traits, such as longevity, fecundity, egg hatchability, or development time. After 45 generations of selection, the selection was relaxed for a set of populations. Even after 15 generations, the postinfection survivorship of populations under relaxed selection regime did not decline. We speculate that either there is a negligible cost to the evolved immune response or that trade‐offs occur on traits such as reproductive behavior or other immune mechanisms that we have not investigated in this study. Our research suggests that at least under certain conditions, life‐history trade‐offs might play little role in maintaining variation in immunity.     

Changes in thermotolerance and Hsp70 expression with domestication in Drosophila melanogaster

To examine how the duration of laboratory domestication may affect Drosophila stocks used in studies of thermotolerance, we measured expression of the inducible heat‐shock protein Hsp70 and survival after heat shock in D. melanogaster strains recently collected from nature and maintained in laboratory culture for up to 50 or more generations. After an initial increase in both Hsp70 expression and thermotolerance immediately after transfer to laboratory medium, both traits remained fairly constant over time and variation among strains persisted through laboratory domestication. Furthermore, variation in heat tolerance and Hsp70 expression did not correlate with the length of time populations evolved in the laboratory. Therefore, while environmental variation likely contributed most to early shifts in strain tolerance and Hsp70 expression, other population parameters, for example genetic drift, inbreeding, and selection likely affected these traits little. As long as populations are maintained with large numbers of individuals, the culture of insects in the laboratory may have little effect on the tolerance of different strains to thermal stress.     

Evidence for a robust sex-specific trade-off between cold resistance and starvation resistance in Drosophila melanogaster

In insects changes in lipid metabolism may underlie a trade-off between cold resistance and starvation resistance. To test this we examined correlated responses in independent sets of Drosophila melanogaster lines selected for increased cold resistance and increased starvation resistance. The starvation lines showed correlated patterns found in other D. melanogaster populations selected for this trait, including higher lipid levels and increased resistance to desiccation, although the selected lines did not show a longer development time as found in some other studies. Consistent with the trade-off hypothesis, selected lines with increased starvation resistance showed decreased resistance to a cold stress as measured by mortality, whereas selected lines with increased cold resistance showed a decrease in starvation resistance. To counter the possibility of inadvertent selection accounting for these patterns, selected and control lines from both selection regimes were crossed to form mass bred populations, which were left for four generations prior to establishing isofemale lines. By scoring starvation and cold resistance in these lines derived from both sets of selection regimes, we confirmed the negative association between resistance to these stresses in females but not in males. Potential implications of this trade-off for surviving cold conditions when food resources are limiting are discussed.     

Evolution of increased adult longevity in Drosophila melanogaster populations selected for adaptation to larval crowding

In holometabolous animals such as Drosophila melanogaster, larval crowding can affect a wide range of larval and adult traits. Adults emerging from high larval density cultures have smaller body size and increased mean life span compared to flies emerging from low larval density cultures. Therefore, adaptation to larval crowding could potentially affect adult longevity as a correlated response. We addressed this issue by studying a set of large, outbred populations of D. melanogaster, experimentally evolved for adaptation to larval crowding for 83 generations. We assayed longevity of adult flies from both selected (MCUs) and control populations (MBs) after growing them at different larval densities. We found that MCUs have evolved increased mean longevity compared to MBs at all larval densities. The interaction between selection regime and larval density was not significant, indicating that the density dependence of mean longevity had not evolved in the MCU populations. The increase in longevity in MCUs can be partially attributed to their lower rates of ageing. It is also noteworthy that reaction norm of dry body weight, a trait probably under direct selection in our populations, has indeed evolved in MCU populations. To the best of our knowledge, this is the first report of the evolution of adult longevity as a correlated response of adaptation to larval crowding.     

Reverse evolution of fitness in Drosophila melanogaster

Abstract The evolution of fitness is central to evolutionary theory, yet few experimental systems allow us to track its evolution in genetically and environmentally relevant contexts. Reverse evolution experiments allow the study of the evolutionary return to ancestral phenotypic states, including fitness. This in turn permits well‐defined tests for the dependence of adaptation on evolutionary history and environmental conditions. In the experiments described here, 20 populations of heterogeneous evolutionary histories were returned to their common ancestral environment for 50 generations, and were then compared with both their immediate differentiated ancestors and populations which had remained in the ancestral environment. One measure of fitness returned to ancestral levels to a greater extent than other characters did. The phenotypic effects of reverse evolution were also contingent on previous selective history. Moreover, convergence to the ancestral state was highly sensitive to environmental conditions. The phenotypic plasticity of fecundity, a character directly selected for, evolved during the experimental time frame. Reverse evolution appears to force multiple, diverged populations to converge on a common fitness state through different life‐history and genetic changes.     

Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup

It may be intuitive to predict that host immune systems will evolve to counter a broad range of potential challenges through simultaneous investment in multiple defences. However, this would require diversion of resources from other traits, such as growth, survival and fecundity. Therefore, ecological immunology theory predicts that hosts will specialize in only a subset of possible defences. We tested this hypothesis through a comparative study of a cellular immune response and a putative behavioural defence used by eight fruit fly species against two parasitoid wasp species (one generalist and one specialist). Fly larvae can survive infection by melanotically encapsulating wasp eggs, and female flies can potentially reduce infection rates in their offspring by laying fewer eggs when wasps are present. The strengths of both defences varied significantly but were not negatively correlated across our chosen host species; thus, we found no evidence for a trade‐off between behavioural and cellular immunity. Instead, cellular defences were significantly weaker against the generalist wasp, whereas behavioural defences were similar in strength against both wasps and positively correlated between wasps. We investigated the adaptive significance of wasp‐induced oviposition reduction behaviour by testing whether wasp‐exposed parents produce offspring with stronger cellular defences, but we found no support for this hypothesis. We further investigated the sensory basis of this behaviour by testing mutants deficient in either vision or olfaction, both of which failed to reduce their oviposition rates in the presence of wasps, suggesting that both senses are necessary for detecting and responding to wasps.     

Plastic and evolutionary responses of cell size and number to larval malnutrition in Drosophila melanogaster

Both development and evolution under chronic malnutrition lead to reduced adult size in Drosophila. We studied the contribution of changes in size vs. number of epidermal cells to plastic and evolutionary reduction of wing size in response to poor larval food. We used flies from six populations selected for tolerance to larval malnutrition and from six unselected control populations, raised either under standard conditions or under larval malnutrition. In the control populations, phenotypic plasticity of wing size was mediated by both cell size and cell number. In contrast, evolutionary change in wing size, which was only observed as a correlated response expressed on standard food, was mediated entirely by reduction in cell number. Plasticity of cell number had been lost in the selected populations, and cell number did not differ between the sexes despite males having smaller wings. Results of this and other experimental evolution studies are consistent with the hypothesis that alleles which increase body size through prolonged growth affect wing size mostly via cell number, whereas alleles which increase size through higher growth rate do so via cell size.     

Trade‐off of ovarian lipids and total body lipids for fecundity and starvation resistance in tropical populations of Drosophila melanogaster

In Drosophila melanogaster, clines of starvation resistance along a latitudinal gradient (south to north) have been reported in India, which matched with their cline for total body lipids (T_L). Nevertheless, producing too many reserves is likely to be costly and a trade‐off might exist with life‐history traits. Previous studies on starvation resistance and life‐history traits of D. melanogaster have mainly focused on quantification of total body lipids, instead of separating ovarian lipids from total body lipids. In the present study, we have quantified absolute ovarian lipids (O_L) versus absolute body lipids excluding ovarian lipids (B_L) and examined associations with fecundity as well as starvation resistance in two latitudinal populations (8.34 vs. 32.43°N) of D. melanogaster. Firstly, we observed a trade‐off between B_L and O_L that matched the trade‐off of starvation resistance, longevity versus fecundity and development time in latitudinal populations of D. melanogaster. Southern populations had higher starvation resistance, more B_L and lesser O_L, whereas northern populations had enhanced fecundity, O_L and lesser B_L. Secondly, within population, starvation resistance also correlated with B_L, and fecundity with O_L. However, there was no correlation between starvation resistance and O_L. Moreover, there was utilization of B_L and nonutilization of O_L under starvation stress. Therefore, resources invested for fecundity in the form of O_L were independent of evolved starvation resistance in D. melanogaster. Our results suggest that a common pool of energy storage compounds (lipids) are allocated differentially between fecundity and starvation resistance and are consistent with Y‐model of resource allocation.     

Sexual selection and immune function in Drosophila melanogaster

The evolution of immune function depends not only on variation in genes contributing directly to the immune response, but also on genetic variation in other traits indirectly affecting immunocompetence. In particular, sexual selection is predicted to trade-off with immunocompetence because the extra investment of resources needed to increase sexual competitiveness reduces investment in immune function. Additional possible immunological consequences of intensifying sexual selection include an exaggeration of immunological sexual dimorphism, and the reduction of condition-dependent immunological costs due to selection of 'good genes' (the immunocompetence handicap hypothesis, ICHH). We tested for these evolutionary possibilities by increasing sexual selection in laboratory populations of Drosophila melanogaster for 58 generations by reestablishing a male-biased sex ratio at the start of each generation. Sexually selected flies were larger, took longer to develop, and the males were more sexually competitive than males from control (equal sex ratio) lines. We found support for the trade-off hypothesis: sexually selected males were found to have reduced immune function compared to control males. However, we found no evidence that sexual selection promoted immunological sexual dimorphism because females showed a similar reduction in immune function. We found no evidence of evolutionary changes in the condition-dependent expression of immunocompetence contrary to the expectations of the ICHH. Lastly, we compared males from the unselected base population that were either successful (IS) or unsuccessful (IU) in a competitive mating experiment. IS males showed reduced immune function relative to IU males, suggesting that patterns of phenotypic correlation largely mirror patterns of genetic correlation revealed by the selection experiment. Our results suggest increased disease susceptibility could be an important cost limiting increases in sexual competitiveness in populations experiencing intense sexual selection. Such costs may be particularly important given the high intersex correlation, because this represents an apparent genetic conflict, preventing males from reaching their sexually selected optimum.     

Evolution of foraging behaviour in response to chronic malnutrition in Drosophila melanogaster

Chronic exposure to food of low quality may exert conflicting selection pressures on foraging behaviour. On the one hand, more active search behaviour may allow the animal to find patches with slightly better, or more, food; on the other hand, such active foraging is energetically costly, and thus may be opposed by selection for energetic efficiency. Here, we test these alternative hypotheses in Drosophila larvae. We show that populations which experimentally evolved improved tolerance to larval chronic malnutrition have shorter foraging path length than unselected control populations. A behavioural polymorphism in foraging path length (the rover-sitter polymorphism) exists in nature and is attributed to the foraging locus (for). We show that a sitter strain (for(s2)) survives better on the poor food than the rover strain (for(R)), confirming that the sitter foraging strategy is advantageous under malnutrition. Larvae of the selected and control populations did not differ in global for expression. However, a quantitative complementation test suggests that the for locus may have contributed to the adaptation to poor food in one of the selected populations, either through a change in for allele frequencies, or by interacting epistatically with alleles at other loci. Irrespective of its genetic basis, our results provide two independent lines of evidence that sitter-like foraging behaviour is favoured under chronic larval malnutrition.     

The effects of selection for larval behavior on adult life-history features in Drosophila melanogaster

Selection for late-life fecundity and longevity in adult Drosophila melanogaster is well known to modify numerous characteristics of life history and physiology. We report experiments here in which selection applied to behavior affects features in an identical fashion. Selection for feeding rate of larval D. melanogaster modifies caloric intake, as measured by the uptake and incorporation of labeled glucose. Selection for slow larval feeding produced lines of D. melanogaster in which larvae synthesized significantly less lipid prior to pupation and eclosed to have low early-life fecundity and a long life as adults. They also had greater lifetime fecundity, but lower viability of egg to hatched adult. Alternatively, fast-feeding larvae incorporated more lipid before pupation and eclosed with high early-fecundity that declined rapidly throughout their short adult life. Slow-feeding populations also had a significantly enhanced expression of the stress-resistance genes CuZn-SOD, CATALASE, and HSP70. Selection on larval feeding behavior reproduced the antagonistic evolutionary trade-off found under selection for adult life span and mimicked the physiological response in life span as seen in many species when dietary restriction is imposed on adults. Thus, nutrient acquisition during development appears to share a common evolutionary and genetic basis with the allocation processes that determine adult life-history traits and the related phenotypic dietary restriction phenomena.     

Starvation tolerance associated with prolonged sleep bouts upon starvation in a single natural population of Drosophila melanogaster

Large genetic variations in starvation tolerance in animals indicate that there are multiple strategies to cope with low‐nutrient conditions. Fruit flies (Drosophila melanogaster) typically respond to starvation by suppressing sleep and enhancing locomotor activity presumably to search for food. However, we hypothesized that in a natural population, there are costs and benefits to sleep suppression under low‐nutrient conditions and that conserving energy through sleep could be a better strategy depending on food availability. In this study, we quantified the variation in sleep‐related traits in 21 wild‐derived inbred lines from Katsunuma, Japan, under fed and starved conditions and analysed the relationship between those traits and starvation tolerance. Although most of the lines responded to starvation by suppressing the total time in sleep, there were indeed two lines that responded by significantly increasing the sleep‐bout durations and thus not reducing the total time in sleep. These genotypes survived longer in acute starvation conditions compared to genotypes that responded by the immediate suppression of sleep, which could be due to the reduced metabolic rate during the long uninterrupted sleep bouts. The coexistence of the enhanced foraging and resting strategies upon starvation within a single population is consistent with the presence of a behavioural trade‐off between food search and energy conservation due to unpredictable food availability in nature. These results provide insights into the evolutionary mechanisms that contribute to the maintenance of genetic variations underlying environmental stress resistance.     

Parasitism offers large rewards but carries high risks: Predicting parasitic strategies under different life history conditions in lampreys

The loss of parasitism in metazoan lineages is often seen as unlikely, but it has occurred in some lineages (e.g., leeches, lampreys). How and why parasitism is lost is aptly addressed by studying lampreys, because extant species include a range of feeding modes and parasitism has been lost repeatedly. An individual‐based model was developed to determine whether variations in survival and growth rates in the larval and juvenile stages could favour parasitic or nonparasitic strategies. A realization of the model for a Lampetra spp. population, a genus which includes parasitic and nonparasitic animals, indicated that both strategies could be successful. A different model realization of the nonparasitic species Lethenteron appendix also agreed with expectations, and only nonparasitic strategies were successful. Modelling anadromous Petromyzon marinus produced only parasitic animals, as expected, but suggested two different adult sizes should appear in the population, which has not been reported in the literature. Finally, a realization of an Ichthyomyzon castaneus population, known to be parasitic only, rarely selected for parasitism (c. 7% of model iterations), possibly because the population used to parameterize the model was unusual for the species. The results suggest that nonparasitic lineages in lampreys are common because parasitism, while offering better growth, also has lower survival. Additionally, nonparasitic species may be generated at different rates because growth and survival thresholds in the model favouring parasitism are close to observed estimates in some populations. Loss of parasitism can occur when life stages have different trade‐offs in growth and survivability.     

Adaptation to fluctuating environments in a selection experiment with Drosophila melanogaster

A fundamental question in life‐history evolution is how organisms cope with fluctuating environments, including variation between stressful and benign conditions. For short‐lived organisms, environments commonly vary between generations. Using a novel experimental design, we exposed wild‐derived Drosophila melanogaster to three different selection regimes: one where generations alternated between starvation and benign conditions, and starvation was always preceded by early exposure to cold; another where starvation and benign conditions alternated in the same way, but cold shock sometimes preceded starvation and sometimes benign conditions; and a third where conditions were always benign. Using six replicate populations per selection regime, we found that selected flies increased their starvation resistance, most strongly for the regime where cold and starvation were reliably combined, and this occurred without decreased fecundity or extended developmental time. The selected flies became stress resistant, displayed a pronounced increase in early life food intake and resource storage. In contrast to previous experiments selecting for increased starvation resistance in D. melanogaster, we did not find increased storage of lipids as the main response, but instead that, in particular for females, storage of carbohydrates was more pronounced. We argue that faster mobilization of carbohydrates is advantageous in fluctuating environments and conclude that the phenotype that evolved in our experiment corresponds to a compromise between the requirements of stressful and benign environments.     

The trade‐off between fecundity and egg size in a polymorphic population of Arctic charr (Salvelinus alpinus (L.)) in Skogsfjordvatn,subarctic Norway

Reproductive traits differ between intralacustrine Arctic charr morphs. Here, we examine three sympatric lacustrine Arctic charr morphs with respect to fecundity, egg size and spawning time/site to assess reproductive investments and trade‐offs, and possible fitness consequences. The littoral omnivore morph (LO‐morph) utilizes the upper water for feeding and reproduction and spawn early in October. The large profundal piscivore morph (PP‐morph) and the small profundal benthivore morph (PB‐morph) utilize the profundal habitat for feeding and reproduction and spawn in December and November, respectively. Females from all morphs were sampled for fecundity and egg‐size analysis. There were large differences between the morphs. The PB‐morph had the lowest fecundity (mean = 45, SD = 13) and smallest egg size (mean = 3.2 mm, SD = 0.32 mm). In contrast, the PP‐morph had the highest fecundity (mean = 859.5, SD = 462) and the largest egg size (mean = 4.5 mm, SD = 0.46 mm), whereas the LO‐morph had intermediate fecundity (mean = 580, SD = 225) and egg size (mean = 4.3, SD = 0.24 mm). Fecundity increased with increasing body size within each morph. This was not the case for egg size, which was independent of body sizes within morph. Different adaptations to feeding and habitat utilization have apparently led to a difference in the trade‐off between fecundity and egg size among the three different morphs.     

Experimental evolution of slowed cognitive aging in Drosophila melanogaster

Reproductive output and cognitive performance decline in parallel during aging, but it is unknown whether this reflects a shared genetic architecture or merely the declining force of natural selection acting independently on both traits. We used experimental evolution in Drosophila melanogaster to test for the presence of genetic variation for slowed cognitive aging, and assess its independence from that responsible for other traits’ decline with age. Replicate experimental populations experienced either joint selection on learning and reproduction at old age (Old + Learning), selection on late‐life reproduction alone (Old), or a standard two‐week culture regime (Young). Within 20 generations, the Old + Learning populations evolved a slower decline in learning with age than both the Old and Young populations, revealing genetic variation for cognitive aging. We found little evidence for a genetic correlation between cognitive and demographic aging: although the Old + Learning populations tended to show higher late‐life fecundity than Old populations, they did not live longer. Likewise, selection for late reproduction alone did not result in improved late‐life learning. Our results demonstrate that Drosophila harbor genetic variation for cognitive aging that is largely independent from genetic variation for demographic aging and suggest that these two aspects of aging may not necessarily follow the same trajectories.     

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.     

Condition‐dependent mortality exacerbates male (but not female) reproductive senescence and the potential for sexual conflict

Disentangling the relationship between age and reproduction is central to understand life‐history evolution, and recent evidence shows that considering condition‐dependent mortality is a crucial piece of this puzzle. For example, nonrandom mortality of ‘low‐condition’ individuals can lead to an increase in average lifespan. However, selective disappearance of such low‐condition individuals may also affect reproductive senescence at the population level due to trade‐offs between physiological functions related to survival/lifespan and the maintenance of reproductive functions. Here, we address the idea that condition‐dependent extrinsic mortality (i.e. simulated predation) may increase the age‐related decline in male reproductive success and with it the potential for sexual conflict, by comparing reproductive ageing in Drosophila melanogaster male/female cohorts exposed (or not) to condition‐dependent simulated predation across time. Although female reproductive senescence was not affected by predation, male reproductive senescence was considerably higher under predation, due mainly to an accelerated decline in offspring viability of ‘surviving’ males with age. This sex‐specific effect suggests that condition‐dependent extrinsic mortality can exacerbate survival‐reproduction trade‐offs in males, which are typically under stronger condition‐dependent selection than females. Interestingly, condition‐dependent extrinsic mortality did not affect mating success, hinting that accelerated reproductive senescence is due to a decrease in male post‐copulatory fitness components. Our results support the recent proposal that male ageing can be an important source of sexual conflict, further suggesting this effect could be exacerbated under more natural conditions.