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.     

Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster

Laboratory studies on Drosophila have revealed that resistance to one environmental stress often correlates with resistance to other stresses. There is also evidence on genetic correlations between stress resistance, longevity and other fitness-related traits. The present work investigates these associations using artificial selection in Drosophila melanogaster. Adult flies were selected for increased survival after severe cold, heat, desiccation and starvation stresses as well as increased heat-knockdown time and lifespan (CS, HS, DS, SS, KS and LS line sets, respectively). The number of selection generations was 11 for LS, 27 for SS and 21 for other lines, with selection intensity being around 0.80. For each set of lines, the five stress-resistance parameters mentioned above as well as longevity (in a nonstressful environment) were estimated. In addition, preadult developmental time, early age productivity and thorax length were examined in all lines reared under nonstressful conditions. Comparing the selection lines with unselected control revealed clear-cut direct selection responses for the stress-resistance traits. Starvation resistance increased as correlated response in all sets of selection lines, with the exception of HS. Positive correlated responses were also found for survival after cold shock (HS and DS) and heat shock (KS and DS). With regard to values of resistance across different stress assays, the HS and KS lines were most similar. The resistance values of the SS lines were close to those of the LS lines and tended to be the lowest among all selection lines. Developmental time was extended in the SS and KS lines, whereas the LS lines showed a reduction in thorax length. The results indicate a possibility of different multiple-stress-resistance mechanisms for the examined traits and fitness costs associated with stress resistance and longevity.     

Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster

Drosophila melanogaster can be artificially selected for increased resistance against parasitoid wasps that attack the larvae. Lines selected for greater resistance are poorer larval competitors under conditions of resource scarcity. Here we investigated the mechanistic basis of this apparent trade-off. We found that resistant lines have approximately twice the density of haemocytes (blood cells) than that of controls. Haemocytes are involved in encapsulation, the chief cellular immune defence against parasitoids. We have previously shown that resistant lines feed more slowly than controls and hypothesize that limiting resources are being switched from trophic to defensive functions.     

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

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

Longevity and resistance to cold stress in cold‐stress selected lines and their controls in Drosophila melanogaster

Thermal environments can influence many fitness‐related traits including life span. Here, we assess whether longevity in Drosophila melanogaster can experimentally evolve as a correlated response to cold‐stress selection, and whether genotype‐by‐temperature and sex‐by‐temperature interactions are significant components of variation in life span. Three replicated S lines were cold‐stress selected and compared with their respective unselected controls (Clines) in the 16^th generation of thermal selection. Cold‐stress resistance exhibited a substantial direct response to selection, and also showed a significant interaction between sex and type of line. Mean longevity exhibited a significant interaction between adult test temperature (14 and 25 °C) and line (with suggestive evidence for increased longevity of S lines when tested at 14 °C), but there was no evidence for increased longevity in S lines at normal temperatures (i.e. 25 °C). Another temperature‐dependent effect was sex‐specific, with males being the longer lived sex at 25 °C but the less long‐lived sex at 14 °C. Additionally, we tested in an exploratory way the relationship between longevity and cold‐stress resistance by also measuring resistance to a prefreezing temperature before and after one generation of longevity selection at 14 °C (selection intensity, i = 1.47 for S lines, and 1.42 for C lines). In this longevity selection, we found that cold‐stress resistance increased by about 6% in S lines and 18% in C lines. However, taken together, the results indicate no simple relationship between longevity and cold‐stress resistance, with genotype‐by‐sex interactions in both traits. Temperature dependent interaction in longevity is apparent between S and C lines, and sex‐specific variation in mean longevity also depends on temperature.     

Host ecology shapes geographical variation for resistance to bacterial infection in Drosophila melanogaster

1. Geographically distinct host populations often experience very different ecological conditions. These variable ecological conditions impact the strength of selection that these hosts experience from their parasites. 2. Numerous studies have characterized geographical patterns of resistance to infection among natural populations in the context of host-parasite local adaptation, but what other factors might contribute to these differences? 3. Here, we determined whether 20 naturally isolated populations of Drosophila melanogaster collected along the East Coast of the United States varied for survival after being inoculated with one of two species of bacteria--Lactococcus lactis and Pseudomonas aeruginosa. We then asked whether host environment accounted for the observed patterns of resistance. 4. Resistance to both types of infection varied spatially. The hosts' natural environment was predictive of the observed spatial variation in resistance to L. lactis, but not P. aeruginosa, infection. Specifically, hosts exposed to species-rich bacterial communities were more likely to survive the infection. 5. We conclude that biotic characteristics of the host environment, specifically the number of species of bacteria hosts encounter, shape host resistance to bacterial infection in nature. We discuss our results in the context of what is known about the evolutionary ecology of resistance in invertebrate systems.     

Host preference and survival in selected lines of a Drosophila parasitoid,Asobara tabida

Host selection behaviour of parasitoids has important fitness consequences, if hosts of different quality are available. Here the host selection behaviour, the ability to distinguish between hosts differing in their suitability, of the Drosophila parasitizing wasp Asobara tabida was studied. Females from five lines selected for higher survival in the encapsulating host species D. melanogaster ( 16 ) were compared with females from control lines. Females from all five selected lines more readily accepted the encapsulating host species for oviposition when offered together with a nonencapsulating host species than females from the control lines. We found no evidence for pleiotropic effects and suggest that host selection behaviour evolved parallel to the ability to escape encapsulation in the hosts. Our results also suggest that given the appropriate selection pressures, host selection behaviour can quickly evolve in parasitoids, enabling them to adapt fast to changing circumstances.     

An indirect approach to imply trade-off shapes: population level patterns in resistance suggest a decreasingly costly resistance mechanism in a model insect system

Trade-offs between life history and other traits play a key role in shaping the evolution of individuals. It is well established theoretically that the shapes of trade-off curves are as crucial to the evolutionary outcome as their strengths. However, measuring the shape of these relationships directly is often impractical. Here we use an indirect approach that examines the patterns seen within a population and then use theory to infer the shape of the trade-off curve. Using a bioassay we found that most individuals had either high susceptibility or relatively high resistance to a microparasite in a lepidopteran host population. According to general theory, this type of pattern in resistance would be most likely with a deceleratingly costly impact on fitness of increasing resistance. The implications and generality of the approach are discussed, along with the implications of the results to our understanding of the nature of innate resistance to parasites.     

Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience

Although the neural and genetic pathways underlying learning and memory formation seem strikingly similar among species of distant animal phyla, several more subtle inter- and intraspecific differences become evident from studies on model organisms. The true significance of such variation can only be understood when integrating this with information on the ecological relevance. Here, we argue that parasitoid wasps provide an excellent opportunity for multi-disciplinary studies that integrate ultimate and proximate approaches. These insects display interspecific variation in learning rate and memory dynamics that reflects natural variation in a daunting foraging task that largely determines their fitness: finding the inconspicuous hosts to which they will assign their offspring to develop. We review bioassays used for oviposition learning, the ecological factors that are considered to underlie the observed differences in learning rate and memory dynamics, and the opportunities for convergence of ecology and neuroscience that are offered by using parasitoid wasps as model species. We advocate that variation in learning and memory traits has evolved to suit an insect's lifestyle within its ecological niche.     

Seasonal trade-off between starvation resistance and cold resistance in temperate wild-caught Drosophila simulans

Abstract  Selection experiments with Drosophila have revealed a possible evolutionary trade-off between cold resistance and starvation resistance that may be controlled by lipid metabolism. To test this trade-off in naturally occurring Drosophila simulans populations, flies were simultaneously collected from two temperate locales experiencing contrasting seasons. Flies from a tropical locale served as a control. Cold coma recovery, starvation resistance and lipid proportion were assayed on adult males and females from each locale. Compared with the summer-collected flies from Canberra, the winter-collected flies from San Diego recovered from cold coma more quickly, were less starvation resistant and had lower lipid levels. These results support an evolutionary trade-off between cold resistance and starvation resistance. Combined, these data also suggest that differences in lipid metabolism may be an underlying mechanism for this trade-off.     

Selection for adult desiccation resistance in Drosophila melanogaster: fitness components, larval resistance and stress correlations

In previous experiments we found that Drosophila melanogaster lines selected for increased adult desiccation resistance had increased resistance to other environmental stresses at the adult stage including starvation, intense ⁶⁰Co-γ radiation and a toxic ethanol level. In further studies on these lines, we now show that selection did not alter resistance to desiccation and ethanol at the larval stage. As well as having a lower early fecundity, selected lines showed increased adult male longevity and increased viability at high larval densities compared with control lines. There were no changes in development time or mating success. The increased male longevity is consistent with the reduced metabolic rate of the selected lines.
A genetic correlation between resistance to different stresses was confirmed by an analysis of isofemale lines derived from a population founded by flies from a stress-resistant line and an unselected line. The results are consistent with the existence of genes segregating in natural populations conferring increased general stress resistance.     

Evidence for a trade-off between translational efficiency and splicing regulation in determining synonymous codon usage in Drosophila melanogaster

In Drosophila melanogaster, synonymous codons corresponding to the most abundant cognate tRNAs are used more frequently, especially in highly expressed genes. Increased use of such "optimal" codons is considered an adaptation for translational efficiency. Need it always be the case that selection should favor the use of a translationally optimal codon? Here, we investigate one possible confounding factor, namely, the need to specify information in exons necessary to enable correct splicing. As expected from such a model, in Drosophila many codons show different usage near intron-exon boundaries versus exon core regions. However, this finding is in principle also consistent with Hill-Robertson effects modulating usage of translationally optimal codons. However, several results support the splice model over the translational selection model: 1) the trends in codon usage are strikingly similar to those in mammals in which codon usage near boundaries correlates with abundance in exonic splice enhancers (ESEs), 2) codons preferred near boundaries tend to be enriched for A and avoid C (conversely those avoided near boundaries prefer C rather than A), as expected were ESEs involved, and 3) codons preferred near boundaries are typically not translationally optimal. We conclude that usage of translationally optimal codons usage is compromised in the vicinity of splice junctions in intron-containing genes, to the effect that we observe higher levels of usage of translationally optimal codons at the center of exons. On the gene level, however, controlling for known correlates of codon bias, the impact on codon usage patterns is quantitatively small. These results have implications for inferring aspects of the mechanism of splicing given nothing more than a well-annotated genome.     

Evolution of starvation resistance in Drosophila melanogaster: measurement of direct and correlated responses to artificial selection

Laboratory selection for resistance to starvation has been conducted under relatively controlled conditions to investigate direct and correlated responses to artificial selection. With regard to starvation resistance, there are three physiological routes by which the trait can evolve: resource accumulation, energy conservation and starvation tolerance. A majority of energetic compounds and macromolecules including triglycerides, trehalose and other sugars, and soluble protein increased in abundance as a result of selection. Movement was additionally investigated with selected males moving less than control males and selected females exhibiting a similar response to selection. Results obtained from this study supported two of the possible evolutionary mechanisms for adaptation to starvation: energy compound storage and conservation. If the response to selection is based on an evolutionarily conserved pattern of genetic correlations (elevated lipid, elevated sugars and reduced movement), then the response to selection is medically relevant and the genetic architecture should be investigated in depth.     

Automated analysis of courtship suppression learning and memory in Drosophila melanogaster

Study of the fruit fly, Drosophila melanogaster, has yielded important insights into the underlying molecular mechanisms of learning and memory. Courtship conditioning is a well-established behavioral assay used to study Drosophila learning and memory. Here, we describe the development of software to analyze courtship suppression assay data that correctly identifies normal or abnormal learning and memory traits of individual flies. Development of this automated analysis software will significantly enhance our ability to use this assay in large-scale genetic screens and disease modeling. The software increases the consistency, objectivity, and types of data generated.     

The association between malathion resistance and acetylcholinesterase in Drosophila melanogaster

The relationship between the 50% survival time for flies feeding on a malathion-containing medium and the activity of acetylcholinesterase (AChE) was determined for 15 isofemale lines of Drosophila melanogaster. A significant correlation was found (r=0.28, P<0.05), with more resistant lines tending to have a lower level of AChE activity. An association between AChE and malathion resistance was also observed in a selection experiment. The AChE activity decreased in two of two populations selected for malathion resistance. AChE from these populations was altered in kinetic parameters (measured in crude head extracts) and electrophoretic mobility. Although the resistant AChE had a lower activity (V _m) on either a per milligram protein or a per individual basis, its apparent K _m for acetylthiocholine was lower than that of susceptible AChE. Recombination mapping of both low activity and fast electrophoretic mobility localized these traits to the region of the structural locus (Ace) on the third chromosome. The AChE activity of flies heterozygous for a variety of Ace lesions (kindly provided by Dr. W. M. Gelbart) was consistent with this location. The changes in AChE were suggested to have been caused by selection of alleles at the Ace locus.This work was supported by NSERC Grants A5857, G0183, and A0629.     

Antagonistic selection between adult thorax and wing size in field released Drosophila melanogaster independent of thermal conditions

Attempts to explain size variation in Drosophila and other small insects often focus on the larval stage and association between development time and size, but patterns are also influenced by direct selection on size-related traits in the adults. Here we use multiple field releases of Drosophila melanogaster to test the association between size and one component of field fitness, the ability of Drosophila to locate resources for feeding and breeding. We find antagonistic selection between wing length and thorax length in both males and females, such that capture at baits is higher for flies with relatively larger thorax lengths and smaller wings. However flies with large wings relative to thoraces disperse further as reflected in the longer distances moved to baits. These patterns did not depend strongly on weather conditions, suggesting that selection on adult size is at least partly independent of temperature. Antagonistic selection between size traits can generate changes in size along gradients if the distribution of resources in the environment varies and selects for different dispersal patterns, particularly as dispersal is relatively higher under warmer conditions.     

Autosomal variation for male body size and sperm competition phenotypes is uncorrelated in Drosophila melanogaster

Correlations between male body size and phenotypes impacting post-copulatory sexual selection are commonly observed during the manipulation of male body size by environmental rearing conditions. Here, we control for environmental influences and test for genetic correlations between natural variation in male body size and phenotypes affecting post-copulatory sexual selection in Drosophila melanogaster. Dry weights of virgin males from 90 second-chromosome and 88 third-chromosome substitution lines were measured. Highly significant line effects (p<0.001) documented a genetic basis to variation in male body size. No significant correlations were identified between male body size and the components of sperm competitive ability. These results suggest that natural autosomal variation for male body size has little impact on post-copulatory sexual selection. If genetic correlations exist between male body size and post-copulatory sexual selection then variation in the sex chromosomes are likely candidates, as might be expected if sexually antagonistic coevolution was responsible.     

Response of fluctuating and directional asymmetry to selection on wing shape in Drosophila melanogaster

We tested whether directional selection on an index-based wing character in Drosophila melanogaster affected developmental stability and patterns of directional asymmetry. We selected for both an increase (up selection) and a decrease (down selection) of the index value on the left wing and compared patterns of fluctuating and directional asymmetry in the selection index and other wing traits across selection lines. Changes in fluctuating asymmetry across selection lines were predominantly small, but we observed a tendency for fluctuating asymmetry to decrease in the up-selected lines in both replicates. Because changes in fluctuating asymmetry depended on the direction of selection, and were not related to changes in trait size, these results fail to support existing hypotheses linking directional selection and developmental stability. Selection also produced a pattern of directional asymmetry that was similar in all selected lines whatever the direction of selection. This result may be interpreted as a release of genetic variance in directional asymmetry under selection.     

Competitiveness and life‐history characteristics of Daphnia with respect to susceptibility to a bacterial pathogen

Costs of resistance, i.e. trade‐offs between resistance to parasites or pathogens and other fitness components, may prevent the fixation of resistant genotypes and therefore explain the maintenance of genetic polymorphism for resistance in the wild. Using two approaches, the cost of resistance to a sterilizing bacterial pathogen were tested for in the crustacean Daphnia magna. First, groups of susceptible and resistant hosts from each of four natural populations were compared in terms of their life‐history characteristics. Secondly, we examined the competitiveness of nine clones from one population for which more detailed information on genetic variation for resistance was known. In no case did the results show that competitiveness or life history characteristics of resistant Daphnia systematically differed from susceptible ones. These results suggest that costs of resistance are unlikely to explain the maintenance of genetic variation in D. magna populations. We discuss methods for measuring fitness and speculate on which genetic models of host‐parasite co‐evolution may apply to the Daphnia‐microparasite system.