Adam K. Chippindale

Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction

While it is commonplace for biologists to use the response to environmental manipulation as a guide to evolutionary responses to selection, the relationship between phenotypic plasticity and genetic change is not generally well‐established. The life‐histories of laboratory Drosophila populations are among the few experimental systems which simultaneously afford information on phenotypic plasticity and evolutionary trajectories. We employed a combination of two replicated selectively differentiated stocks (postponed aging stocks and their controls; 10 populations in total) and two different environmental manipulations (nutrition and mating) to explore the empirical relationship between phenotypic plasticity and evolutionary trajectories. While there are a number of parallels between the results obtained using these two approaches, there are important differences. In particular, as the detail of the biological characterization of either type of response increases, so their disparities multiply. Nonetheless, the combination of environmental manipulation with evolutionary divergence provides valuable information about the biological connections between life‐history, caloric reserves, and reproductive physiology in Drososphila.

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.

Metabolic Reserves and Evolved Stress Resistance in Drosophila melanogaster

We have examined starvation and desiccation resistance in 43 outbred populations of Drosophila melanogaster that have diverged from a common ancestral population as a result of a variety of defined selection protocols. The populations differ up to 8.5‐fold in desiccation resistance and up to 10fold in starvation resistance. We used these populations to search for evolved physiological changes that might explain the differences in stress resistance. We examined two hypotheses for increased stress resistance that had been proposed previously in the literature: (1) that increments in starvation resistance are principally the result of differential lipid accumulation, and (2) that changes in glycogen accumulation play a role in evolved increases in resistance to desiccation stress. By quantifying desiccation resistance, starvation resistance, lipid content, and carbohydrate content in each of our populations of flies, we were able to demonstrate strong correlations between the capacity of the flies to resist starvation and the quantity of lipid or carbohydrate that the flies had stored. The strongest correlation (R2 = 0.99) was observed when the total energy content of both the lipid and carbohydrate stores was regressed against starvation resistance. These results demonstrate that the flies responded to selection for starvation resistance through a genetically determined increase in both lipid and carbohydrate storage. Similar analyses of the correlation between lipid storage or total energy storage and desiccation resistance revealed no significant correlations. Carbohydrate storage was significantly correlated with desiccation resistance in female but not in male flies. These results suggest that different forms of stress are resisted with distinct physiological mechanisms and that the evolutionary response of the flies to stress selection is specific to the stress imposed.

Intralocus Sexual Conflict Diminishes the Benefits of Sexual Selection

Evolution based on the benefits of acquiring “good genes” in sexual selection is only plausible with the reliable transmission of genetic quality from one generation to the next. Accumulating evidence suggests that sexually antagonistic (SA) genes with opposite effects on Darwinian fitness when expressed in the two different sexes may be common in animals and plants. These SA genes should weaken the potential indirect genetic benefits of sexual selection by reducing the fitness of opposite-sex progeny from high-fitness parents. Here we use hemiclonal analysis in the fruit fly, Drosophila melanogaster, to directly measure the inheritance of fitness across generations, over the entire genome. We show that any potential genetic benefits of sexual selection in this system are not merely weakened, but completely reversed over one generation because high-fitness males produce low-fitness daughters and high-fitness mothers produce low-fitness sons. Moreover, male fitness was not inherited by sons, consistent with both theory and recent evidence connecting this form of SA variation with the X chromosome. This inheritance pattern may help to explain how genetic variation for fitness is sustained despite strong sexual selection, and why the ZW sex chromosome system found in birds and butterflies appears to foster the evolution of extreme secondary sexual characters in males.

RESOURCE ACQUISITION AND THE EVOLUTION OF STRESS RESISTANCE IN DROSOPHILA MELANOGASTER

Resistance to environmental stress is one of the most important forces molding the distribution and abundance of species. We investigated the evolution of desiccation stress resistance using 20 outbred Drosophila melanogaster populations directly selected in the laboratory for adult desiccation resistance (D), postponed senescence (O), and their respective controls (C and B). Both aging and desiccation selection increased desiccation resistance relative to their controls, creating a spectrum of desiccation resistance levels across selection treatments. We employed an integrative approach, merging data on the life histories of these populations with a detailed physiology of water balance. The physiological basis of desiccation resistance may be mechanisms enhancing either resource conservation or resource acquisition and allocation. Desiccation‐resistant populations had increased water and carbohydrate stores, and showed age‐specific patterns of desiccation resistance consistent with the resource accumulation mechanism. A significant proportion of the resources relevant to resistance of the stress were accumulated in the larval stage. Males and females of desiccation‐selected lines exhibited distinctly different patterns of desiccation resistance and resource acquisition, in a manner suggesting intersexual antagonism in the evolution of stress resistance. Preadult viability of stress‐selected populations was lower than that of controls, and development was slowed. Our results suggest that there is a cost to preadult resource acquisition, pointing out a complex trade‐off architecture involving characters distributed across distinct life‐cycle stages.

LONG-TERM LABORATORY EVOLUTION OF A GENETIC LIFE-HISTORY TRADE-OFF IN DROSOPHILA MELANOGASTER. 1. THE ROLE OF GENOTYPE-BY-ENVIRONMENT INTERACTION

Trade‐offs among life‐history traits are often thought to constrain the evolution of populations. Here we report the disappearance of a trade‐off between early fecundity on the one hand, and late‐life fecundity, starvation resistance, and longevity on the other, over 10 yr of laboratory selection for late‐life reproduction. Whereas the selected populations showed an initial depression in early‐life fecundity, they later converged upon the controls and then surpassed them. The evolutionary loss of the trade‐off among life‐history traits is considered attributable to the following factors: (1) the existence of differences in the culture regimes of the short‐ and long‐generation populations other than the demographic differences deliberately imposed; (2) adaptation of one or both of these sets of populations to the unique aspects of their culture regimes; (3) the existence of an among‐environment trade‐off in the expression of early fecundity in the two culture regimes, as reflected in assays that mimic those regimes. The trade‐off between early and late‐life reproductive success, as manifest among divergently selected populations, is apparent or not depending on the assay environment. This demonstration that strong genotype‐by‐environment interactions can obscure a fundamental trade‐off points to the importance of controlling all aspects of the culture regime of experimental populations and the difficulty of doing so even in the laboratory.

An evolutionary cost of separate genders revealed by male-limited evolution.

Theory predicts that intralocus sexual conflict can constrain the evolution of sexual dimorphism, preventing each sex from independently maximizing its fitness. To test this idea, we limited genome‐wide gene expression to males in four replicate Drosophila melanogaster populations, removing female‐specific selection. Over 25 generations, male fitness increased markedly, as sexually dimorphic traits evolved in the male direction. When male‐evolved genomes were expressed in females, their fitness displayed a nearly symmetrical decrease. These results suggest that intralocus conflict strongly limits sex‐specific adaptation, promoting the maintenance of genetic variation for fitness. Populations may carry a heavy genetic load as a result of selection for separate genders.

EXPERIMENTAL EVOLUTION OF ACCELERATED DEVELOPMENT IN DROSOPHILA. 1. DEVELOPMENTAL SPEED AND LARVAL SURVIVAL

Developmental time is a trait of great relevance to fitness in all organisms. In holometabolous species that occupy ephemeral habitat, like Drosophila melanogaster, the impact of developmental time upon fitness is further exaggerated. We explored the trade‐offs surrounding developmental time by selecting 10 independent populations from two distantly related selection treatments (CB1‐5 and CO1‐5) for faster development. After 125 generations, the resulting accelerated populations (ACB1‐5 and ACO1‐5) displayed net selection responses for development time of ‐33.4 hours (or 15%) for ACB and ‐38.6 hours (or 17%) for ACO. Since most of the change in egg‐to‐adult developmental time was accounted for by changes in larval duration, the “accelerated” larvae were estimated to develop 25‐30% faster than their control/ancestor populations. The responses of ACB and ACO lines were remarkably parallel, despite being founded from populations evolved independently for more than 300 generations. On average, these “A” populations developed from egg to adult in less than eight days and produced fertile eggs less than 24 hours after emerging. Accelerated populations showed no change in larval feeding rate, but a reduction in pupation height, the latter being a trait relating to larval energetic expenditure in wandering prior to pupation. This experiment demonstrates the existence of a negative evolutionary correlation between preadult developmental time and viability, as accelerated populations experienced a severe cost in preadult survivorship. In the final assay generation, viability of accelerated treatments had declined by more than 10%, on average. A diallel cross demonstrated that the loss of viability in the ACO lines was not due to inbreeding depression. These results suggest the existence of a rapid development syndrome, in which the fitness benefits of fast development are balanced by fitness costs resulting from reduced preadult survivorship, marginal larval storage of metabolites, and reduced adult size.

BREAKDOWN IN CORRELATIONS DURING LABORATORY EVOLUTION. I. COMPARATIVE ANALYSES OF DROSOPHILA POPULATIONS

Abstract We provide evidence from comparisons of populations of Drosophila that evolutionary correlations between longevity and stress resistance break down over the course of laboratory evolution. Using 15 distinct evolutionary regimes, we created 75 populations that were differentiated for early fecundity, longevity, starvation resistance, desiccation resistance, and developmental time. In earlier experiments, selection for postponed aging produced increases in stress resistance, whereas selection for increased stress resistance produced increases in longevity. Direct estimates of correlations also indicated an antagonistic relationship between early fecundity on one hand and longevity or stress resistance on the other. Laboratory evolution of extreme values of stress resistance, however, led to a breakdown in these evolutionary relationships. There was no evidence that these significant changes in correlation resulted from genotype‐by‐environment interactions or inbreeding. These findings suggest that correlations between functional characters are not necessarily durable features of a species, and that short‐term evolutionary responses cannot be extrapolated reliably to longer‐term evolutionary patterns.

The evolution of hybrid infertility: Perpetual coevolution between gender-specific and sexually antagonistic genes

A new hypothesis is proposed for the rapid evolution of postzygotic reproductive isolation via hybrid infertility. The hypothesis is motivated by two lines of experimental research from Drosophila melanogaster that demonstrate that sexually antagonistic fitness variation is abundant and that epistatic fitness variation on the Y chromosome is common. The hypothesis states that the expression of sexually antagonistic genes leads to a ‘gender-load’ in each sex. In response, gender-limited reproductive genes are selected to ameliorate, through pleiotropy, the expression of sexually antagonistic genes. Chronic coevolution between gender-limited genes and gender-unlimited sexually antagonistic genes causes rapid divergence of reproductive proteins among allopatric populations, ultimately leading to hybrid infertility.