N. G. Prasad

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.

What have two decades of laboratory life-history evolution studies onDrosophila melanogaster taught us?

A series of laboratory selection experiments onDrosophila melanogaster over the past two decades has provided insights into the specifics of life-history tradeoffs in the species and greatly refined our understanding of how ecology and genetics interact in life-history evolution. Much of what has been learnt from these studies about the subtlety of the microevolutionary process also has significant implications for experimental design and inference in organismal biology beyond life-history evolution, as well as for studies of evolution in the wild. Here we review work on the ecology and evolution of life-histories in laboratory populations ofD. melanogaster, emphasizing how environmental effects on life-history-related traits can influence evolutionary change. We discuss life-history tradeoffs—many unexpected—revealed by selection experiments, and also highlight recent work that underscores the importance to life-history evolution of cross-generation and cross-life-stage effects and interactions, sexual antagonism and sexual dimorphism, population dynamics, and the possible role of biological clocks in timing life-history events. Finally, we discuss some of the limitations of typical selection experiments, and how these limitations might be transcended in the future by a combination of more elaborate and realistic selection experiments, developmental evolutionary biology, and the emerging discipline of phenomics.

CORRELATED RESPONSES TO SELECTION FOR FASTER DEVELOPMENT AND EARLY REPRODUCTION IN DROSOPHILA: THE EVOLUTION OF LARVAL TRAITS

Abstract.— Studies on selection for faster development in Drosophila have typically focused on the trade‐offs among development time, adult weight, and adult life span. Relatively less attention has been paid to the evolution of preadult life stages and behaviors in response to such selection. We have earlier reported that four laboratory populations of D. melanogaster selected for faster development and early reproduction, relative to control populations, showed considerably reduced preadult development time and survivorship, dry weight at eclosion, and larval growth rates. Here we study the larval phase of these populations in greater detail. We show here that the reduction in development time after about 50 generations of selection is due to reduced duration of the first and third larval instars and the pupal stage, whereas the duration of the second larval instar has not changed. About 90% of the preadult mortality in the selected populations is due to larval mortality. The third instar larvae, pupae, and freshly eclosed adults of the selected populations weigh significantly less than controls, and this difference appears during the third larval instar. Thereafter, percentage weight loss during the pupal stage does not differ between selected and control populations. The minimum amount of time a larva must feed to subsequently complete development is lower in the selected populations, which also exhibit a syndrome of reduced energy expenditure through reduction in larval feeding rate, larval digging and foraging activity, and pupation height. Comparison of these results with those observed earlier in populations selected for adaptation to larval crowding and faster development under a different protocol from ours reveal differences in the evolved traits that suggest that the responses to selection for faster development are greatly affected by the larval density at which selection acts and on details of the selection pressures acting on the timing of reproduction.

Evolution of reduced pre-adult viability and larval growth rate in laboratory populations of Drosophila melanogaster selected for shorter development time.

Four large (n > 1000) populations of Drosophila melanogaster, derived from control populations maintained on a 3 week discrete generation cycle, were subjected to selection for fast development and early reproduction. Egg to eclosion survivorship and development time and dry weight at eclosion were monitored every 10 generations. Over 70 generations of selection, development time in the selected populations decreased by approximately 36 h relative to controls, a 20% decline. The difference in male and female development time was also reduced in the selected populations. Flies from the selected populations were increasingly lighter at eclosion than controls, with the reduction in dry weight at eclosion over 70 generations of selection being approximately 45% in males and 39% in females. Larval growth rate (dry weight at eclosion/development time) was also reduced in the selected lines over 70 generations, relative to controls, by approximately 32% in males and 24% in females. However, part of this relative reduction was due to an increase in growth rate of the controls populations, presumably an expression of adaptation to conditions in our laboratory. After 50 generations of selection had elapsed, a considerable and increasing pre-adult viability cost to faster development became apparent, with viability in the selected populations being about 22% less than that of controls at generation 70 of selection.

Variation in adult life history and stress resistance across five species of Drosophila.

Dry weight at eclosion, adult lifespan, lifetime fecundity, lipid and carbohydrate content at eclosion, and starvation and desiccation resistance at eclosion were assayed on a long-term laboratory population ofDrosophila melanogaster, and one recently wild-caught population each of four other species ofDrosophila, two from themelanogaster and two from theimmigrans species group. The relationships among trait means across the five species did not conform to expectations based on correlations among these traits inferred from selection studies onD. melanogaster. In particular, the expected positive relationships between fecundity and size/lipid content, lipid content and starvation resistance, carbohydrate (glycogen) content and desiccation resistance, and the expected negative relationship between lifespan and fecundity were not observed. Most traits were strongly positively correlated between sexes across species, except for fractional lipid content and starvation resistance per microgram lipid. For most traits, there was evidence for significant sexual dimorphism but the degree of dimorphism did not vary across species except in the case of adult lifespan, starvation resistance per microgram lipid, and desiccation resistance per microgram carbohydrate. Overall,D. nasuta nasuta andD. sulfurigaster neonasuta (immigrans group) were heavier at eclosion than themelanogaster group species, and tended to have somewhat higher absolute lipid content and starvation resistance. Yet, these twoimmigrans group species were shorter-lived and had lower average daily fecundity than themelanogaster group species. The smallest species,D. malerkotliana (melanogaster group), had relatively high daily fecundity, intermediate lifespan and high fractional lipid content, especially in females.D. ananassae (melanogaster group) had the highest absolute and fractional carbohydrate content, but its desiccation resistance per microgram carbohydrate was the lowest among the five species. In terms of overall performance, the laboratory population ofD. melanogaster was clearly superior, under laboratory conditions, to the other four species if adult lifespan, lifetime fecundity, average daily fecundity, and absolute starvation and desiccation resistance are considered. This finding is contrary to several recent reports of substantially higher adult lifespan and stress resistance in recently wild-caught flies, relative to flies maintained for a long time in discretegeneration laboratory cultures. Possible explanations for these apparent anomalies are discussed in the context of the differing selection pressures likely to be experienced byDrosophila populations in laboratory versus wild environments.

K-selection, α-selection, effectiveness, and tolerance in competition: Density-dependent selection revisited

In theDrosophila literature, selection for faster development and selection for adapting to high density are often confounded, leading, for example, to the expectation that selection for faster development should also lead to higher competitive ability. At the same time, results from experimental studies on evolution at high density do not agree with many of the predictions from classical density-dependent selection theory. We put together a number of theoretical and empirical results from the literature, and some new experimental results onDrosophila populations successfully subjected to selection for faster development, to argue for a broader interpretation of density-dependent selection. We show that incorporating notions of α-selection, and the division of competitive ability into effectiveness and tolerance components, into the concept of density-dependent selection yields a formulation that allows for a better understanding of the empirical results. We also use this broader formulation to predict that selection for faster development inDrosophila should, in fact, lead to the correlated evolution of decreased competitive ability, even though it does lead to the evolution of greater efficiency and higher population growth rates at high density when in monotypic culture.

The evolution of population stability as a by-product of life-history evolution

Proposed mechanisms for the evolution of population stability include group selection through longterm persistence, individual selection acting directly on stability determining the demographic parameters, and the evolution of stability as a by-product of life-history evolution. None of these hypotheses currently has clear empirical support. Using two sets of Drosophila melanogaster populations, we provide experimental evidence of stability evolving as a correlated response to selection on traits not directly related to demography. Four populations (FEJs) were selected for faster development and early reproduction for 125 generations, and the other four (JBs) were ancestral controls. All FEJ and JB populations have been maintained on discrete generations at moderate density, thus eliminating differential selection on stability determining demographic parameters. We derived eight small populations from each FEJ and JB population, and subjected four small populations each to either stabilizing or destabilizing food regimes. Census data on these 64 small populations over 20 generations clearly showed that the FEJ populations have significantly less temporal fluctuations in their numbers in both food regimes compared to their controls. This greater stability of the FEJ populations is probably a by-product of the evolution of reduced fecundity and pre-adult survivorship, as a correlated response to selection for rapid development.

Sexual conflict in plants

.2003). Sexualconflictcanfurtherbedividedinto two components: interlocus and intralocus conflict.Interlocus conflict designates the form of conflict inwhich the expression of a sex-limited locus results in a netfitness benefitto thesexexpressingit anda fitness costto theother sex, usually through direct reproductive interactions.Thisleadstostrongselectionforacounteractingmechanism,usually governed by a different locus, in the other sex. Theresult is rapid evolution of the loci involved and open-endedcycles of antagonistic coevolution between the sexes (Hol-land and Rice 1998).Intralocus conflict involves traits (and hence alleles) thatareexpressedinbothsexes,buthavedifferentoptimaineachsex (Rice and Chippindale 2001), thereby creating divergentselection pressures across sexes. However, because malesand females of the same species share the same genome, ge-netic correlations for the same trait between sexes impedethe independent evolution of the trait within each sex, lead-ing to a conflict between the sexes. A part of the conflict canpotentially be resolved by evolution of sex-limited gene ex-pression leading to sexual dimorphism. The unresolved partof the conflict maintains each sex away from its optimum,creating a gender load.Sexual conflict has mainly been investigated in animalsand the interlocus component has been the principal focusof past studies. However, among the very large diversityof reproductive systems of plants, dioecy gathers all the

Sexual conflict and environmental change: trade-offs within and between the sexes during the evolution of desiccation resistance

Intralocus sexual conflict occurs when males and females experience sex-specific selection on a shared genome. With several notable exceptions, intralocus sexual conflict has been investigated in constant environments to which the study organisms have had an opportunity to adapt. However, a change in the environment can result in differential or even opposing selection pressures on males and females, creating sexual conflict. We used experimental evolution to explore the interaction between intralocus sexual conflict, sexual dimorphism and environmental variation in Drosophila melanogaster. Six populations were selected for adult desiccation resistance (D), with six matched control populations maintained in parallel (C). After 46 generations, the D populations had increased in survival time under arid conditions by 68% and in body weight by 20% compared to the C populations. The increase in size was the result of both extended development and faster growth rate of D juveniles. Adaptation to the stress came at a cost in terms of preadult viability and female fecundity. Because males are innately less tolerant of desiccation stress, very few D males survived desiccation-selection; while potentially a windfall for survivors, these conditions mean that most males’ fitness was determined posthumously. We conjectured that selection for early maturation and mating in males was in conflict with selection for survival and later reproduction in females. Consistent with this prediction, the sexes showed different patterns of age-specific desiccation resistance and resource acquisition, and there was a trend towards increasingly female-biased sexual size dimorphism. However, levels of desiccation resistance were unaffected, with D males and females increasing in parallel. Either there is a strong positive genetic correlation between the sexes that limits independent evolution of desiccation resistance, or fitness pay-offs from the strategy of riding out the stress bout are great enough to sustain concordant selection on the two sexes. We discuss the forces that mould fitness in males under a regimen where trade-offs between survival and reproduction may be considerable.

Correlates of sexual dimorphism for dry weight and development time in five species of Drosophila

Pre-adult development time, dry weight at eclosion, and daily fecundity over the first 10 days of adult life were measured in five species of Drosophila from the melanogaster and immigrans species groups. Overall, the three species of the melanogaster group (D. melanogaster, D. ananassae, D. malerkotliana) developed faster, were lighter at eclosion, and produced more eggs per unit weight at eclosion than the two species of the immigrans group (D. n. nasuta, D. sulfurigaster neonasuta). The degree of sexual dimorphism in dry weight was greater than that in development time, but did not vary significantly among species, and was not correlated with fecundity, contrary to expectations that sexual selection for increased fecundity drives sexual size dimorphism in Drosophila. The degree of dimorphism in development time was significantly correlated with dry weight and fecundity, with lighter species tending to be more dimorphic for development time as well as more fecund, both in absolute terms and in terms of fecundity per unit weight. The results suggest that our understanding of the evolutionary forces maintaining sexual size dimorphism in Drosophila will probably benefit from more detailed studies on the correlates of sexual dimorphism within and among Drosophila species, and on the shape of reaction norms for the degree of sexual dimorphism across different levels of ecologically relevant environmental variables.