Mutation accumulation affects male virility in Drosophila selected for later reproduction

An intensive study of longevity, female fecundity, and male reproductive behavior in Drosophila melanogaster was undertaken in order to establish whether late-life fitness characters in short-lived populations might be affected by the increase in deleterious alleles due to random genetic drift. We also sought to determine whether selection for late-life fertility could eliminate alleles that produce a decline in later fitness components in short-lived populations, as predicted by the mutation accumulation hypothesis for the evolution of aging. These experiments employed long-lived (O) populations, short-lived (B) populations, and hybrids made from crosses of independent lines from within the O and B populations. No detectable longevity differences were seen between hybrid B males and females and purebred B males and females. Reproduction in aged B purebred females was significantly less than in hybrid females at 3 wk of age only. A full diallel cross of the five replicate B lines showed a steady increase in hybrid male reproductive performance after the first week of adult life, relative to the parental lines. A full diallel cross of the five replicate O lines revealed no significant increase in hybrid O age-specific male reproductive success compared with the purebred O lines when assayed over the first 5 wk of adult life. The results on male reproductive behavior are consistent with the idea that relaxed age-specific selection in the B populations has been accompanied by an increase in deleterious, recessive traits that exhibit age-specific expression. Consequently, we conclude that a mutation accumulation process has been at least partly responsible for the age-specific decline in male B virility relative to that of the O populations.     

Reproductive and post‐reproductive life history of wild‐caught Drosophila melanogaster under laboratory conditions

The life history of the fruit fly (Drosophila melanogaster) is well understood, but fitness components are rarely measured by following single individuals over their lifetime, thereby limiting insights into lifetime reproductive success, reproductive senescence and post‐reproductive lifespan. Moreover, most studies have examined long‐established laboratory strains rather than freshly caught individuals and may thus be confounded by adaptation to laboratory culture, inbreeding or mutation accumulation. Here, we have followed the life histories of individual females from three recently caught, non‐laboratory‐adapted wild populations of D. melanogaster. Populations varied in a number of life‐history traits, including ovariole number, fecundity, hatchability and lifespan. To describe individual patterns of age‐specific fecundity, we developed a new model that allowed us to distinguish four phases during a female's life: a phase of reproductive maturation, followed by a period of linear and then exponential decline in fecundity and, finally, a post‐ovipository period. Individual females exhibited clear‐cut fecundity peaks, which contrasts with previous analyses, and post‐peak levels of fecundity declined independently of how long females lived. Notably, females had a pronounced post‐reproductive lifespan, which on average made up 40% of total lifespan. Post‐reproductive lifespan did not differ among populations and was not correlated with reproductive fitness components, supporting the hypothesis that this period is a highly variable, random ‘add‐on’ at the end of reproductive life rather than a correlate of selection on reproductive fitness. Most life‐history traits were positively correlated, a pattern that might be due to genotype by environment interactions when wild flies are brought into a novel laboratory environment but that is unlikely explained by inbreeding or positive mutational covariance caused by mutation accumulation.     

Evolution of late-life mortality in Drosophila melanogaster

Abstract.— Aging appears to cease at late ages, when mortality rates roughly plateau in large-scale demographic studies. This anomalous plateau in late-life mortality has been explained theoretically in two ways: (1) as a strictly demographic result of heterogeneity in life-long robustness between individuals within cohorts, and (2) as an evolutionary result of the plateau in the force of natural selection after the end of reproduction. Here we test the latter theory using cohorts of Drosophila melanogaster cultured with different ages of reproduction for many generations. We show in two independent comparisons that populations that evolve with early truncation of reproduction exhibit earlier onset of mortality-rate plateaus, in conformity with evolutionary theory. In addition, we test two population genetic mechanisms that may be involved in the evolution of late-life mortality: mutation accumulation and antagonistic pleiotropy. We test mutation accumulation by crossing genetically divergent, yet demographically identical, populations, testing for hybrid vigor between the hybrid and nonhybrid parental populations. We found no difference between the hybrid and nonhybrid populations in late-life mortality rates, a result that does not support mutation accumulation as a genetic mechanism for late-life mortality, assuming mutations act recessively. Finally, we test antagonistic pleiotropy by returning replicate populations to a much earlier age of last reproduction for a short evolutionary time, testing for a rapid indirect response of late-life mortality rates. The positive results from this test support antagonistic pleiotropy as a genetic mechanism for the evolution of late-life mortality. Together these experiments comprise the first corroborations of the evolutionary theory of late-life mortality.     

Patterns of male fitness conform to predictions of evolutionary models of late life

We studied lifetime male virility, a male fitness component, in five populations of Drosophila melanogaster. Virility was measured as the number of females, of eight total, that a male could fertilize in 24 h. Individual males were measured at weekly intervals until they died. Virility declined in an approximately linear fashion for the first 3 weeks of adult life. It then stayed low but relatively constant for another 3 weeks, exhibiting a clear plateau. These observations are consistent with the evolutionary theories of late life. The results were not consistent with a simple heterogeneity theory of late life. This is the first demonstration of a late-life plateau for a male fitness component. We also found that the virility of males that were within 7 days of death was significantly lower than that of similarly aged males that were not about to die. This rapid deterioration of virility prior to death, or death spiral, is similar to a decline in fecundity that we had previously documented.     

The Effects of Spontaneous Mutation on Quantitative Traits. I. Variances and Covariances of Life History Traits

We have accumulated spontaneous mutations in the absence of natural selection in Drosophila melanogaster by backcrossing 200 heterozygous replicates of a single high fitness second chromosome to a balancer stock for 44 generations. At generations 33 and 44 of accumulation, we extracted samples of chromosomes and assayed their homozygous performance for female fecundity early and late in adult life, male and female longevity, male mating ability early and late in adult life, productivity (a measure of fecundity times viability) and body weight. The variance among lines increased significantly for all traits except male mating ability and weight. The rate of increase in variance was similar to that found in previous studies of egg-to-adult viability, when calculated relative to trait means. The mutational correlations among traits were all strongly positive. Many correlations were significantly different from 0, while none was significantly different from 1. These data suggest that the mutation-accumulation hypothesis is not a sufficient explanation for the evolution of senescence in D. melanogaster. Mutation-selection balance does seem adequate to explain a substantial proportion of the additive genetic variance for fecundity and longevity.     

Sex differences in relationships between habitat use and reproductive performance in Soay sheep (Ovis aries)

The role of habitat use in generating individual variation in fitness has rarely been examined empirically in natural populations of long‐lived mammals, particularly for both sexes simultaneously. This is the case despite the increase in studies attempting to understand evolutionary change in such populations. Using data from the St. Kilda Soay sheep population, we quantified the association between lifetime reproductive performance (lifetime breeding and reproductive success) and the proportion of the home range covered by a key grass species, H. lanatus, for 490 females and 304 males. Increased H. lanatus cover was associated only with increased female lifetime reproductive success, but increased lifetime breeding success for both sexes, arising through increased male longevity and increased female fecundity. This work suggests that improved understanding of the causes and consequences of fitness differences will likely require us to better account for habitat‐derived individual variation, and to do so for the sexes appropriately.     

Climate‐dependent costs of reproduction: Survival and fecundity costs decline with length of the growing season and summer temperature

Costs of reproduction are expected to vary with environmental conditions thus influencing selection on life‐history traits. Yet, the effects of habitat conditions and climate on trade‐offs among fitness components remain poorly understood. For 2–5 years, we quantified costs of experimentally increased reproduction in two populations (coastal long‐season vs. inland short‐season) of two long‐lived orchids that differ in natural reproductive effort (RE; 30 vs. 75% fruit set). In both species, survival costs were found only at the short‐season site, whereas growth and fecundity costs were evident at both sites, and both survival and fecundity costs declined with increasing growing season length and/or summer temperature. The results suggest that the expression of costs of reproduction depend on the local climate, and that climate warming could result in selection favouring increased RE in both study species.     

Sexual selection on spontaneous mutations strengthens the between‐sex genetic correlation for fitness

A proposed benefit to sexual selection is that it promotes purging of deleterious mutations from populations. For this benefit to be realized, sexual selection, which is usually stronger on males, must purge mutations deleterious to both sexes. Here, we experimentally test the hypothesis that sexual selection on males purges deleterious mutations that affect both male and female fitness. We measured male and female fitness in two panels of spontaneous mutation‐accumulation lines of the fly, Drosophila serrata, each established from a common ancestor. One panel of mutation accumulation lines limited both natural and sexual selection (LS lines), whereas the other panel limited natural selection, but allowed sexual selection to operate (SS lines). Although mutation accumulation caused a significant reduction in male and female fitness in both the LS and SS lines, sexual selection had no detectable effect on the extent of the fitness reduction. Similarly, despite evidence of mutational variance for fitness in males and females of both treatments, sexual selection had no significant impact on the amount of mutational genetic variance for fitness. However, sexual selection did reshape the between‐sex correlation for fitness: significantly strengthening it in the SS lines. After 25 generations, the between‐sex correlation for fitness was positive but considerably less than one in the LS lines, suggesting that, although most mutations had sexually concordant fitness effects, sex‐limited, and/or sex‐biased mutations contributed substantially to the mutational variance. In the SS lines this correlation was strong and could not be distinguished from unity. Individual‐based simulations that mimick the experimental setup reveal two conditions that may drive our results: (1) a modest‐to‐large fraction of mutations have sex‐limited (or highly sex‐biased) fitness effects, and (2) the average fitness effect of sex‐limited mutations is larger than the average fitness effect of mutations that affect both sexes similarly.     

Genetics of Life History in DROSOPHILA MELANOGASTER. II. Exploratory Selection Experiments

Two types of small-scale selection experiments were performed. (1) Artificial selection experiments were performed on age-specific female fecundity. Selection for early fecundity over three generations produced a statistically detectable direct response. There was no detectable indirect response in other life-history characters. Selection for late fecundity over three generations did not produce any detectable direct response. Indirect responses were detected: early egg-laying decreased and longevity increased. (2) Natural selection for late-age fitness components increased late fecundity, female longevity, and the duration of female reproduction, while early fecundity and mean egg-laying rate decreased.     

Artificial selection,pre‐release diet,and gut symbiont inoculation effects on sterile male longevity for area‐wide fruit‐fly management

Longevity is an important life‐history trait for successful and cost‐effective application of the sterile insect technique. Furthermore, it has been shown that females of some species – e.g., Anastrepha ludens (Loew) (Diptera: Tephritidae) – preferentially copulate with ‘old’, sexually experienced males, rather than younger and inexperienced males. Long‐lived sterile males may therefore have greater opportunity to find and mate with wild females than short‐lived males, and be more effective in inducing sterility into wild populations. We explored the feasibility of increasing sterile male lifespan through selection of long‐lived strains and provision of pre‐release diets with added protein, and inoculated with bacterial symbionts recovered from cultures of the gut of wild Anastrepha obliqua (Macquart). Artificial selection for long‐lived A. ludens resulted in a sharp drop of fecundity levels for F1 females. Nevertheless, the cross of long‐lived males with laboratory females produced a female F1 progeny with fecundity levels comparable to those of females in the established colony. However, the male progeny of long‐lived males*laboratory females did not survive in higher proportions than laboratory males. Provision of sugar to A. obliqua adults resulted in increased survival in comparison to adults provided only with water, whereas the addition of protein to sugar‐only diets had no additional effect on longevity. Non‐irradiated males lived longer than irradiated males, and supplying a generic probiotic diet produced no noticeable effect in restoring irradiated male longevity of A. obliqua. We discuss the need to evaluate the time to reach sexual maturity and survival under stress for long‐lived strains, and the inclusion of low amounts of protein and specific beneficial bacteria in pre‐release diets to increase sterile male performance and longevity in the field.     

Heterosis for viability,fecundity, and male fertility in Drosophila melanogaster: comparison of mutational and standing variation.

If genetic variation for fitness traits in natural populations ("standing" variation) is maintained by recurrent mutation, then quantitative-genetic properties of standing variation should resemble those of newly arisen mutations. One well-known property of standing variation for fitness traits is inbreeding depression, with its converse of heterosis or hybrid vigor. We measured heterosis for three fitness traits, pre-adult viability, female fecundity, and male fertility, among a set of inbred Drosophilia melanogaster lines recently derived from the wild, and also among a set of lines that had been allowed to accumulate spontaneous mutations for over 200 generations. The inbred lines but not the mutation-accumulation (MA) lines showed heterosis for pre-adult viability. Both sets of lines showed heterosis for female fecundity, but heterosis for male fertility was weak or absent. Crosses among a subset of the MA lines showed that they were strongly differentiated for male fertility, with the differences inherited in autosomal fashion; the absence of heterosis for male fertility among the MA lines was therefore not caused by an absence of mutations affecting this trait. Crosses among the inbred lines also gave some, albeit equivocal, evidence for male fertility variation. The contrast between the results for female fecundity and those for male fertility suggests that mutations affecting different fitness traits may differ in their average dominance properties, and that such differences may be reflected in properties of standing variation. The strong differentiation among the MA lines in male fertility further suggests that mutations affecting this trait occur at a high rate.     

Early reproductive investment,senescence and lifetime reproductive success in female Asian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early‐life over late‐life reproduction. Studies on natural vertebrate populations show early reproduction may impair later‐life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early‐life reproduction and female age‐specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age‐specific fecundity and offspring survival, but significantly impaired a female's own later‐life survival. Despite the negative effects of early reproduction on late‐life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade‐off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later‐life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi‐)captive breeding programmes of this endangered species.     

Effectiveness of sexual selection in preventing fitness deterioration in bulb mite populations under relaxed natural selection

Under the 'good genes' mechanism of sexual selection (SS), females benefit from mate choice indirectly: their offspring inherit genes of the preferred, high quality fathers. Recent models assume that the genetic variance for male quality is maintained by deleterious mutations. Consequently, SS can be predicted to remove deleterious mutations from populations. We tested this prediction by relaxing selection in populations of the bulb mite, thus increasing their rate of accumulation of deleterious mutation. SS, allowed to operate in half of these populations, did not prevent the fitness decline observed in the other half of the relaxed selection lines. After 11 generations of relaxed selection, female fecundity in lines in which males were allowed to compete for females declined compared with control populations by similar amount as in monogamous lines (17.5 and 14.5%, respectively), whereas other fitness components (viability, longevity, male reproductive success) did not differ significantly between both types of lines and control populations.     

The short‐ and long‐term fitness consequences of natal dispersal in a wild bird population

Dispersal is a key process in population and evolutionary ecology. Individual decisions are affected by fitness consequences of dispersal, but these are difficult to measure in wild populations. A long‐term dataset on a geographically closed bird population, the Mauritius kestrel, offers a rare opportunity to explore fitness consequences. Females dispersed further when the availability of local breeding sites was limited, whereas male dispersal correlated with phenotypic traits. Female but not male fitness was lower when they dispersed longer distances compared to settling close to home. These results suggest a cost of dispersal in females. We found evidence of both short‐ and long‐term fitness consequences of natal dispersal in females, including reduced fecundity in early life and more rapid aging in later life. Taken together, our results indicate that dispersal in early life might shape life history strategies in wild populations.     

MULTIPLE GENETIC MECHANISMS FOR THE EVOLUTION OF SENESCENCE IN DROSOPHILA MELANOGASTER

We present the results of selection experiments designed to distinguish between antagonistic pleiotropy and mutation accumulation, two mechanisms for the evolution of senescence. Reverse selection for early-life fitness was applied to laboratory populations of Drosophila melanogaster that had been previously selected for late-life fitness. These populations also exhibited reduced early-age female fecundity and increased resistance to the stresses of starvation, desiccation, and ethanol, when compared to control populations. Reverse selection was carried out at both uncontrolled, higher larval rearing density and at controlled, lower larval density. In the uncontrolled-density selection lines, early-age female fecundity increased to control-population levels in response to the reintroduction of selection for early-age fitness. Concomitantly, resistance to starvation declined in agreement with previous observations of a negative genetic correlation between these two characters and in accordance with the antagonistic-pleiotropy mechanism. However, resistance to stresses of desiccation and ethanol did not decline in the uncontrolled-density lines during 22 generations of reverse selection for early-life fitness. The latter results provide evidence that mutation accumulation has also played a role in the evolution of senescence in this set of Drosophila populations. No significant response in early-age fecundity or starvation resistance was observed in the controlled-density reverse-selection lines, supporting previous observations that selection on Drosophila life-history characters is critically sensitive to larval rearing density.     

Genetic admixture accelerates invasion via provisioning rapid adaptive evolution

Genetic admixture, the intraspecific hybridization among divergent introduced sources, can immediately facilitate colonization via hybrid vigor and profoundly enhance invasion via contributing novel genetic variation to adaption. As hybrid vigor is short‐lived, provisioning adaptation is anticipated to be the dominant and long‐term profit of genetic admixture, but the evidence for this is rare. We employed the 30 years' geographic‐scale invasion of the salt marsh grass, Spartina alterniflora, as an evolutionary experiment and evaluated the consequences of genetic admixture by combining the reciprocal transplant experiment with quantitative and population genetic surveys. Consistent with the documentation, we found that the invasive populations in China had multiple origins from the southern Atlantic coast and the Gulf of Mexico in the US. Interbreeding among these multiple sources generated a “hybrid swarm” that spread throughout the coast of China. In the northern and mid‐latitude China, natural selection greatly enhanced fecundity, plant height and shoot regeneration compared to the native populations. Furthermore, genetic admixture appeared to have broken the negative correlation between plant height and shoot regeneration, which was genetically‐based in the native range, and have facilitated the evolution of super competitive genotypes in the invasive range. In contrast to the evolved northern and mid‐latitude populations, the southern invasive populations showed slight increase of plant height and shoot regeneration compared to the native populations, possibly reflecting the heterotic effect of the intraspecific hybridization. Therefore, our study suggests a critical role of genetic admixture in accelerating the geographic invasion via provisioning rapid adaptive evolution.     

POLYANDRY INCREASES OFFSPRING FECUNDITY IN THE BULB MITE

Abstract The common occurrence of polyandry continues to puzzle evolutionary biologists, as female reproductive success is thought to be limited mostly by her fecundity. Here we test whether females of the bulb mite, a species in which the females are highly promiscuous, benefit from polyandry in terms of increased fitness of their progeny. Females were given opportunity to mate with either one or six males, but the experiment was designed to allow the same number of matings per female in both groups, that is, irrespective of the number of males. We found that daughters of females mated to six males had significantly higher fecundity than daughters of females mated to one male, whereas other fitness components of progeny (male virility and longevity of both sexes) were not affected. These findings appear to support hypotheses proposing that multi-male mating enables females to exercise postcopulatory mate-choice (direct or indirect, via sperm competition) and thus accrue genetic benefits.     

Hatching asynchrony can have long‐term consequences for offspring fitness in zebra finches under captive conditions

Hatching asynchrony can have profound short‐term consequences for offspring, although the long‐term consequences are less well understood. The purpose of this study was to examine the long‐term consequences of hatching asynchrony for offspring fitness in birds. Specifically, we aimed to test the hypothesis that hatching asynchrony increases the sexual attractiveness and fecundity, respectively, of early‐hatched male and female zebra finch, Taeniopygia guttata (Vieillot, 1817) offspring. Mate‐choice trials comparing male nestlings with the same parents, but that were reared in asynchronous or experimentally synchronous broods, revealed no female preference in relation to hatching regime. We did however find strong evidence that, as adults, late‐hatched males were more attractive to females than siblings that had hatched earlier. Meanwhile, we found a weak trend towards early‐hatched females depositing more carotenoids and retinol in the egg yolk than late‐hatched or synchronously hatched females, although there were no differences in terms of clutch characteristics or the deposition of α‐tocopherol or γ‐tocopherol in the egg yolk. Therefore, we found that the beneficial long‐term consequences of hatching asynchrony were sex specific, being accrued by late‐hatched male nestlings and by early‐hatched female nestlings. Consequently, we conclude that the long‐term consequences of hatching asynchrony are more complex than previously realised. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 430–438.     

Sex differences in the effects of juvenile and adult diet on age‐dependent reproductive effort

Sexual selection should cause sex differences in patterns of resource allocation. When current and future reproductive effort trade off, variation in resource acquisition might further cause sex differences in age‐dependent investment, or in sensitivity to changes in resource availability over time. However, the nature and prevalence of sex differences in age‐dependent investment remain unclear. We manipulated resource acquisition at juvenile and adult stages in decorated crickets, Gryllodes sigillatus, and assessed effects on sex‐specific allocation to age‐dependent reproductive effort (calling in males, fecundity in females) and longevity. We predicted that the resource and time demands of egg production would result in relatively consistent female strategies across treatments, whereas male investment should depend sharply on diet. Contrary to expectations, female age‐dependent reproductive effort diverged substantially across treatments, with resource‐limited females showing much lower and later investment in reproduction; the highest fecundity was associated with intermediate lifespans. In contrast, long‐lived males always signalled more than short‐lived males, and male age‐dependent reproductive effort did not depend on diet. We found consistently positive covariance between male reproductive effort and lifespan, whereas diet altered this covariance in females, revealing sex differences in the benefits of allocation to longevity. Our results support sex‐specific selection on allocation patterns, but also suggest a simpler alternative: males may use social feedback to make allocation decisions and preferentially store resources as energetic reserves in its absence. Increased calling effort with age therefore could be caused by gradual resource accumulation, heightened mortality risk over time, and a lack of feedback from available mates.     

Stressful environments can indirectly select for increased longevity

Longevity is modulated by a range of conserved genes in eukaryotes, but it is unclear how variation in these genes contributes to the evolution of longevity in nature. Mutations that increase life span in model organisms typically induce trade‐offs which lead to a net reduction in fitness, suggesting that such mutations are unlikely to become established in natural populations. However, the fitness consequences of manipulating longevity have rarely been assessed in heterogeneous environments, in which stressful conditions are encountered. Using laboratory selection experiments, we demonstrate that long‐lived, stress‐resistant Caenorhabditis elegans age‐1(hx546) mutants have higher fitness than the wild‐type genotype if mixed genotype populations are periodically exposed to high temperatures when food is not limited. We further establish, using stochastic population projection models, that the age‐1(hx546) mutant allele can confer a selective advantage if temperature stress is encountered when food availability also varies over time. Our results indicate that heterogeneity in environmental stress may lead to altered allele frequencies over ecological timescales and indirectly drive the evolution of longevity. This has important implications for understanding the evolution of life‐history strategies.