Evolutionary responses of Drosophila melanogaster life history to differences in larval density

The study examined the effects of evolution at two different larval densities on pre-adult and adult fitness traits. Five replicate selection lines each were cultured at either 50 or 150 larvae per vial, avoiding selection on development time, age at breeding or for adaptation to adult density, one or more of which factors has been a confounding variable in previous studies. Low density selection lines evolved extended development times at both growth densities. The extended development times were associated with greater adult body size at the lower growth density only, and particularly in females. The lines did not differ significantly in larval competitive ability at either growth density. At neither growth density did the early adult fertility of females or the lifespan of either sex differ between the lines from the two selection regimes, but at the lower growth density the late fertility of low density line females was significantly enhanced. The results suggest that larval density does have important effects on the expression and resolution of life history trade-offs in Drosophila melanogaster, but that these may be somewhat different from those reported in previous studies.     

DIRECT AND CORRELATED RESPONSES TO SELECTION ON AGE AT REPRODUCTION IN DROSOPHILA MELANOGASTER

Aging may be a consequence of mutation accumulation or of negative pleiotropic correlations between performance late and earlier in the lifespan. This study used artificial selection on flies derived from two different base stocks to produce “young” and “old” lines, propagated by breeding from young and old adults respectively. Virgin and mated adults of both sexes from the “old” lines lived longer than “young” line flies. “Young” and “old” mated females did not differ in fecundity or fertility early in the lifespan, but “old” line females had higher fecundity and fertility late in life. The results therefore suggested either that the response to selection had revealed the effect of mutation accumulation, or that pleiotropy involving characters other than early fecundity must have been involved. Development time from egg to adult was longer in the “old” lines. Competition of selected line larvae from one base stock against mutant marked larvae from the same base stock revealed that, at a wide range of larval densities, “old” line larvae showed lower survival rates than “young” line larvae. Thorax length and wet weight were significantly greater in the “old” line flies from one base stock. The results may imply that the selection regime in the “old” lines favored extended growth during development to produce a more durable adult soma, despite the cost in increased larval mortality and delayed reproduction, because the potential reproductive benefits later in life were increased. However, the differences between larvae from “old” and “young” lines could also be attributable to density differences, and this possibility needs systematic investigation.     

Complex life cycles and the responses of insects to climate change

Many organisms have complex life cycles with distinct life stages that experience different environmental conditions. How does the complexity of life cycles affect the ecological and evolutionary responses of organisms to climate change? We address this question by exploring several recent case studies and synthetic analyses of insects. First, different life stages may inhabit different microhabitats, and may differ in their thermal sensitivities and other traits that are important for responses to climate. For example, the life stages of Manduca experience different patterns of thermal and hydric variability, and differ in tolerance to high temperatures. Second, life stages may differ in their mechanisms for adaptation to local climatic conditions. For example, in Colias, larvae in different geographic populations and species adapt to local climate via differences in optimal and maximal temperatures for feeding and growth, whereas adults adapt via differences in melanin of the wings and in other morphological traits. Third, we extend a recent analysis of the temperature-dependence of insect population growth to demonstrate how changes in temperature can differently impact juvenile survival and adult reproduction. In both temperate and tropical regions, high rates of adult reproduction in a given environment may not be realized if occasional, high temperatures prevent survival to maturity. This suggests that considering the differing responses of multiple life stages is essential to understand the ecological and evolutionary consequences of climate change.     

Direct and correlated responses to selection on age at physiological maturity in Drosophila simulans

Biologists who study the timing of development in insects have focused on variation in duration of pre‐adult stages almost without exception. However, development is not complete until adults are not only morphologically mature, but also reproductively mature. Here we describe an experiment in the fruit fly, Drosophila simulans, in which we used artificial selection to create lines with shortened and lengthened duration from eclosion to the age when the first egg was laid. We found significant genetic variation for this trait. The response to selection on age when the first egg was laid was due to variation among females. Delayed adult development was correlated with rapid pre‐adult development and longer life span in females. The approach we use here resolves some difficulties with previous approaches used to study the genetics of senescence, and provides an opportunity to study the hitherto unexamined predictions derived from classic models for the evolution of senescence.     

动物生活史进化理论研究进展

综述了生活史性状、生活史对策、权衡、适合度及进化种群统计学等动物生活史进化领域的进展。权衡是生活史性状之间相互联系的纽带,分为生理权衡与进化权衡。适合度是相对的,与个体所处的特定环境条件有关,性状进化与适合度之间关系紧密。适合度是生活史进化理论研究的焦点。探讨动物生活史对策的理论很多,影响最大的是MacArthur和Wilson提出的r对策及K对策理论。随年龄的增长,动物存活率及繁殖率逐步下降的过程,称为衰老;解释衰老的进化理论主要有突变-选择平衡假设和多效对抗假设。进化种群统计学将种群统计学应用于生活史进化研究,为探讨表型适合度的进化提供了有效的手段。将进化种群统计学、数量遗传学及特定种系效应理论进行整合,建立完整的动物生活史进化综合理论体系,是当代此领域的最大挑战。     

Predictable modification of body size and competitive ability following a host shift by a seed beetle

Interfertile populations of the seed beetle Callosobruchus maculatus differ genetically in several behavioral, morphological, and life-history traits, including traits that affect the intensity of larval competition within seeds. Previous studies have suggested that this variation depends on differences in host size. I performed a selection experiment in which replicate beetle lines were either maintained on a small, ancestral host (mung bean) or switched to a larger, novel host (cowpea). After 40 generations, I estimated survival, development time, and adult mass on each host, both in the presence and absence of larval competition. The shift to cowpea substantially reduced body size; irrespective of rearing host, adults from the cowpea lines were more than 10% lighter than those from the mung bean lines. Switching to cowpea also improved survival and reduced development time on this host, but without decreasing performance on the ancestral host. The most striking effect of the shift to a larger host was a reduction in larval competitiveness. When two even-aged larvae co-existed within a seed, the probability that both survived to adult emergence was > or = 65% if larvae were from the cowpea lines but < or = 12% if they were from the mung bean lines. The adverse effects of competition on development time and adult mass were also less severe in the cowpea lines than in the mung bean lines. By rapidly evolving smaller size and reduced competitiveness, the cowpea lines converged toward populations chronically associated with cowpea. These results suggest that evolutionary trajectories can be predictable, and that host-specific selection can play a major role in the diversification of insect life histories. Because host shifts by small, endophagous insects are comparable to the colonization of new habitats, adaptive responses may often include traits (such as larval competitiveness) that are not directly related to host use.     

Molecular evolution, mutation size and gene pleiotropy: a geometric reexamination

The influence of phenotypic effects of genetic mutations on molecular evolution is not well understood. Neutral and nearly neutral theories of molecular evolution predict a negative relationship between the evolutionary rate of proteins and their functional importance; nevertheless empirical studies seeking relationships between evolutionary rate and the phenotypic role of proteins have not produced conclusive results. In particular, previous studies have not found the expected negative correlation between evolutionary rate and gene pleiotropy. Here, we studied the effect of gene pleiotropy and the phenotypic size of mutations on the evolutionary rate of genes in a geometrical model, in which gene pleiotropy was characterized by n molecular phenotypes that affect organismal fitness. For a nearly neutral process, we found a negative relationship between evolutionary rate and mutation size but pleiotropy did not affect the evolutionary rate. Further, for a selection model, where most of the substitutions were fixed by natural selection in a randomly fluctuating environment, we also found a negative relationship between evolutionary rate and mutation size, but interestingly, gene pleiotropy increased the evolutionary rate as √n. These findings may explain part of the disagreement between empirical data and traditional expectations.     

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.     

EVOLUTIONARY EFFECTS OF SELECTION ON AGE AT REPRODUCTION IN LARVAL AND ADULT: DROSOPHILA MELANOGASTER

Two sets of three replicate lines of Drosophila melanogaster were artificially selected by reproduction at either a ‘young’ or an ‘old’ age. The pure lines, the hybrids between the lines within a selection regimen and the base stock from which the lines were derived were compared for longevity, early and late fertility, development time, larval viability and adult thorax length. Comparison of hybrid with pure lines showed some evidence for inbreeding depression in the lines from both selection regimes. Comparison of hybrid lines with the base stock did not provide evidence for any trade-off in either males or females between early fertility on the one hand and late life fertility and longevity on the other. Nor was there any clear evidence of a trade-off between pre-adult and adult fitness components. There was evidence of inadvertent selection for rapid development in both selection regimens, especially in the females of the ‘young’ lines, and this complicated the interpretation of the responses and correlated responses to selection. An improvement in adult performance in the ‘old’ line males relative to the base stock appeared to be attributable to reversal of mutation accumulation. Comparison of the hybrid ‘young’ and ‘old’ lines with the base stock did not support the idea that the superior longevity and late life fertility of the ‘old’ lines relative to the ‘young’ lines could be accounted for by the effects of mutation accumulation in the ‘young’ lines. The results point to the need to compare selected lines with their base stock when deducing responses and correlated responses to selection and to avoid unintentional selection. In this type of experiment, larval density should be standardized during selection, and adults should not be under pressure for rapid maturation.     

ARTIFICIAL SELECTION FOR DEVELOPMENTAL TIME IN DROSOPHILA MELANOGASTER IN RELATION TO THE EVOLUTION OF AGING: DIRECT AND CORRELATED RESPONSES

A wild-type strain of Drosophila melanogaster was successfully selected for both fast and slow larval development. The realized heritabilities (h²) ranged from 0.20 to 0.30 for the fast lines and 0.35 to 0.60 for the slow lines. The selection applied is relevant in relation to the evolution of aging. The longevity of adults, either virgin or mated, was not affected by selection for developmental time, indicating that developmental time is not a causal determinant of life span, thus confirming the results of the studies on environmental effects on aging (Zwaan et al. 1991, 1992). However, adult body weights were higher in the slow developmental lines and lower in the fast lines, relative to the control flies. Furthermore, slow females showed relatively high early fecundity and low late fecundity, as compared with control and fast females. Mated longevities and total lifetime progeny productions were not statistically different. Previous results obtained by other authors from selection experiments on age at reproduction either supported the mutation accumulation or the negative pleiotropy theory of aging (Luckinbill et al. 1984; Rose 1984b). The impact of the reported results on the interpretation of these studies is discussed, and it is noted that direct selection on adult longevity is needed to settle this issue.     

Why men matter: mating patterns drive evolution of human lifespan

Evolutionary theory predicts that senescence, a decline in survival rates with age, is the consequence of stronger selection on alleles that affect fertility or mortality earlier rather than later in life. Hamilton quantified this argument by showing that a rare mutation reducing survival is opposed by a selective force that declines with age over reproductive life. He used a female-only demographic model, predicting that female menopause at age ca. 50 yrs should be followed by a sharp increase in mortality, a "wall of death." Human lives obviously do not display such a wall. Explanations of the evolution of lifespan beyond the age of female menopause have proven difficult to describe as explicit genetic models. Here we argue that the inclusion of males and mating patterns extends Hamilton's theory and predicts the pattern of human senescence. We analyze a general two-sex model to show that selection favors survival for as long as men reproduce. Male fertility can only result from matings with fertile females, and we present a range of data showing that males much older than 50 yrs have substantial realized fertility through matings with younger females, a pattern that was likely typical among early humans. Thus old-age male fertility provides a selective force against autosomal deleterious mutations at ages far past female menopause with no sharp upper age limit, eliminating the wall of death. Our findings illustrate the evolutionary importance of males and mating preferences, and show that one-sex demographic models are insufficient to describe the forces that shape human senescence.     

THE EVOLUTION OF DEVELOPMENT IN DROSOPHILA MELANOGASTER SELECTED FOR POSTPONED SENESCENCE

The role of development in the evolution of postponed senescence is poorly understood despite the existence of a major gerontological theory connecting developmental rate to aging. We investigate the role of developmental rate in the laboratory evolution of aging using 24 distinct populations of Drosophila melanogaster. We have found a significant difference between the larval developmental rates of our Drosophila stocks selected for early (B) and late-life (O) fertility. This larval developmental time difference of approximately 12% (O > B) has been stable for at least 5 yr, occurs under a wide variety of rearing conditions, responds to reverse selection, and is shown for two other O-like selection treatments. Emerging adults from lines with different larval developmental rates show no significant differences in weight at emergence, thorax length, or starvation resistance. Long-developing lines (O, CO, and CB) have greater survivorship from egg to pupa and from pupa to adult, with and without strong larval competition. Crosses between slower developing populations, and a variety of other lines of evidence, indicate that neither mutation accumulation nor inbreeding depression are responsible for the extended development of our late-reproduced selection treatments. These results stand in striking contrast to other recent studies. We argue that inbreeding depression and inadvertent direct selection in other laboratories' culture regimes explain their results. We demonstrate antagonistic pleiotropy between developmental rate and preadult viability. The absence of any correlation between longevity and developmental time in our stocks refutes the developmental theory of aging.     

To age or not to age

According to the antagonistic pleiotropy theory of ageing, natural selection has favoured genes conferring short-term benefits to the organism at the cost of deterioration in later life. The 'disposable soma' theory expresses this as a life-history strategy in which somatic maintenance is below the level required to prevent ageing, thus enabling higher immediate fertility. It has been argued that a non-ageing strategy will always be bettered by a low but non-zero rate of ageing, because the costs of such ageing will be felt only in the distant future when they are of negligible importance. Here, we examine this argument critically. We find that a non-ageing strategy will be locally optimal if, in the presence of ageing, the onset of deterioration is sufficiently rapid or early. Conversely, ageing will be optimal if deterioration is sufficiently slow or late. As the temporal profile of ageing changes from one of steady deterioration to one involving a sudden loss of vitality after a period of little or no decline, the conditions for a non-ageing strategy to be locally optimal become progressively more stringent. But for all forms of profile considered, conditions can be found for which a strategy involving no ageing is locally optimal.     

Does increased heat resistance result in higher susceptibility to predation? A test using Drosophila melanogaster selection and hardening

Heat resistance of ectotherms can be increased both by plasticity and evolution, but these effects may have trade‐offs resulting from biotic interactions. Here, we test for predation costs in Drosophila melanogaster populations with altered heat resistance produced by adult hardening and directional selection for increased heat resistance. In addition, we also tested for genetic trade‐offs by testing heat resistance in lines that have evolved under increased predation risk. We show that while 35/37 °C hardening increases heat resistance as expected, it does not increase predation risk from jumping spiders or mantids; in fact, there was an indication that survival may have increased under predation following a triple 37 °C compared to a single 35 °C hardening treatment. Flies that survived a 39 °C selection cycle showed lower survival under predation, suggesting a predation cost of exposure to a more severe heat stress. There was, however, no correlated response to selection because survival did not differ between control and selected lines after selection was relaxed for one or two generations. In addition, lines selected for increased predation risk did not differ in heat resistance. Our findings suggest independent evolutionary responses to predation and heat as measured in laboratory assays, and no costs of heat hardening on susceptibility to predation.     

Applying the genetic theories of ageing to the cytoplasm: cytoplasmic genetic covariation for fitness and lifespan

Two genetic models exist to explain the evolution of ageing – mutation accumulation (MA) and antagonistic pleiotropy (AP). Under MA, a reduced intensity of selection with age results in accumulation of late‐acting deleterious mutations. Under AP, late‐acting deleterious mutations accumulate because they confer beneficial effects early in life. Recent studies suggest that the mitochondrial genome is a major player in ageing. It therefore seems plausible that the MA and AP models will be relevant to genomes within the cytoplasm. This possibility has not been considered previously. We explore whether patterns of covariation between fitness and ageing across 25 cytoplasmic lines, sampled from a population of Drosophila melanogaster, are consistent with the genetic associations predicted under MA or AP. We find negative covariation for fitness and the rate of ageing, and positive covariation for fitness and lifespan. Notably, the direction of these associations is opposite to that typically predicted under AP.     

Early-late life trade-offs and the evolution of ageing in the wild

Empirical evidence for declines in fitness components (survival and reproductive performance) with age has recently accumulated in wild populations, highlighting that the process of senescence is nearly ubiquitous in the living world. Senescence patterns are highly variable among species and current evolutionary theories of ageing propose that such variation can be accounted for by differences in allocation to growth and reproduction during early life. Here, we compiled 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life. Our review brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life. We discuss our results in the light of two closely related theories of ageing—the disposable soma and the antagonistic pleiotropy theories—and propose that the principle of energy allocation roots the ageing process in the evolution of life-history strategies. Finally, we outline research topics that should be investigated in future studies, including the importance of natal environmental conditions in the study of trade-offs between early- and late-life performance and the evolution of sex-differences in ageing patterns.     

The force of selection on the human life cycle

In this article, I present evidence for a robust and quite general force of selection on the human life cycle. The force of selection acts in remarkably invariant ways on human life histories, despite a great abundance of demographic diversity. Human life histories are highly structured, with mortality and fertility changing substantially through the life cycle. This structure necessitates the use of structured population models to understand human life history evolution. Using such structured models, I find that the vital rates to which fitness is most sensitive are prereproductive survival probabilities, particularly the survival of children ages 0 to 4 years. The fact that the preponderance of selection falls on transitions related to recruitment combined with the late age at first reproduction characteristic of the human life cycle creates a fitness bottleneck out of recruitment. Because of this, antagonistic pleiotropy with any trait that detracts from the constituent transitions to recruitment is expected. I explore the predictors of variation in the force of selection on early survival. High fertility increases the selective premium placed on early survivorship, whereas high life expectancy at birth decreases it.     

Social structure and winter survival in acorn ants

Fluctuating selection is a major theme in the evolutionary and ecological literature, yet attempts to measure how differential selection across time or space affects long-term change in life history traits or behaviors are still rare. Social evolution among the insects has been broadly studied with respect to how key parameters such as queen number and relatedness vary to influence colony fitness. However, a primary focus on fertility selection in the warm months must be complemented by parallel investigations on survivorship selection during the cold months. Here we provide the first assessment of social structure and overwintering survivorship in the field. We studied the acorn ant, which stays aboveground throughout the cold winters in North America, by varying queen number and colony size over two consecutive winters. We found that winter survival was quite low but unconnected to variable colony structure. Therefore previous studies on how social structure affects fertility selection in acorn ants have not been confounded by countervailing selection during the cold months. Our data support the assumption of the larger literature that selective forces molding social behavior in ants act primarily on fertility selection during the reproductive season.     

Artificial selection on male longevity influences age-dependent reproductive effort in the black field cricket Teleogryllus commodus

Although the trade-off between reproductive effort and longevity is central to both sexual selection and evolutionary theories of aging, there has been little synthesis between these fields. Here, we selected directly on adult longevity of male field crickets Teleogryllus commodus and measured the correlated responses of age-dependent male reproductive effort, female lifetime fecundity, and several other life-history traits. Male longevity responded significantly to five generations of divergent selection. Males from downward-selected lines commenced calling sooner and reached their peak calling effort at a younger age. They called more per night and, despite living less than half as long, called more overall than males selected for increased longevity. Females from the downward-selected lines lived significantly shorter lives than females from the upward-selected lines but still produced the same number of offspring. Nymph survival, development time, and body size and weight at eclosion did not show significant correlated response to selection on male longevity, despite evidence for substantial genetic variation in each of these traits. Collectively, our findings directly support the antagonistic pleiotropy model of aging and suggest an important role for sexual selection in the aging process.     

Expression of genetic and environmental variation during ageing

Summary A selection experiment with Drosophila melanogaster was carried out to test some theories of ageing by calculating genetic parameters for a reproductive fitness trait at different ages. Successful selection for increased lifespan showed that longevity is a trait under genetic control. Positive genetic correlations between early and late fitness were found. These results do not support the pleiotropy theory of ageing which predicts a negative genetic correlation. Both environmental and additive genetic variation clearly increased with age. Increased environmental variation probably reflects the individuals' difficulties in coping with environmental stress. The increase in additive genetic variation supports the mutation accumulation theory of ageing, as well as other theories that postulate increased additive genetic variation with age.