Evolution of male age‐specific reproduction under differential risks and causes of death: males pay the cost of high female fitness

Classic theories of ageing evolution predict that increased extrinsic mortality due to an environmental hazard selects for increased early reproduction, rapid ageing and short intrinsic lifespan. Conversely, emerging theory maintains that when ageing increases susceptibility to an environmental hazard, increased mortality due to this hazard can select against ageing in physiological condition and prolong intrinsic lifespan. However, evolution of slow ageing under high‐condition‐dependent mortality is expected to result from reallocation of resources to different traits and such reallocation may be hampered by sex‐specific trade‐offs. Because same life‐history trait values often have different fitness consequences in males and females, sexually antagonistic selection can preserve genetic variance for lifespan and ageing. We previously showed that increased condition‐dependent mortality caused by heat shock leads to evolution of long‐life, decelerated late‐life mortality in both sexes and increased female fecundity in the nematode, Caenorhabditis remanei. Here, we used these cryopreserved lines to show that males evolving under heat shock suffered from reduced early‐life and net reproduction, while mortality rate had no effect. Our results suggest that heat‐shock resistance and associated long‐life trade‐off with male, but not female, reproduction and therefore sexually antagonistic selection contributes to maintenance of genetic variation for lifespan and fitness in this population.     

THE ECOLOGY OF SEXUAL CONFLICT: BACKGROUND MORTALITY CAN MODULATE THE EFFECTS OF MALE MANIPULATION ON FEMALE FITNESS

Sexual and parental conflicts can arise because males benefit by inducing elevated reproductive effort in their mates. For females, the costs of such manipulation are often manifested later in life, and may therefore covary with female life expectancy. Here, I outline a simple female life‐history model where female life expectancy reflects extrinsic mortality rate, and elevated reproductive effort causes accelerated senescence. Using this model, I show that variation in extrinsic mortality rate can modulate the magnitude and sign of fitness effects that male manipulation has on females. This result has several interesting implications. First, it suggests that the fitness effects of sexual interactions can depend on ecological factors, such as predation, that influence life expectancy. Second, if mortality risk is condition‐dependent but reproductive effort is not fully optimized in relation to individual condition, then sexual conflict intensity may increase with individual condition, selecting for condition‐dependent reproductive strategies. Third, if males vary in manipulativeness, then the fitness effects of mating with a given male phenotype may depend on both female condition and extrinsic mortality rate. Fourth, life span extension in the laboratory can lead to overestimation of sexual and parental conflicts. Life expectancy may therefore be a key factor in sexual coevolution.     

Age‐dependent effects of predation risk on reproductive success in a freshwater snail

Reproductive performance is often age‐dependent, showing patterns of improvement and/or senescence as well as trade‐offs with other traits throughout the lifespan. High levels of extrinsic mortality (e.g., from predators) have been shown to sometimes, but not always, select for accelerated actuarial senescence in nature and in the lab. Here, we explore the inductive (i.e., plastic) effects of predation risk (i.e., nonlethal exposure to chemical cues from predators) on the reproductive success of freshwater snails (Physa acuta). Snails were reared either in the presence or absence of chemical cues from predatory crayfish and mated early in life or late in life (a 2 × 2 factorial design); we measured egg hatching and early post‐hatching survival of their offspring. Both age and predation risk reduced reproductive success, illustrating that predation risk can have a cross‐generational effect on the early survival of juveniles. Further, the decline in reproductive success was over three times faster under predation risk compared to the no‐predator treatment, an effect that stemmed from a disproportionate, negative effect of predation risk on the post‐hatching survival instead of hatching rate. We discuss our results in terms of a hypothesized consequence of elevated stress hormone levels.     

Testing the effect of early‐life reproductive effort on age‐related decline in a wild insect

The disposable soma theory of ageing predicts that when organisms invest in reproduction they do so by reducing their investment in body maintenance, inducing a trade‐off between reproduction and survival. Experiments on invertebrates in the lab provide support for the theory by demonstrating the predicted responses to manipulation of reproductive effort or lifespan. However, experimental studies in birds and evidence from observational (nonmanipulative) studies in nature do not consistently reveal trade‐offs. Most species studied previously in the wild are mammals and birds that reproduce over multiple discrete seasons. This contrasts with temperate invertebrates, which typically have annual generations and reproduce over a single season. We expand the taxonomic range of senescence study systems to include life histories typical of most temperate invertebrates. We monitored reproductive effort, ageing, and survival in a natural field cricket population over ten years to test the prediction that individuals investing more in early‐reproduction senesce faster and die younger. We found no evidence of a trade‐off between early‐life reproductive effort and survival, and only weak evidence for a trade‐off with phenotypic senescence. We discuss the possibility that organisms with multiple discrete breeding seasons may have greater opportunities to express trade‐offs between reproduction and senescence.     

Age at mating and male quality influence female patterns of reproductive investment and survival

The trade‐off between the allocation of resources toward somatic maintenance or reproduction is one of the fundamentals of life history theory and predicts that females invest in offspring at the expense of their longevity or vice versa. Mate quality may also affect life history trade‐offs through mechanisms of sexual conflict; however, few studies have examined the interaction between mate quality and age at first mating in reproductive decisions. Using house crickets (Acheta domesticus), this study examines how survival and reproductive trade‐offs change based on females’ age at first reproduction and exposure to males of varying size. Females were exposed to either a large (presumably high‐quality) or small male at an early (young), middle (intermediate), or advanced (old) age, and longevity and reproductive investment were subsequently tracked. Females mated at a young age had the largest number of eggs but the shortest total lifespans while females mated at older ages produced fewer eggs but had longer total lifespans. The trade‐off between age at first mating and eggs laid appears to be mediated through higher egg‐laying rates and shorter postmating lifespans in females mated later in life. Exposure to small males resulted in shorter lifespans and higher egg‐laying rates for all females indicating that male manipulation of females, presumably through spermatophore contents, varies with male size in this species. Together, these data strongly support a trade‐off between age at first reproduction and lifespan and support the role of sexual conflict in shaping patterns of reproduction.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

SEXUAL SELECTION AFFECTS THE EVOLUTION OF LIFESPAN AND AGEING IN THE DECORATED CRICKET GRYLLODES SIGILLATUS

Recent work suggests that sexual selection can influence the evolution of ageing and lifespan by shaping the optimal timing and relative costliness of reproductive effort in the sexes. We used inbred lines of the decorated cricket, Gryllodes sigillatus, to estimate the genetic (co)variance between age‐dependent reproductive effort, lifespan, and ageing within and between the sexes. Sexual selection theory predicts that males should die sooner and age more rapidly than females. However, a reversal of this pattern may be favored if reproductive effort increases with age in males but not in females. We found that male calling effort increased with age, whereas female fecundity decreased, and that males lived longer and aged more slowly than females. These divergent life‐history strategies were underpinned by a positive genetic correlation between early‐life reproductive effort and ageing rate in both sexes, although this relationship was stronger in females. Despite these sex differences in life‐history schedules, age‐dependent reproductive effort, lifespan, and ageing exhibited strong positive intersexual genetic correlations. This should, in theory, constrain the independent evolution of these traits in the sexes and may promote intralocus sexual conflict. Our study highlights the importance of sexual selection to the evolution of sex differences in ageing and lifespan in G. sigillatus.     

Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata)

Little is known about the importance of trade-offs between ageing and other life history traits, or the effects of ageing on sexual selection, particularly in wild populations suffering high extrinsic mortality rates. Life history theory suggests that trade-offs between reproduction and somatic maintenance may constrain individuals with higher initial reproductive rates to deteriorate more rapidly, resulting in reduced sexual selection strength. However, this trade-off may be masked by increased condition dependence of reproductive effort in older individuals. We tested for this trade-off in males in a wild population of antler flies (Protopiophila litigata). High mating rate was associated with reduced longevity, as a result of increased short-term mortality risk or accelerated ageing in traits affecting viability. In contrast, large body size was associated with accelerated ageing in traits affecting mating success, resulting in reduced sexual selection for large body size. Thus, ageing can affect sexual selection and evolution in wild populations.     

Experimental evolution reveals differences between phenotypic and evolutionary responses to population density

Group living can select for increased immunity, given the heightened risk of parasite transmission. Yet, it also may select for increased male reproductive investment, given the elevated risk of female multiple mating. Trade‐offs between immunity and reproduction are well documented. Phenotypically, population density mediates both reproductive investment and immune function in the Indian meal moth, Plodia interpunctella. However, the evolutionary response of populations to these traits is unknown. We created two replicated populations of P. interpunctella, reared and mated for 14 generations under high or low population densities. These population densities cause plastic responses in immunity and reproduction: at higher numbers, both sexes invest more in one index of immunity [phenoloxidase (PO) activity] and males invest more in sperm. Interestingly, our data revealed divergence in PO and reproduction in a different direction to previously reported phenotypic responses. Males evolving at low population densities transferred more sperm, and both males and females displayed higher PO than individuals at high population densities. These positively correlated responses to selection suggest no apparent evolutionary trade‐off between immunity and reproduction. We speculate that the reduced PO activity and sperm investment when evolving under high population density may be due to the reduced population fitness predicted under increased sexual conflict and/or to trade‐offs between pre‐ and post‐copulatory traits.     

Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird

Theories of ageing predict that early reproduction should be associated with accelerated reproductive senescence and reduced longevity. Here, the influence of age of first reproduction on reproductive senescence and lifespan, and consequences for lifetime reproductive success (LRS), were examined using longitudinal reproductive records of male and female blue-footed boobies (Sula nebouxii) from two cohorts (1989 and 1991). The two sexes showed different relationships between age of first reproduction and rate of senescent decline: the earlier males recruited, the faster they experienced senescence in brood size and breeding success, whereas in females, recruiting age was unrelated to age-specific patterns of reproductive performance. Effects of recruiting age on lifespan, number of reproductive events and LRS were cohort- and/or sex-specific. Late-recruiting males of the 1989 cohort lived longer but performed as well over the lifetime as early recruits, suggesting the existence of a trade-off between early recruitment and long lifespan. In males of the 1991 cohort and females of both cohorts, recruiting age was apparently unrelated to lifespan, but early recruits reproduced more frequently and fledged more chicks over their lifetime than late recruits. Male boobies may be more likely than females to incur long-term costs of early reproduction, such as early reproductive senescence and diminished lifespan, because they probably invest more heavily than females. In the 1991 cohort, which faced the severe environmental challenge of an El Ni?o event in the first year of life, life-history trade-offs of males may have been masked by effects of individual quality.     

Diversity of age‐specific reproductive rates may result from ageing and optimal resource allocation

This paper reports the results of a dynamic programming model which optimizes resource allocation to growth, reproduction and repair of somatic damage, based on the disposable soma theory of ageing. Here it is shown that different age‐dependent patterns of reproductive rates are products of optimal lifetime strategies of resource partitioning. The array of different reproductive patterns generated by the model includes those in which reproduction begins at the maximum rate at maturity and then declines to the end of life, or increases up to a certain age and then drops. The observed patterns reflect optimal resource allocation shaped by the level of extrinsic mortality. A continuous decline in the reproductive rate from the start of reproduction is associated with high extrinsic mortality, and an early increase in the reproductive rate occurs under low extrinsic mortality. A long‐lived organism shows a low reproductive rate early in life, and short‐lived organisms start reproduction at the maximum rate.     

Sexual selection did not contribute to the evolution of male lifespan under curtailed age at reproduction in a seed beetle

1. Sexual selection is a powerful evolutionary force that is hypothesised to play an important role in the evolution of lifespan. Here we test for the potential contribution of sexual selection to the rapid evolution of male lifespan in replicated laboratory populations of the seed beetle, Callosobruchus maculatus. 2. For 35 generations, newly hatched virgin male beetles from eight different populations were allowed to mate for 24 h and then discarded. Sexual selection was removed in half of these populations by enforcing random monogamy. 3. Classic theory predicts that because of sexual competition, males from sexually selected lines would have higher age‐specific mortality rates and shorter lifespan than males from monogamous lines. 4. Alternatively, condition‐dependent sexual selection may also favour genes that have positive pleiotropic effects on lifespan and ageing. 5. Males from all eight populations evolved shorter lifespans compared with the source population. However, there was no difference in lifespan between males from populations with or without sexual selection. Thus, sexual selection did not contribute to the evolution of male lifespan despite the fact that such evolution did occur in our study populations.     

Sexual signals reflect telomere dynamics in a wild bird

Telomere dynamics in natural populations have been linked to survival, reproduction, and energetic investment. Given their putative role in mediating life‐history trade‐offs, telomeres are also a likely candidate for maintaining honesty in sexually selected signals; few studies to date, however, have demonstrated a correlation between sexual signals and telomere dynamics. Here, we show that plumage coloration in male common yellowthroats (Geothlypis trichas) is correlated with both relative telomere length and with the rate of telomere loss between years. Elevated antioxidant capacity is also associated with reduced telomere loss, but only among older males. Previous work in this population has demonstrated that males with brighter plumage are in better condition, have higher reproductive success, and are more likely to survive over winter. Thus, the signal attribute associated with mate choice in this system also conveys reliable information about telomere dynamics. At present, it is unclear whether telomere maintenance plays a causal role in maintaining signal honesty or whether the correlation arises due to underlying variation in individual resources or genotypes. We suggest that subsequent work should consider the possibility that fundamental trade‐offs between signal investment and cell‐level processes that influence aging and reproductive senescence may provide a foundation for understanding the maintenance of sexual signal honesty.     

Phenotypes optimized for early‐life reproduction exhibit faster somatic deterioration with age,revealing a latent cost of high condition

High condition enables individuals to express a phenotype with greater reproductive potential. However, life‐history theory predicts that reproduction will trade off with somatic maintenance and viability, and several studies have reported faster age‐related decline in performance in high‐condition individuals, suggesting that high condition in early life is associated with accelerated somatic deterioration. This trade‐off may be especially pronounced in males, which often express condition‐dependent secondary sexual traits that can impose viability costs during development and through damage‐inflicting adult sexual behaviours. To test this prediction, we reared larvae of the neriid fly Telostylinus angusticollis on diets of varying nutrient content and quantified somatic deterioration in solitary males, males housed in all‐male or mixed‐sex groups and immobilized males subjected to mechanical stress. We found that males reared on a nutrient‐rich larval diet (high‐condition males) suffered a higher rate of somatic deterioration with age, particularly when housed in groups. Perhaps as a result of accelerated somatic deterioration, high‐condition males did not outlive low‐condition males. In addition, high‐condition males housed in all‐male groups experienced a greater reduction in escape response with age than males housed in mixed‐sex groups, suggesting that male–male combat promotes somatic deterioration. However, even when immobilized, high‐condition males were still found to be more susceptible to somatic damage than low‐condition males. Our findings suggest that a high‐condition male phenotype is more prone to somatic damage, both as a result of associated behaviours such as combat, and because of the inherent fragility of the high‐condition body.     

Female access and diet affect insemination success,senescence and the cost of reproduction in the male Mexican fruit fly Anastrepha ludens

Hypotheses exploring the influence of dietary conditions on the life‐history trade‐off between survival and reproductive success are extensively tested in female insects but only rarely explored in males. The present study examines the impact of dietary quality and female access on age‐specific reproduction and survival of the male Mexican fruit fly Anastrepha ludens Loew (Diptera: Tephritidae). There is a clear cost of female access for males with access to dietary protein, measurable as a decrease in life expectancy, which is further influenced by the age when females are introduced. A protein deficient diet reduces the lifespan benefit of virginity and masks the detrimental effect of female access on male life expectancy. Dietary protein is not necessary for reproductive success, although access to protein at eclosion improves the lifetime reproductive success of males compared to when it is delayed. Overall, reproductive success diminishes as the male flies age, regardless of the dietary conditions, providing evidence for reproductive senescence in males. Delaying the males' access to a protein source fails to influence the negative effect of age on reproductive ability. Because age‐specific reproductive rates decline with age, regardless of diet, male fitness does not benefit from lifespan extension. Therefore, males can be expected to allocate available resources towards reproductive effort in favour of an extended lifespan, regardless of mate and protein availability.     

Reproductive effort accelerates actuarial senescence in wild birds: an experimental study

Optimality theories of ageing predict that the balance between reproductive effort and somatic maintenance determines the rate of ageing. Laboratory studies find that increased reproductive effort shortens lifespan, but through increased short‐term mortality rather than ageing. In contrast, high fecundity in early life is associated with accelerated senescence in free‐living vertebrates, but these studies are non‐experimental. We performed lifelong brood size manipulation in free‐living jackdaws. Actuarial senescence – the increase in mortality rate with age – was threefold higher in birds rearing enlarged‐ compared to reduced broods, confirming a key prediction of the optimality theory of ageing. Our findings contrast with the results of single‐year brood size manipulation studies carried out in many species, in which there was no overall discernible manipulation effect on mortality. We suggest that our and previous findings are in agreement with predictions based on the reliability theory of ageing and propose further tests of this proposition.     

The Evolution of Senescence and Post-Reproductive Lifespan in Guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history. Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness. Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.     

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.     

On the evolution,life history,and proximate mechanisms of human male reproductive senescence

Reproductive senescence is a central and defining life‐history characteristic of every known mammal. Within the scope of human senescence research, attention has been mainly focused on females, particularly in reference to the uniqueness of menopause. However, consideration of the evolution of human male reproductive senescence has been minimal, primarily due to the assumption that male fertility, as compared to that of females, is relatively invariant with age. Moreover, theoretical development of our understanding of human male reproductive senescence has not been extensive despite increasing awareness of the importance of life‐history trade‐offs in association with aging. Emerging research now illustrates important aspects of male reproductive senescence, exhibit significant variation and phenotypic plasticity, while others are less malleable. Changes in hormone‐modulated somatic integrity with age also show important population differences, most likely as the result of reaction norms in response to environmental variation. Coupled with emerging ideas about the energetics of life‐history trade‐offs in human males, a new perspective is beginning to emerge. It suggests that human males exhibit potentially adaptive shifts in reproductive function in association with age.     

The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history.

Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness.

Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.