Is There Adaptive Value to Reproductive Termination in Japanese Macaques? A Test of Maternal Investment Hypotheses

Evolutionary biologists often argue that menopause evolved in the human female as the result of selection for a postreproductive phase of life, during which increased maternal investment in existing progeny could lead to enhanced survivorship of descendents. Adaptive theories relating menopause to enhanced maternal investment are known as the mother (first-generation) and grandmother (second-generation-offspring) hypotheses. Although menopause—universal midlife termination of reproduction—has not been documented in primates other than humans, some researchers have argued that postreproductive alloprimates also have a positive impact on the survivorship of first and second generation progeny. We tested the maternal investment hypotheses in Japanese macaques by comparing the survivorship of offspring, final infants, and great-offspring of females that terminated reproduction before death with females that continued to reproduce until death. SURVIVAL analyses revealed no significant difference in the survivorship of descendents of postreproductive and reproductive females, though final infants of postreproductive females were 13% more likely to survive than final infants of females that reproduced until death were. We also explored possible differences between these two groups of females, other than survivorship of progeny. We found no difference in dominance rank, matrilineal affiliation, body weight, infant sex ratio, age at first birth, fecundity rate or lifetime reproductive success. However, postreproductive females are significantly longer-lived than reproductive females and as a result experienced more years of reproduction and produced more infants in total. Apart from final infants, offspring survival is marginally lower in postreproductive females. Since offspring survival is not significantly enhanced in postreproductive females, the greater number of infants produced did not translate into greater lifetime reproductive success. Our findings fail to support the maternal investment hypotheses and instead suggest that reproductive termination in this population of Japanese macaques is most closely associated with enhanced longevity and its repercussions.     

Reproductive senescence and terminal investment in female Barbary macaques (Macaca sylvanus) at Salem

The reproductive history of 207 female Barbary macaques, living in a large outdoor enclosure in Southwest Germany, was studied during an 11-year period. The results yielded a significant relationship between female age and fecundity, with fertility rates lower than expected among young and old females. Analysis of the reproductive history of individual females revealed a significant decline in fertility from prime age (7–12 years) to mid age (13–19 years), and from mid age to old age (20–25 years). The proportion of long interbirth intervals increased steadily among aging females. Infant survival was not significantly related to maternal age, but offspring of old females showed the highest survivorship. Behavioral observations revealed that old mothers weaned their offspring significantly later than younger mothers, suggesting that prolongation of interbirth intervals is due not only to deteriorating physical condition but also to increased maternal investment, as life history theory predicts. Reproduction ceased during the middle of the third decade of life. Final cessation of estrous cycling invariably occurred 3 or 4 years after the birth of the last offspring, but a postreproductive life span of 5 years appears to be common in this population. Available data suggest that reproductive senescence and menopause are more common among nonhuman primates than widely believed and that both traits are part of an adaptive life history strategy.     

Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago

Long-lived iteroparous species often show aging-related changes in reproduction that may be explained by 2 non-mutually exclusive hypotheses. The terminal investment hypothesis predicts increased female reproductive effort toward the end of the life span, as individuals have little to gain by reserving effort for the future. The senescence hypothesis predicts decreased female reproductive output toward the end of the life span due to an age-related decline in body condition. Nonhuman primates are ideal organisms for testing these hypotheses, as they are long lived and produce altricial offspring heavily dependent on maternal investment. In this study, we integrated 50 years of continuous demographic records for the Cayo Santiago rhesus macaque (Macaca mulatta) population with new morphometric and behavioral data to test the senescence and terminal investment hypotheses. We examined relationships between maternal age and activity, mother and infant body condition, interbirth intervals, measures of behavioral investment in offspring, and offspring survival and fitness to test for age-associated declines in reproduction that would indicate senescence, and for age-associated increases in maternal effort that would indicate terminal investment. Compared with younger mothers, older mothers had lower body mass indices and were less active, had longer interbirth intervals, and spent more time in contact with infants, but had infants of lower masses and survival rates. Taken together, our results provide strong evidence for the occurrence of reproductive senescence in free-ranging female rhesus macaques but are also consistent with some of the predictions of the terminal investment hypothesis.     

Sex‐specific pathways of parental age effects on offspring lifetime reproductive success in a long‐lived seabird

The conditions under which individuals are reared vary and sensitivity of offspring to such variation is often sex‐dependent. Parental age is one important natal condition with consequences for aspects of offspring fitness, but reports are mostly limited to short‐term fitness consequences and do not take into account offspring sex. Here we used individual‐based data from a large colony of a long‐lived seabird, the common tern Sterna hirundo, to investigate longitudinal long‐term fitness consequences of parental age in relation to both offspring and parental sex. We found that recruited daughters from older mothers suffered from reduced annual reproductive success. Recruited sons from older fathers were found to suffer from reduced life span. Both effects translated to reductions in offspring lifetime reproductive success. Besides revealing novel sex‐specific pathways of transgenerational parental age effects on offspring fitness, which inspire studies of potential underlying mechanisms, our analyses show that reproductive senescence is only observed in the common tern when including transgenerational age effects. In general, our study shows that estimates of selective pressures underlying the evolution of senescence, as well as processes such as age‐dependent mate choice and sex allocation, will depend on whether causal transgenerational effects exist and are taken into account.     

THE EFFECT OF MATERNAL AGE AND REPRODUCTIVE HISTORY ON OFFSPRING SURVIVAL AND LIFETIME REPRODUCTION IN PREINDUSTRIAL HUMANS

Senescence is one of the least understood aspects of organism life history. In part, this stems from the relatively late advent of complete individual‐level datasets and appropriate statistical tools. In addition, selection against senescence should depend on the contribution to population growth arising from physiological investment in offspring at given ages, but offspring are rarely tracked over their entire lives. Here, we use a multigenerational dataset of preindustrial (1732–1860) Finns to describe the association of maternal age at offspring birth with offspring survival and lifetime reproduction. We then conduct longitudinal analyses to understand the drivers of this association. At the population level, offspring lifetime reproductive success (LRS) declined by 22% and individual λ, which falls with delays to reproduction, declined by 45% as maternal age at offspring birth increased from 16 to 50 years. These results were mediated by within‐mother declines in offspring survival and lifetime reproduction. We also found evidence for modifying effects of offspring sex and maternal socioeconomic status. We suggest that our results emerge from the interaction of physiological with social drivers of offspring LRS, which further weakens selection on late‐age reproduction and potentially molds the rate of senescence in humans.     

Availability and adaptive value of reproductive and postreproductive Japanese macaque mothers and grandmothers

Prior tests of the grandmother hypothesis have suggested that postreproductive female Japanese macaques,Macaca fuscata , do not significantly improve the survivorship of their descendents. However, not all postreproductive females are grandmothers, and not all grandmothers are postreproductive. In this study we looked at the daughters and grandchildren of 70 female Japanese macaques to assess the availability and adaptive value of reproductive and postreproductive mothers and grandmothers. We found that postreproductive Japanese macaque grandmothers are very rare. Only 2.8% of the sample of daughters had a postreproductive grandmother available when they began to reproduce, and only 4.2% of the reproductive life span of the daughter (less than 6 months for the average female) was spent with a postreproductive grandmother available to help the daughter. Grandchildren who survived to age 5 had a postreproductive grandmother available to them for only 4% of the first 5 years of life (i.e. a couple of months on average). The presence of a living mother, irrespective of her reproductive status, was associated with improved reproduction in her adult daughters, and the presence of a postreproductive grandmother was associated with significantly improved survivorship of grandchildren to age 1. While improved maternal investment does not appear to be the primary explanation for reproductive termination in Japanese monkeys, the few postreproductive females that have unweaned grandchildren available appear to have a positive influence on their survival. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause

Human menopause is remarkable in that reproductive senescence is markedly accelerated relative to somatic aging, leaving an extended postreproductive period for a large proportion of women. Functional explanations for this are debated, in part because comparative data from closely related species are inadequate. Existing studies of chimpanzees are based on very small samples and have not provided clear conclusions about the reproductive function of aging females. These studies have not examined whether reproductive senescence in chimpanzees exceeds the pace of general aging, as in humans, or occurs in parallel with declines in overall health, as in many other animals. In order to remedy these problems, we examined fertility and mortality patterns in six free-living chimpanzee populations. Chimpanzee and human birth rates show similar patterns of decline beginning in the fourth decade, suggesting that the physiology of reproductive senescence was relatively conserved in human evolution. However, in contrast to humans, chimpanzee fertility declines are consistent with declines in survivorship, and healthy females maintain high birth rates late into life. Thus, in contrast to recent claims, we find no evidence that menopause is a typical characteristic of chimpanzee life histories.     

The evolution of postreproductive life span as an insurance against indeterminacy

Postreproductive life span remains a puzzle for evolutionary biologists. The explanation of increased inclusive fitness through parental care after reproduction that applies for humans is unrealistic for many species. We propose a new selective mechanism, independent of parental care, which relies on the hypothesis that postreproductive life span can evolve as an insurance against indeterminacy: longer life expectancy reduces the risk of dying by chance before the cessation of reproductive activity. We demonstrate numerically that the duration of evolved postreproductive life span is indeed expected to increase with variability in life span duration. An unprecedented assay of 11 strains of the collembola Folsomia candida shows the existence of (1) postreproductive life span in the absence of parental care; (2) genetic variability in mean postreproductive life span and postreproductive life span variability itself; (3) strong genetic correlation between latter traits. This new explanation brings along the novel idea that loose canalization of a trait (here, somatic life span) can itself act as a selective pressure on other traits.     

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.     

Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion

We examine and discuss evidence of contrasting differences in fertility patterns between captive and wild female chimpanzees, Pan troglodytes, as they age; in the wild females reproduce in their 40s, but captive studies suggest that menopause occurs around that time. Thus, despite the increased longevity generally observed in captive populations reproductive life span is shortened. We outline a hypothesis to explain the apparent differential pace of reproductive decline observed between wild and captive populations. The breeding schedules of captive primates may contribute to accelerated reproductive senescence because continuous cycling in captive animals results in early depletion of the ovarian stock and premature senescence. Available evidence supports the hypothesis that women with patterns of high oocyte loss experience earlier menopause. Chimpanzees in captivity live longer, and thus, similar to humans, they may experience follicular depletion that precedes death by many years. In captivity, chimpanzees typically have an early age at menarche and first birth, shorter interbirth intervals associated with short lactational periods as young mature faster, and nursery rearing, which allows mothers to begin cycling earlier. Variables typical of wild chimpanzee populations, including late age at menarche and first birth, long interbirth intervals associated with prolonged lactational periods, and a long period of female infertility after immigration, spare ovulations and may be responsible for the later age at reproductive termination. Finally, we describe and discuss the timing of specific reproductive landmarks that occur as female chimpanzees age, distinguishing between functional menopause (age at last birth) and operational menopause (end of cycling). Am. J. Primatol. 71:271–282, 2009. © 2008 Wiley‐Liss, Inc.     

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.     

Early-life reproduction is associated with increased mortality risk but enhanced lifetime fitness in pre-industrial humans

The physiology of reproductive senescence in women is well understood, but the drivers of variation in senescence rates are less so. Evolutionary theory predicts that early-life investment in reproduction should be favoured by selection at the cost of reduced survival and faster reproductive senescence. We tested this hypothesis using data collected from preindustrial Finnish church records. Reproductive success increased up to age 25 and was relatively stable until a decline from age 41. Women with higher early-life fecundity (ELF; producing more children before age 25) subsequently had higher mortality risk, but high ELF was not associated with accelerated senescence in annual breeding success. However, women with higher ELF experienced faster senescence in offspring survival. Despite these apparent costs, ELF was under positive selection: individuals with higher ELF had higher lifetime reproductive success. These results are consistent with previous observations in both humans and wild vertebrates that more births and earlier onset of reproduction are associated with reduced survival, and with evolutionary theory predicting trade-offs between early reproduction and later-life survival. The results are particularly significant given recent increases in maternal ages in many societies and the potential consequences for offspring health and fitness.     

Brief Communication: Orphaned male Chimpanzees die young even after weaning

If a social‐living animal has a long life span, permitting different generations to co‐exist within a social group, as is the case in many primate species, it can be beneficial for a parent to continue to support its weaned offspring to increase the latter's survival and/or reproductive success. Chimpanzees have an even longer period of dependence on their mothers' milk than do humans, and consequently, offspring younger than 4.5–5 years old cannot survive if the mother dies. Most direct maternal investments, such as maternal transportation of infants and sharing of night shelters (beds or nests), end with nutritional weaning. Thus, it had been assumed that a mother's death was no longer critical to the survival of weaned offspring, in contrast to human children, who continue to depend on parental care long after weaning. However, in theory at least, maternal investment in a chimpanzee son after weaning could be beneficial because in chimpanzees' male‐philopatric society, mother and son co‐exist for a long time after the offspring's weaning. Using long‐term demographic data for a wild chimpanzee population in the Mahale Mountains, Tanzania, we show the first empirical evidence that orphaned chimpanzee sons die younger than expected even if they lose their mothers after weaning. This suggests that long‐lasting, but indirect, maternal investment in sons continues several years after weaning and is vital to the survival of the sons. The maternal influence on males in the male‐philopatric societies of hominids may be greater than previously believed. Am J Phys Anthropol, 153:139–143, 2014. © 2013 Wiley Periodicals, Inc.     

Senescence and costs of reproduction in the life history of a small precocial species

Species following a fast life history are expected to express fitness costs mainly as increased mortality, while slow‐lived species should suffer fertility costs. Because observational studies have limited power to disentangle intrinsic and extrinsic factors influencing senescence, we manipulated reproductive effort experimentally in the cavy (Cavia aperea) which produces extremely precocial young. We created two experimental groups: One was allowed continuous reproduction (CR) and the other intermittent reproduction (IR) by removing males at regular intervals. We predicted that the CR females should senesce (and die) earlier and produce either fewer and/or smaller, slower growing offspring per litter than those of the IR group. CR females had 16% more litters during three years than IR females. CR females increased mass and body condition more steeply and both remained higher until the experiment ended. Female survival showed no group difference. Reproductive senescence in litter size, litter mass, and reproductive effort (litter mass/maternal mass) began after about 600 days and was slightly stronger in CR than IR females. Litter size, litter mass, and offspring survival declined with maternal age and were influenced by seasonality. IR females decreased reproductive effort less during cold seasons and only at higher age than CR females. Nevertheless, offspring winter mortality was higher in IR females. Our results show small costs of reproduction despite high reproductive effort, suggesting that under ad libitum food conditions costs depend largely on internal regulation of allocation decisions.     

Influence of maternal characteristics and oceanographic conditions on survival and recruitment probabilities of Weddell seals

For long‐lived animals, maternal age and breeding experience can vary widely and affect offspring survival and recruitment probabilities. In addition, these vital rates may be influenced by annual variation in environmental conditions. We evaluated various hypotheses regarding how offspring survival and recruitment probabilities vary as functions of maternal characteristics and oceanographic conditions, using 25 years of data from a study of individually‐marked Weddell seals in Erebus Bay, Antarctica. We predicted that survival and recruitment would be positively related to maternal age and experience up to some threshold value and considered three hypothesized shapes for the relationship beyond the threshold age (steadily increasing, pseudo‐threshold, or decreasing). We predicted an inverse relationship between maternal age at first reproduction and offspring survival and recruitment probabilities. We predicted that sea‐ice extent, which positively influences primary productivity, would be positively related to annual recruitment probabilities. Results revealed contrasting influences of maternal age on probabilities of survival and recruitment of young. Survival rate was best modeled by a pseudo‐threshold relationship with maternal age, e.g. in 1999, survival rate was estimated as 0.61, 0.69 and 0.72, respectively, for seals born to 6‐, 14‐ and 22‐yr‐old mothers. In contrast, estimated recruitment probability was highest for seals born to young mothers, e.g. recruitment probability for a 7‐yr‐old who had not yet had a pup was estimated as 0.51 vs 0.30, respectively, if she was born to a 6‐ versus a 14‐yr‐old mother. The combined results for offspring survival and recruitment suggest countervailing selection where genotypes favored for reproductive success are generally selected against as juveniles, resulting in high recruitment probabilities for individuals that had low juvenile survival rates. Finally, we found support for our prediction that oceanographic conditions affected annual recruitment rates, but not survival rates. Specifically, annual recruitment probability was positively related to the sea‐ice extent in September of the previous year.     

Trans‐generational effects on ageing in a wild bird population

Ageing, long thought to be too infrequent to study effectively in natural populations, has recently been shown to be ubiquitous, even in the wild. A major challenge now is to explain variation in the rates of ageing within populations. Here, using 49 years of data from a population of great tits (Parus major), we show that offspring life‐history trajectories vary with maternal age. Offspring hatched from older mothers perform better early in life, but suffer from an earlier onset, and stronger rate, of reproductive senescence later in life. Offspring reproductive lifespan is, however, unaffected by maternal age, and the different life‐history trajectories result in a similar fitness payoff, measured as lifetime reproductive success. This study therefore identifies maternal age as a new factor underlying variation in rates of ageing, and, given the delayed trans‐generational nature of this effect, poses the question as to proximate mechanisms linking age‐effects across generations.     

Maternal effects across life stages: larvae experiencing predation risk increase offspring provisioning

1. Maternal provisioning can reduce offspring vulnerability to predators by promoting offspring growth and eliciting of antipredator behaviours. Mothers perceiving predation risk may improve offspring survival if producing larger, higher‐quality offspring. However, empirical evidence suggests that offspring quality is often reduced, probably reflecting predator‐induced physiological costs, or a selfish maternal strategy aimed at producing more offspring by sacrificing their quality. While perception and impact of predators can vary across the prey's life stage, a majority of studies have focused on understanding how reproductive allocation decisions are influenced by the risk of predation during adulthood. 2. In this study, Leptinotarsa decemlineata beetles were used to examine if the risk of predation during the larval stage: (i) impacts the mother's physiological condition, including body mass and metabolic rate; and (ii) alters maternal allocation of reproductive resources to offspring quantity versus quality. 3. Results revealed that L. decemlineata mothers responded to perceived predation risk by producing clutches with fewer but larger eggs, thus increasing offspring provisioning. Surprisingly, while females that had faced predation risk as larva emerged with a similar body mass to control females, they exhibited lower metabolic rates. 4. Although predation risk in L. decemlineata larvae is known to impair their ability to acquire and maintain energy resources, adult females appeared to ameliorate such costs by improving their metabolic efficiency and by allocating more of their limited reproductive resources to produce fewer but better‐quality offspring.     

Maternal caloric restriction partially rescues the deleterious effects of advanced maternal age on offspring

While many studies have focused on the detrimental effects of advanced maternal age and harmful prenatal environments on progeny, little is known about the role of beneficial non‐Mendelian maternal inheritance on aging. Here, we report the effects of maternal age and maternal caloric restriction (CR) on the life span and health span of offspring for a clonal culture of the monogonont rotifer Brachionus manjavacas. Mothers on regimens of chronic CR (CCR) or intermittent fasting (IF) had increased life span compared with mothers fed ad libitum (AL). With increasing maternal age, life span and fecundity of female offspring of AL‐fed mothers decreased significantly and life span of male offspring was unchanged, whereas body size of both male and female offspring increased. Maternal CR partially rescued these effects, increasing the mean life span of AL‐fed female offspring but not male offspring and increasing the fecundity of AL‐fed female offspring compared with offspring of mothers of the same age. Both maternal CR regimens decreased male offspring body size, but only maternal IF decreased body size of female offspring, whereas maternal CCR caused a slight increase. Understanding the genetic and biochemical basis of these different maternal effects on aging may guide effective interventions to improve health span and life span.     

A delay in age at first mating results in the loss of future reproductive potential via apoptosis

Summary Women who delay childbearing risk subfertility. However, this loss of fertility is not a simple function of aging. Women who have had children early in life tend to maintain fertility longer, measured as a later age at menopause. But why should otherwise healthy women lose reproductive capacity? Loss of fertility independent of senescence, menopause, has been approached from two perspectives: evolution and development. Evolutionary biologists focus on how natural selection favors survival after reproductive ability has ceased, whereas reproductive biologists examine mechanisms by which women lose fertility with age and factors that influence the rate of reproductive aging. Combining mechanistic studies with evolutionary theory should allow us to define principles of the evolution of postembryonic development of ovaries, including the role of reproductive timing relative to sexual maturation. Achieving this will require identifying appropriate, and more experimentally tractable, taxa in which to study how early reproductive events influence lifetime fertility. We work with an invertebrate species, the cockroach Nauphoeta cinerea, with a complex reproductive biology in which females experience reproductive cycles, give live birth, and show age‐related decline in fertility. Thus, N. cinerea provides an opportunity to use an experimental approach to examine mechanisms by which females lose reproductive potential as they delay reproduction. Our results demonstrate that the loss of both oocytes ready for fertilization and future oocytes in females that delay mating is because of apoptosis. We suggest that loss of fertility because of delayed mating may originate in a nonadaptive response in control of apoptosis through mistiming of reproduction.     

Life span,reproductive output,and reproductive opportunity in captive Goeldi's monkeys (Callimico goeldii)

In the absence of long‐term field studies, demographic and reproductive records from animals housed in zoos and research laboratories are a valuable tool for the study of life history variables relating to reproduction. In this study, we analyzed studbook records of more than 2,000 individuals born over a 40‐year period (1965–2004) to describe life history patterns of captive Goeldi's monkeys (Callimico goeldii) housed in North America and Europe. Using Kaplan–Meier survival analysis methods, we found the mean life span to be 5.5 years. The rate of infant mortality, defined as death before 30 days, was approximately 30%, with European animals being more likely to survive infancy than North American animals. When individuals surviving at least 1.5 years are considered, lifetime reproductive output averaged 3.5 offspring, yet more than one‐third of individuals did not produce any offspring. Using a smaller dataset of individuals with known pairing histories, we developed a measure of opportunity for reproduction (OFR), which represented the total time an individual was known to be housed with a potential mate. For both sexes, we found that the correlation between OFR and number of offspring produced was much higher than the correlation between life span and number of offspring produced. This result highlights the importance of taking into account an individual's OFR. As a whole, our findings help characterize the life histories of captive Goeldi's monkeys and emphasize the impact management practices may have on reproductive success. Zoo Biol 29:1–15, 2010. © 2009 Wiley‐Liss, Inc.