Bone loss is a physiological cost of reproduction in white-footed mice (Peromyscus leucopus)

Investment in offspring production often requires the mobilization of endogenous resources, a strategy that may negatively impact maternal condition. In mammals, skeletal ossification in growing offspring requires a large investment of calcium by mothers, and bone loss has been described in several species as a means of supporting this demand. Although bone loss can have adverse effects on the mother, its potential role in a reproductive trade-off has not been addressed. Using white-footed mice (Peromyscus leucopus), we tested the effect of dietary calcium availability on maternal skeletal condition during reproduction to assess if calcium availability drives a trade-off between maternal skeletal condition and offspring production. We provided mice with a low-calcium or standard diet and monitored reproductive output along with changes in bone mineral density and bone resorption (via serum concentrations of pyridinoline cross-links) throughout reproduction. Reproductive performance was not impaired by low calcium intake. Reproductive females on the low-calcium diet showed a significant reduction in bone mineral density relative to reproductive females consuming the standard diet and non-reproductive mice consuming the low-calcium diet, but no difference in bone resorptive activity. Our results suggest that when dietary calcium is limited white-footed mice reproduce at the expense of their skeletal condition, and may do so by limiting bone mineral accretion relative to resorption.     

Maternal size and age affect offspring sex ratio in the solitary egg parasitoid Anaphes nitens

In this study, the effects of maternal age, diet, and size on offspring sex ratio were investigated for the solitary egg parasitoid, Anaphes nitens Girault (Hymenoptera: Mymaridae), both outdoors, during the winter, and inside a climatic chamber under favourable constant conditions. During the winter of 2005–2006, each of seven groups containing 40 1‐day‐old females was mated and randomly distributed among two treatments: (treatment 1) a droplet of undiluted honey ad libitum + one fresh egg capsule of the snout beetle Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae) as host; (treatment 2) drops of water + one fresh egg capsule of G. scutellatus. We recorded the lifetime fecundity, the daily sex allocation, and the lifetime offspring sex ratio to study the existence of a relationship with maternal characteristics. Moreover, we assessed the effect of location (outdoors vs. indoors) and group (groups are representative of early, mid, and late winter) on sex ratio. The most important factor that biased the sex ratio was maternal body size: larger females of both treatments produced more female offspring. As females of A. nitens could gain more advantage than males from body size, larger mothers have a higher fitness return if they produce more daughters. The effect of the treatment was significant: starved females produced more females. Location and group were not significant. Fecundity and sex ratio were age dependent. Old mothers that received honey (treatment 1) had fewer offspring and a more male‐biased offspring sex ratio, probably due to reproductive senescence and sperm depletion. Starved females (treatment 2) experienced reproductive decline earlier, perhaps because they invested more energy in maintenance rather than in reproduction.     

Evaluating the contributions of change in investment and change in efficiency to age‐related declines in male and female reproduction

It is commonly observed that reproduction decreases with age, often at a different rate in males and females. This phenomenon is generally interpreted as senescence. Such reproductive declines may stem from at least two sources: a change in resource allocation and a decline in the ability to convert resources into offspring. This distinction is important because a shift in resource allocation may be favoured by selection, while reduced efficiency is purely deleterious. We propose a way to distinguish whether a decline in reproduction is purely deleterious based on estimating reproductive investment, output, and their ratio, efficiency. We apply this approach to the hermaphroditic snail Physa acuta and demonstrate that both male and female functions decline with age. The male decline largely stems from reduced investment into male activity while female decline is due to increased reproductive inefficiency. This shows that age‐related declines in reproduction can occur for a number of different reasons, a distinction that is usually masked by the general term ‘senescence’. This approach could be applied to any species to evaluate age‐related reproductive decline. We advocate that future studies measure age trajectories of reproductive investment and output to explore the potential processes hidden behind the observation that reproduction declines with age.     

Size delays female senescence in a medium sized marsupial: The effects of maternal traits on annual fecundity in the northern brown bandicoot (Isoodon macrourus)

The degree to which females allocate resources between current reproduction, future fecundity and survival is a central theme in life history theory. We investigated two hypotheses proposed to explain patterns of reproductive investment, terminal investment and senescence, by examining the effects of maternal traits (age and maternal mass) on annual fecundity in female northern brown bandicoots, Isoodon macrourus (Marsupialia: Peramelidae). We found that annual fecundity in females declined in their final year of reproduction, indicating reproductive senescence. Maternal mass significantly influenced the rate of senescence and, in turn, a female's lifetime reproductive output. Mass had little effect on fecundity in 1st and 2nd year females, but a positive relationship with fecundity in 3rd year females. This meant that heavy, 3rd year females did not suffer the decline in fecundity shown in light 3rd year females. For 1st year females, mass and leg length increased between their first and second reproductive seasons, indicating a temporary shift, from the allocation of resources to reproduction, to increasing condition or structural size post their first breeding event. There were no net changes to body mass in subsequent years. We suggest that this year of post‐reproductive growth has important consequences for senescent effects on reproduction. Overall, results provided support for the effects of senescence on annual fecundity. Our findings were not consistent with the terminal investment hypothesis; reproductive output did not increase in females' final reproductive season despite a rapid decline in survival. However, this notion cannot be entirely dismissed; other measures of reproductive performance not examined here (e.g. offspring mass) may have provided an indication that females did increase their effort at the end of their lifespan. This study highlights the difficulty of measuring reproductive costs and the importance of understanding the combined effects of specific characteristics of an individual when interpreting reproductive strategies in iteroparous organisms.     

Facultative Sex Allocation and Sex‐Specific Offspring Survival in Barrow's Goldeneyes

Sex allocation theory predicts that females should bias their reproductive investment towards the sex generating the greatest fitness returns. The fitness of male offspring is often more dependent upon maternal investment, and therefore, high‐quality mothers should invest in sons. However, the local resource competition hypothesis postulates that when offspring quality is determined by maternal quality or when nest site and maternal quality are related, high‐quality females should invest in the philopatric sex. Waterfowl – showing male‐biased size dimorphism but female‐biased philopatry – are ideal for differentiating between these alternatives. We utilized molecular sexing methods and high‐resolution maternity tests to study the occurrence and fitness consequences of facultative sex allocation in Barrow's goldeneyes (Bucephala islandica). We determined how female structural size, body condition, nest‐site safety and timing of reproduction affected sex allocation and offspring survival. We found that the overall sex ratio was unbiased, but in line with the local resource competition hypothesis, larger females produced female‐biased broods and their broods survived better than those of smaller females. This bias occurred despite male offspring being larger and tending to have lower post‐hatching survival. The species shows strong female breeding territoriality, so the benefit of inheriting maternal quality by philopatric daughters may exceed the potential mating benefit for sons of high‐quality females.     

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.     

You are what your mother eats: evidence for maternal preconception diet influencing foetal sex in humans

Facultative adjustment of sex ratios by mothers occurs in some animals, and has been linked to resource availability. In mammals, the search for consistent patterns is complicated by variations in mating systems, social hierarchies and litter sizes. Humans have low fecundity, high maternal investment and a potentially high differential between the numbers of offspring produced by sons and daughters: these conditions should favour the evolution of facultative sex ratio variation. Yet little is known of natural mechanisms of sex allocation in humans. Here, using data from 740 British women who were unaware of their foetus's gender, we show that foetal sex is associated with maternal diet at conception. Fifty six per cent of women in the highest third of preconceptional energy intake bore boys, compared with 45% in the lowest third. Intakes during pregnancy were not associated with sex, suggesting that the foetus does not manipulate maternal diet. Our results support hypotheses predicting investment in costly male offspring when resources are plentiful. Dietary changes may therefore explain the falling proportion of male births in industrialized countries. The results are relevant to the current debate about the artificial selection of offspring sex in fertility treatment and commercial 'gender clinics'.     

The song of the old mother: Reproductive senescence in female drosophila

Among animals with multiple reproductive episodes, changes in adult condition over time can have profound effects on lifetime reproductive fitness and offspring performance. The changes in condition associated with senescence can be particularly acute for females who support reproductive processes from oogenesis through fertilization. The pomace fly Drosophila melanogaster is a well-established model system for exploring the physiology of reproduction and senescence. In this review, we describe how increasing maternal age in Drosophila affects reproductive fitness and offspring performance as well as the genetic foundation of these effects. Describing the processes underlying female reproductive senescence helps us understand diverse phenomena including population demographics, condition-dependent selection, sexual conflict, and transgenerational effects of maternal condition on offspring fitness. Understanding the genetic basis of reproductive senescence clarifies the nature of life-history trade-offs as well as potential ways to augment and/or limit female fertility in a variety of organisms.     

The song of the old mother: Reproductive senescence in female drosophila

Among animals with multiple reproductive episodes, changes in adult condition over time can have profound effects on lifetime reproductive fitness and offspring performance. The changes in condition associated with senescence can be particularly acute for females who support reproductive processes from oogenesis through fertilization. The pomace fly Drosophila melanogaster is a well-established model system for exploring the physiology of reproduction and senescence. In this review, we describe how increasing maternal age in Drosophila affects reproductive fitness and offspring performance as well as the genetic foundation of these effects. Describing the processes underlying female reproductive senescence helps us understand diverse phenomena including population demographics, condition-dependent selection, sexual conflict, and transgenerational effects of maternal condition on offspring fitness. Understanding the genetic basis of reproductive senescence clarifies the nature of life-history trade-offs as well as potential ways to augment and/or limit female fertility in a variety of organisms.     

Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women

Evolutionary theory of senescence emphasizes the importance of intense selection on early reproduction owing to the declining force of natural selection with age that constrains lifespan. In humans, recent studies have, however, suggested that late-life mortality might be more closely related to late rather than early reproduction, although the role of late reproduction on fitness remains unclear. We examined the association between early and late reproduction with longevity in historical post-reproductive Sami women. We also estimated the strength of natural selection on early and late reproduction using path analysis, and the effect of reproductive timing on offspring survival to adulthood and maternal risk of dying at childbirth. We found that natural selection favoured both earlier start and later cessation of reproduction, and higher total fecundity. Maternal age at childbirth was not related to offspring or maternal survival. Interestingly, females who produced their last offspring at advanced age also lived longest, while age at first reproduction and total fecundity were unrelated to female longevity. Our results thus suggest that reproductive and somatic senescence may have been coupled in these human populations, and that selection could have favoured late reproduction. We discuss alternative hypotheses for the mechanisms which might have promoted the association between late reproduction and longevity.     

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.     

Effects of calcium availability on reproductive output of big brown bats

Reproduction is a period of high calcium demand in vertebrates; therefore, calcium deficiency can limit reproductive output in mammals. Nutritional analyses show that insects are a poor calcium source, suggesting that insectivorous species are more likely to be calcium deficient. During pregnancy, big brown bats Eptesicus fuscus consume between 8 and 18 times less calcium than they are estimated to require. To accommodate calcium demand during pregnancy, many mammals mobilize more calcium from the skeleton, and extensive bone loss has been observed in some bats during pregnancy. A conflict may arise between the female and developing embryo over allocation of limited calcium supplies, which could limit reproductive output with respect to offspring size, mass and number. The effects of calcium deficiency on these three factors were tested by providing pregnant captive big brown bats with either a calcium-deficient diet or a diet providing the daily calcium requirement, as estimated for pregnant big brown bats, from the time of capture until parturition. Neonates were compared between groups for size, mass and number per female, as were the effects of maternal mass and size on neonate mass and size. Maternal mass and litter mass were positively related for the calcium-deficient group, but not for the calcium-supplemented group. This suggests that there is some interaction between maternal mass and calcium availability, most likely due to the relationship between body mass and skeletal mass, and that calcium availability is limiting the overall biomass of young that a female can produce.     

Mothers adjust offspring sex to match the quality of the rearing environment

Theory predicts that mothers should adjust offspring sex ratios when the expected fitness gains or rearing costs differ between sons and daughters. Recent empirical work has linked biased offspring sex ratios to environmental quality via changes in relative maternal condition. It is unclear, however, whether females can manipulate offspring sex ratios in response to environmental quality alone (i.e. independent of maternal condition). We used a balanced within-female experimental design (i.e. females bred on both low- and high-quality diets) to show that female parrot finches (Erythrura trichroa) manipulate primary offspring sex ratios to the quality of the rearing environment, and not to their own body condition and health. Individual females produced an unbiased sex ratio on high-quality diets, but over-produced sons in poor dietary conditions, even though they maintained similar condition between diet treatments. Despite the lack of sexual size dimorphism, such sex ratio adjustment is in line with predictions from sex allocation theory because nutritionally stressed foster sons were healthier, grew faster and were more likely to survive than daughters. These findings suggest that mothers may adaptively adjust offspring sex ratios to optimally match their offspring to the expected quality of the rearing environment.     

Maternal correlates of brood sex ratio variation in the lekking lance-tailed manakin Chiroxiphia lanceolata

Theory predicts that overall population sex ratios should be around parity. But when individual females can receive higher fitness from offspring of one sex, they may benefit by biasing their brood sex ratios accordingly. In lekking species, higher variance in male reproductive success relative to that of females predicts that male offspring gain disproportionately from favorable rearing conditions. Females should therefore produce male-biased broods when they are in a position to raise higher quality offspring: i.e., in better body condition or when they reproduce earlier in the breeding season. To investigate these hypotheses, we studied brood sex ratios of lance-tailed manakins Chiroxiphia lanceolata . We found that overall sex ratios and mean brood sex ratios were not different from random expectation. Brood sex ratios were not related to laying date or female body condition. However, we detected a quadratic relationship between brood sex ratios and maternal age: both young (1–2 years) and old (8+ years) females produced female-biased brood sex ratios. This relationship was most clear in a year also distinguished by early rainy and breeding seasons. We suggest that breeding inexperience in young females and senescence in older females is the most plausible explanation for these results, and that the relationship between female age and brood sex ratio is mediated by environmental conditions.     

Does the differential cost of sons and daughters lead to sex ratio adjustment in great frigatebirds Fregataminor?

Sex allocation theory predicts that if benefits of producing sons and daughters differ and outweigh the costs of sex ratio adjustment, parents should produce more of the offspring that provide them with greater fitness. Potential benefits may be more likely to outweigh costs where sexual size dimorphism and, in birds, single‐egg clutches exist. Great frigatebirds Fregataminor are seabirds in which females are larger than males and clutch size is one egg. In our study population, sexual size dimorphism develops primarily during the period of complete juvenile dependence on parental care, consistent with a higher cost of producing daughters than sons. Over the course of the 1998 breeding season there was a shift from early season prevalence of daughters to late‐season prevalence of sons. Variation in food availability at time of egg laying, as indexed by sea surface temperature (SST), was a strong predictor of offspring sex in 1998. In contrast, SST in 2003 was not a predictor of offspring sex, nor was there a seasonal shift in the hatching sex ratio, despite a seasonal shift in SST. Besides food availability, we tested two additional factors in 2003 that could explain sex ratio adjustment in relation to the cost of reproduction. Offspring sex in 2003 was not related to natural or experimentally induced variation in maternal body condition; pre‐laying food supplements raised the body condition of females at the time of egg laying but did not affect offspring sex or egg mass. In addition, offspring sex was not predicted by the length of maternal telomere restriction fragments (TRFs), an index of age and possibly of reproductive experience. Broad confidence intervals on effect size suggest that undetected effects of maternal condition on offspring sex ratio could easily exist, but confidence intervals were narrower on the non‐significant effects of SST and TRF length on offspring sex ratio. The cause of different seasonal patterns of hatching sex ratio and different SST effects in 1998 and 2003 is unclear.     

An offspring signal of quality affects the timing of future parental reproduction

Solicitation signals by offspring are well known to influence parental behaviour, and it is commonly assumed that this behavioural effect translates into an effect on residual reproduction of parents. However, this equivalence assumption concerning behavioural and reproductive effects caused by offspring signals remains largely untested. Here, we tested the effect of a chemical offspring signal of quality on the relative timing and amount of future reproduction in the European earwig (Forficula auricularia). We manipulated the nutritional condition of earwig nymphs and exposed females to their extract, or to solvent as a control. There were no significant main effects of exposure treatment on 2nd clutch production, but exposure to extracts of well-fed nymphs induced predictable timing of the 2nd relative to the 1st clutch. This result demonstrates for the first time that an offspring signal per se, in the absence of any maternal behaviour, affects maternal reproductive timing, possibly through an effect on maternal reproductive physiology.     

Reproductive success and failure: the role of winter body mass in reproductive allocation in Norwegian moose

A life history strategy that favours somatic growth over reproduction is well known for long-lived iteroparous species, especially in unpredictable environments. Risk-sensitive female reproductive allocation can be achieved by a reduced reproductive effort at conception, or the subsequent adjustment of investment during gestation or lactation in response to unexpected environmental conditions or resource availability. We investigated the relative importance of reduced investment at conception compared with later in the reproductive cycle (i.e. prenatal, perinatal or neonatal mortality) in explaining reproductive failure in two high-density moose (Alces alces) populations in southern Norway. We followed 65 multiparous, global positioning system (GPS)-collared females throughout the reproductive cycle and focused on the role of maternal nutrition during gestation in determining reproductive success using a quasi-experimental approach to manipulate winter forage availability. Pregnancy rates in early winter were normal (≥0.8) in all years while spring calving rates ranged from 0.4 to 0.83, with prenatal mortality accounting for most of the difference. Further losses over summer reduced autumn recruitment rates to 0.23–0.69, despite negligible predation. Over-winter mass loss explained variation in both spring calving and autumn recruitment success better than absolute body mass in early or late winter. Although pregnancy was related to body mass in early winter, overall reproductive success was unrelated to pre-winter body condition. We therefore concluded that reproductive success was limited by winter nutritional conditions. However, we could not determine whether the observed reproductive allocation adjustment was a bet-hedging strategy to maximise reproduction without compromising survival or whether females were simply unable to invest more resources in their offspring.     

Survival and reproduction when food is scarce: implications for a lekking Hawaiian Drosophila

Abstract.  1. In insects, larval diet can have a major impact on development, survival, and reproductive success. However, resource availability at the adult phase of the life cycle is also likely to have strong effects in species where there is an extended period of sexual maturation following adult eclosion.
2. The effect of diet on the survival and reproductive success of the lekking Hawaiian fruit fly, Drosophila grimshawi , was explored. Two generations of emerging adults were exposed to one of two feeding regimes: 'constant' and 'varied' (corresponding to food 'each day' or 'every other day' respectively). The impact of resource availability on survival and reproductive success in each generation was then investigated.
3. The probability of survival to 5 weeks old was higher for individuals fed a constant diet than individuals fed a varied diet, but was comparable for males and females.
4. There was a significant maternal effect on offspring survival. Offspring whose mothers were reared on a constant feeding regime had higher survival than offspring whose mothers were reared on a varied diet.
5. There was no relationship between feeding regime and the quantity of pheromones deposited by males (a measure of male reproductive investment); however F₂ sons were more likely to deposit pheromones and deposited a larger quantity of pheromone than their F₁ sires. The number and sex ratio of offspring (a measure of female reproductive effort) emerging from the F₁ generation was unrelated to maternal or paternal feeding regime.
6. The implications of variation in the foraging environment for mate choice in D. grimshawi are discussed.     

Co‐foundress confinement elicits kinship effects in a naturally sub‐social parasitoid

Kinship among interacting individuals is often associated with sociality and also with sex ratio effects. Parasitoids in the bethylid genus Goniozus are sub‐social, with single foundress females exhibiting post‐ovipositional maternal care via short‐term aggressive host and brood defence against conspecific females. Due to local mate competition (LMC) and broods normally being produced by a single foundress, sex ratios are female‐biased. Contests between adult females are, however, not normally fatal, and aggression is reduced when competing females are kin, raising the possibility of multi‐foundress reproduction on some hosts. Here, we screen for further life‐history effects of kinship by varying the numbers and relatedness of foundresses confined together with a host resource and also by varying the size of host. We confined groups of 1–8 Goniozus nephantidis females together with a host for 5+ days. Multi‐foundress groups were either all siblings or all nonsiblings. Our chief expectations included that competition for resources would be more intense among larger foundress groups but diminished by both larger host size and closer foundress relatedness, affecting both foundress mortality and reproductive output. From classical LMC theory, we expected that offspring group sex ratios would be less female‐biased when there were more foundresses, and from extended LMC theory, we expected that sex ratios would be more female‐biased when foundresses were close kin. We found that confinement led to the death of some females (11% overall) but only when host resources were most limiting. Mortality of foundresses was less common when foundresses were siblings. Developmental mortality among offspring was considerably higher in multi‐foundress clutches but was unaffected by foundress relatedness. Groups of sibling foundresses collectively produced similar numbers of offspring to nonsibling groups. There was little advantage for individual females to reproduce in multi‐foundress groups: single foundresses suppressed even the largest hosts presented and had the highest per capita production of adult offspring. Despite single foundress reproduction being the norm, G. nephantidis females in multi‐foundress groups appear to attune sex allocation according to both foundress number and foundress relatedness: broods produced by sibling foundresses had sex ratios similar to broods produced by single foundresses (ca. 11% males), whereas the sex ratios of broods produced by nonsibling females were approximately 20% higher and broadly increased with foundress number. We conclude that relatedness and host size may combine to reduce selection against communal reproduction on hosts and that, unlike other studied parasitoids, G. nephantidis sex ratios conform to predictions of both classical and extended LMC theories.     

Tradeoff between offspring mass and subsequent reproduction in a highly iteroparous mammal

When resources are limited, current maternal investment should reduce subsequent reproductive success or survival. We used longitudinal data on marked mountain goats Oreamnos americanus to assess if offspring mass at weaning affected maternal survival and future reproduction. Offspring mass was positively correlated with survival of old mothers, suggesting that mothers produced lighter kids, and hence reduced reproductive effort, in their last reproduction. Offspring mass at weaning did not affect survival of young and prime‐aged mothers, but females that had weaned heavy offspring had a reduced probability of subsequent reproduction in years of low population density. Because offspring survival is correlated with weaning mass, mothers’ allocation to reproduction involves a tradeoff between current and future fitness returns. We demonstrate for the first time that allocation to current offspring mass in an iteroparous mammal reduces the probability of subsequent reproduction.