A Prisoner's Dilemma model of the evolution of paternal care

The heavy energetic demands of gestation, lactation and rearing of offspring mean that studies of paternal care in primates usually focus on female reproductive effort. Here it is shown that both male and female reproductive effort must be considered in order to understand how paternal care evolved. This is done using the Prisoner's Dilemma, best known as a model of reciprocal altruism. It is found that the relative cost of reproduction for males and females is crucially important in determining co-operative and competitive strategies. In particular, when male reproductive costs are less than female reproductive costs, males co-operate with females even when females do not reciprocate. This surprising behaviour, termed non-reciprocal altruism, is comparable with male investment in a female and her offspring.     

Heterogeneity in individual quality overrides costs of reproduction in female reindeer

Reproductive allocation at one age is predicted to reduce the probability of surviving to the next year or to lead to a decrease in future reproduction. This prediction assumes that reproduction involves fitness costs. However, few empirical studies have assessed whether such costs may vary with the age at primiparity or might be overridden by heterogeneities in individual quality. We used data from 35 years’ monitoring of individually marked semi-domestic reindeer females to investigate fitness costs of reproduction. Using multi-state statistical models, we compared age-specific survival and reproduction among four reproductive states (never reproduced, experienced non-breeders, reproduced but did not wean offspring, and reproduced and weaned offspring) and among contrasted age at primiparity. We assessed whether reproductive costs occurred, resulting in a trade-off between current reproduction and future reproduction or survival, and whether early maturation was costly or rather reflected differences in individual quality of survival and reproduction capabilities. We did not find any evidence for fitness costs of reproduction in female reindeer. We found no cost of gestation and lactation in terms of future reproduction and survival. Conversely, successful breeders had higher survival and subsequent reproductive success than experienced non-breeders and unsuccessful breeders, independently of the age at primiparity. Moreover, it was beneficial to mature earlier, especially for females that successfully weaned their first offspring. Successful females at early primiparity remained successful throughout their life, clearly supporting the existence of marked among-female differences in quality. The weaning success peaked for multiparous females and was lower for first-time breeders, indicating a positive effect of experience on reproductive performance. Our findings emphasize an overwhelming importance of individual quality and experience to account for observed variation in survival and reproductive patterns of female reindeer that override trade-offs between current reproduction and future performance, at least in the absence of harsh winters.     

Activity budgets and activity rhythms in red ruffed lemurs (Varecia rubra) on the Masoala Peninsula, Madagascar: seasonality and reproductive energetics

The activity budgets and daily activity rhythms of Varecia rubra were examined over an annual cycle according to season and reproductive stage. Given the relatively high reproductive costs and patchy food resources of this species, I predicted that V. rubra would 1) travel less and feed more during seasonal resource scarcity in an attempt to maintain energy balance, and 2) show sex differences in activity budgets due to differing reproductive investment. Contrary to the first prediction, V. rubra does not increase feeding time during seasonal food scarcity; rather, females feed for a consistent amount of time in every season, whereas males feed most during the resource-rich, hot dry season. The results are consistent with other predictions: V. rubra travels less in the resource-scarce cold rainy season, and there are some pronounced sex differences, with females feeding more and resting less than males in every season and in every reproductive stage except gestation. However, there are also some provocative similarities between the sexes when activity budgets are examined by reproductive stage. During gestation, female and male activity budgets do not differ and appear geared toward energy accumulation: both sexes feed and rest extensively and travel least during this stage. During lactation, activity budgets are geared toward high energy expenditure: both sexes travel most and in equal measure, and rest least, although it remains the case that females feed more and rest less than males. These similarities between female and male activity budgets appear related to cooperative infant care. The high energetic costs of reproduction in V. rubra females may require that they allot more time to feeding year round, and that their overall activity budget be more directly responsive to seasonal climate change, seasonal food distribution, and reproductive schedules.     

No evidence for sex biases in milk macronutrients,energy, or breastfeeding frequency in a sample of filipino mothers

Maternal reproductive investment includes both the energetic costs of gestation and lactation. For most humans, the metabolic costs of lactation will exceed those of gestation. Mothers must balance reproductive investment in any single offspring against future reproductive potential. Among mammals broadly, mothers may differentially invest in offspring based on sex and maternal condition provided such differences investment influence future offspring reproductive success. For humans, there has been considerable debate if there are physiological differences in maternal investment by offspring sex. Two recent studies have suggested that milk composition differs by infant sex, with male infants receiving milk containing higher fat and energy; prior human studies have not reported sex‐based differences in milk composition. This study investigates offspring sex‐based differences in milk macronutrients, milk energy, and nursing frequency (per 24 h) in a sample of 103 Filipino mothers nursing infants less than 18 months of age. We found no differences in milk composition by infant sex. There were no significant differences in milk composition of mothers nursing first‐born versus later‐born sons or daughters or between high‐ and low‐income mothers nursing daughters or sons. Nursing frequency also showed no significant differences by offspring sex, sex by birth order, or sex by maternal economic status. In the Cebu sample, there is no support for sex‐based differences in reproductive investment during lactation as indexed by milk composition or nursing frequency. Further investigation in other populations is necessary to evaluate the potential for sex‐based differences in milk composition among humans. Am J Phys Anthropol 152:209–216, 2013. © 2013 Wiley Periodicals, Inc.     

Survival costs of reproduction predict age-dependent variation in maternal investment

Life-history theory predicts that older females will increase reproductive effort through increased fecundity. Unless offspring survival is density dependent or female size constrains offspring size, theory does not predict variation in offspring size. However, empirical data suggest that females of differing age or condition produce offspring of different sizes. We used a dynamic state-variable model to determine when variable offspring sizes can be explained by an interaction between female age, female state and survival costs of reproduction. We found that when costs depend on fecundity, young females with surplus state increase offspring size and reduce number to minimize fitness penalties. When costs depend on total reproductive effort, only older females increase offspring size. Young females produce small offspring, because decreasing offspring size is less expensive than number, as fitness from offspring investment is nonlinear. Finally, allocation patterns are relatively stable when older females are better at acquiring food and are therefore in better condition. Our approach revealed an interaction between female state, age and survival costs, providing a novel explanation for observed variation in reproductive traits.     

Infant Carrying Behavior in Callitrichid Primates: Callithrix and Leontopithecus

Care of offspring by individuals other than the mother is ubiquitous in callitrichid primates. In spite of its widespread occurrence, however, there is considerable taxonomic variation in the timing and intensity of parental effort by breeding males and nonbreeding juvenile group members. These differences may be attributable to generic and specifies differences in the costs of reproduction for females or in ecological constraints on travel and foraging. We present data on patterns of infant carrying in social groups of two taxa of callitrichid primates (Callithrix and Leontopithecus) throughout the first 3 months of infant life. We evaluated patterns of care in small groups (two or fewer juvenile or subadult helpers) and in large groups (three or more helpers in addition to the breeding adult male and female). Group size had little effect on levels of maternal carrying effort in either marmosets or lion tamarins, and mothers ceased carrying infants by 3 months of age. Carrying efforts by fathers were significantly reduced in groups with many helpers relative to small groups. Helpers carried at consistent rates during the second and third months of infant life in Leontopithecus, while in Callithrix, carrying by helpers peaked during the second month. These results suggest that if helpers reduce energetic demands on lactating females, the mechanism by which helpers reduce these burdens is independent of maternal carrying effort.     

Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can

All female primates incur energetic costs associated with producing and caring for offspring, but females belonging to the New World primate family Callitrichidae, the marmosets and tamarins, appear to face even further demands. In fact, the energetic demands of rearing callitrichid infants are thought to have led to the evolution of cooperative infant care in these species. If this explanation is true, then one might expect that natural selection should also have shaped patterns of maternal behavior to be sensitive to the costs of reproduction and equipped females to reduce their investment in offspring under certain conditions. Therefore, we examined the maternal effort and postpartum endocrine profiles of individual female marmosets (Callithrix kuhlii) across conditions that represented two hallmarks of callitrichid reproduction-conception during the early postpartum period and alloparental assistance. When females conceived during the early postpartum period and faced the upcoming demands of caring for their newly conceived litters (Study 1), they significantly reduced their caregiving effort and had significantly higher postpartum levels of estradiol relative to breeding attempts in which conception occurred later in the postpartum period. Postpartum estradiol was negatively correlated with maternal carrying effort. When experienced alloparents were present (Study 2), females again reduced their caregiving effort relative to breeding attempts in which experienced alloparents were not present. Postpartum cortisol, however, did not vary as a function of experienced alloparental assistance. The results of these studies suggest that female marmosets have been subjected to similar selection pressures as females of other primate taxa--to maximize their reproductive success by reducing their investment in offspring under the worst and best of conditions--and suggest that hormones may mediate within-female variation in maternal care. These studies also provide support for the notion that mothers are "flexible opportunists" when it comes to providing care to their young.     

Effect of mother’s physical condition during pregnancy and lactation on postnatal growth and reproductive success of offspring in water vole <Emphasis Type="Italic">Arvicola terrestris</Emphasis>

Postnatal growth, life span, and probability of reproduction in the adult state depended on the mother’s physical condition during pregnancy and lactation in water vole. The white fat weight in the female abdominal cavity was shown to significantly increase in pregnancy and to decrease in late lactation. As an indicators for nutritional state of females, their body weight difference after parturition (or in late lactation) and expected from the regression equation relating individual body weight at the beginning and the end of each reproductive stage were used (physical condition indexes in pregnancy or lactation). The correlation of the physical condition index in pregnancy with the storage fat weight was 0.67. The metabolic resources of the mother’s body proved to favor faster offspring development. The female offspring weight at the age of 3 and 10 weeks as well as adult ones positively correlated with the mother’s nutritional state in pregnancy, while the male offspring weight demonstrated a similar correlation at the age of 3 and 6 weeks. Increased negative energy balance during lactation proved to decrease the offspring weight in both sexes after separation from mother and at the age of 6 weeks. High nutritional state of mother in pregnancy favored both the probability of reproduction and life span of female offspring. The reproduction of male offspring did not depend on the mother’s physical condition. The life span peaked in male offspring of mothers in a nutritional state below average in pregnancy and above average in lactation. Thus, the physical condition of the mother’s body is an important sex-dependent factor of phenotypic variation in the offspring body weight, reproductive competence, and life span.     

Effect of mother's physical condition during pregnancy and lactation on postnatal growth and reproductive success of offspring in water vole Arvicola terrestris L

Postnatal growth, life span, and probability of reproduction in the adult state depended on the mother's physical condition during pregnancy and lactation in water vole. The white fat weight in the female abdominal cavity was shown to significantly increase in pregnancy and to decrease in late lactation. As an indicators for nutritional state of females, their body weight difference after parturition (or in late lactation) and expected from the regression equation relating individual body weight at the beginning and the end of each reproductive stage were used (physical condition indexes in pregnancy or lactation). The correlation of the physical condition index in pregnancy with the storage fat weight was 0.67. The metabolic resources of the mother's body proved to favor faster offspring development. The female offspring weight at the age of 3 and 10 weeks as well as adult ones positively correlated with the mother's nutritional state in pregnancy, while the male offspring weight demonstrated a similar correlation at the age of 3 and 6 weeks. Increased negative energy balance during lactation proved to decrease the offspring weight in both sexes after separation from mother and at the age of 6 weeks. High nutritional state of mother in pregnancy favored both the probability of reproduction and life span of female offspring. The reproduction of male offspring did not depend on the mother's physical condition. The life span peaked in male offspring of mothers in a nutritional state below average in pregnancy and above average in lactation. Thus, the physical condition of the mother's body is an important sex-dependent factor of phenotypic variation in the offspring body weight, reproductive competence, and life span.     

Reproductive Decisions in Female European Ground Squirrels: Factors Affecting Reproductive Output and Maternal Investment

Physiological and behavioural parameters associated with reproductive effort and success were investigated in female European ground squirrels Spermophilus citellus . The proportion of reproductive (lactating) females in the study population was over 90% and was not related to age. Timing of oestrus and ovulation was found to be affected by the female's emergence date and condition. Females with low emergence mass showed delayed oestrus. Differences in ovulation dates were shown to affect reproductive output in terms of litter size and sex ratio. Early litters were larger and male biased. X-ray techniques were used to determine intrauterine litter size in individual females. The results indicated that litter size and sex ratio were fixed prenatally. Lactation costs were reflected in the intensity of mass loss and duration of lactation. Mass loss varied with litter size, in that females with large litters showed a more rapid loss than others. The second parental investment parameter, lactation duration, varied among individual females and was dependent on the timing of reproduction and litter size (except yearlings). Early born litters, which were, in most cases, larger than later ones, were nursed longer. Prolonged lactation periods affected female condition in that they started prehibernation fattening later and entered hibernation with a lower mass than individuals that had shorter lactation periods. Yearling females probably could not afford the energetic costs of long lactation, independent of their offspring number. These results indicated that females with higher reproductive output and higher investment were unable to compensate these costs before hibernation. Consequences for these individuals could therefore be lower over-winter survival or a delayed oestrus in the following season.     

Differences in Patterns of Reproductive Allocation between the Sexes in Nicrophorus orbicollis

Organisms are selected to maximize lifetime reproductive success by balancing the costs of current reproduction with costs to future survival and fecundity. Males and females typically face different reproductive costs, which makes comparisons of their reproductive strategies difficult. Burying beetles provide a unique system that allows us to compare the costs of reproduction between the sexes because males and females are capable of raising offspring together or alone and carcass preparation and offspring care represent the majority of reproductive costs for both sexes. Because both sexes perform the same functions of carcass preparation and offspring care, we predict that they would experience similar costs and have similar life history patterns. In this study we assess the cost of reproduction in male Nicrophorus orbicollis and compare to patterns observed in females. We compare the reproductive strategies of single males and females that provided pre- and post-hatching parental care. There is a cost to reproduction for both males and females, but the sexes respond to these costs differently. Females match brood size with carcass size, and thus maximize the lifetime number of offspring on a given size carcass. Males cull proportionately more offspring on all carcass sizes, and thus have a lower lifetime number of offspring compared to females. Females exhibit an adaptive reproductive strategy based on resource availability, but male reproductive strategies are not adaptive in relation to resource availability.     

Costs of reproduction and terminal investment by females in a semelparous marsupial

Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20-40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.     

Behavioral Energetics of Lactation in a Herbivorous Carnivore,the Red Panda (Ailurus fulgens)

In most mammals, the energetic costs of lactation significantly increase a female's daily energy requirements. Previous research indicates that such energetic costs may be met through changes in increased food consumption ranging from around 35 % to 150 %. In this paper, changes in food intake during lactation are measured in the red panda (Ailurus fulgens), a species of the order Carnivora which possesses a digestive system suited for a carnivorous diet but yet exclusively feeds on bamboo. Four feeding characteristics were studied: duration of feeding bouts, number of bamboo leaves consumed per mouthful, number of bamboo leaves consumed per minute, and interval between mouthfuls of bamboo. In three lactating females, three of four feeding behaviors significantly increased up to 200 % above the rate observed during non-lactation. Males showed no change in feeding behavior during the same reproductive months with identical available foods. Red pandas appear to suffer a more severe energetic cost during lactation (at least with respect to food consumption) than other mammals previously studied. This may relate to their inefficient digestive capacity to process a herbivorous diet of bamboo. The data presented here suggest that general discussions of the relative costs of reproduction and in turn parental investment should include a female's relative digestive efficiency during stressful reproductive periods.     

Brood desertion by female shorebirds: a test of the differential parental capacity hypothesis on Kentish plovers.

The aim of this study was to examine whether the energetic costs of reproduction explain offspring desertion by female shorebirds, as is suggested by the differential parental capacity hypothesis. A prediction of the hypothesis is that, in species with biparental incubation in which females desert from brood care after hatching, the body condition of females should decline after laying to a point at which their body reserves are too low for continuing parental care. We tested this prediction on Kentish plovers (Charadrius alexandrinus) in which both sexes incubate but the females desert from brood care before the chicks fledge. We found no changes in either the body masses or body compositions of both individual male and female plovers from early incubation and throughout early chick rearing. Furthermore, the timing of brood desertion by females was not affected by their body condition. Neither did we find gender differences in the energetic costs of incubation. There were no differences in the timing of brood desertion between experimental and control females in an experiment in which we lengthened or shortened the duration of incubation by one week. These results indicate that energetic costs do not explain offspring desertion by female Kentish plovers and that the needs of chicks for parental care rather than cumulative investment by females is what determines the timing of brood desertion.     

The ecology of motherhood: the structuring of lactation costs by chacma baboons

1. Data from a long-term study of Papio hamadryas ursinus (L.) in the De Hoop Nature Reserve, Western Cape, South Africa, were used to test the assumptions and predictions of Altmann's model of maternal time budgets. 2. Female baboons' feeding time was below model predictions, and there was no evidence for a consistent increase in feeding time with infant age. In addition, female feeding time was not significantly higher than observed baseline feeding times for nonlactating females. 3. Female baboons reduced activity levels in the first few months post-partum, as reflected in significant increases in resting time, and there was some indication that females lost body mass over the course of lactation. When feeding demand was high, females sacrificed social time, and conserved resting time. 4. Females increased vigilance levels during the first 4 months of infant life and were more vigilant overall during lactation than when nonlactating. There was a negative relationship between feeding time and vigilance, but a positive relationship between resting time and vigilance. 5. Female baboons at De Hoop appear to cope with the energetic costs of lactation by reducing activity levels, although this cannot compensate completely for increased energetic costs. This may not be so much an'energy-sparing' strategy as a response to threats presented by infanticidal males in this population. Females therefore trade-off feeding time against vigilance.     

The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus)

In mammals, reproduction, especially for females is energetically demanding. Therefore, during the reproductive period females could potentially adjust patterns of thermoregulation and foraging in concert to minimise the energetic constraints associated with pregnancy and lactation. We assessed the influence of pregnancy, lactation, and post-lactation on torpor use and foraging behaviour by female little brown bats, Myotis lucifugus. We measured thermoregulation by recording skin temperature and foraging by tracking bats which carried temperature-sensitive radio-tags. We found that individuals, regardless of reproductive condition, used torpor, but the patterns of torpor use varied significantly between reproductive (pregnant and lactating) females and post-lactating females. As we predicted, reproductive females entered torpor for shorter bouts than post-lactating females. Although all females used torpor frequently, pregnant females spent less time in torpor, and maintained higher skin temperatures than either lactating or post-lactating females. This result suggests that delayed offspring development which has been associated with torpor use during pregnancy, may pose a higher risk to an individual’s reproductive success than reduced milk production during lactation. Conversely, foraging behaviour of radio-tagged bats did not vary with reproductive condition, suggesting that even short, shallow bouts of torpor produce substantial energy savings, likely obviating the need to spend more time foraging. Our data clearly show that torpor use and reproduction are not mutually exclusive and that torpor use (no matter how short or shallow) is an important means of balancing the costs of reproduction for M. lucifugus.     

Direct Male Care and Hominin Evolution: Why Male–Child Interaction Is More Than a Nice Social Idea

ABSTRACT  Early members of the genus Homo experienced heightened absolute metabolic costs, partially owing to increases in body size. However, as is characteristic of modern humans, they also likely began reproducing with shortened interbirth intervals. Male investment in offspring may help explain how this life history shift occurred. Evolutionary models of hominin male investment in offspring have traditionally focused on provisioning of females and young, yet the extent to which direct male care of offspring was evolutionarily important, from an energetic perspective, is largely unaddressed. I propose an evolutionary model of direct male care, demonstrating that males could have helped reduce the energetic burden of caregiving placed on mothers by carrying young. In doing so, males would have assisted females in achieving and maintaining an energetic condition sufficient for reproduction, thereby hastening the advent of shortened interbirth intervals that played a formative role in the success of our genus.     

Strategic female reproductive investment in response to male attractiveness in birds

Life-history theory predicts that individuals should adjust their reproductive effort according to the expected fitness returns on investment. Because sexually selected male traits should provide honest information about male genetic or phenotypic quality, females may invest more when paired with attractive males. However, there is substantial disagreement in the literature whether such differential allocation is a general pattern. Using a comparative meta-regression approach, we show that female birds generally invest more into reproduction when paired with attractive males, both in terms of egg size and number as well as food provisioning. However, whereas females of species with bi-parental care tend to primarily increase the number of eggs when paired with attractive males, females of species with female-only care produce larger, but not more, eggs. These patterns may reflect adaptive differences in female allocation strategies arising from variation in the signal content of sexually selected male traits between systems of parental care. In contrast to reproductive effort, female allocation of immune-stimulants, anti-oxidants and androgens to the egg yolk was not consistently increased when mated to attractive males, which probably reflects the context-dependent costs and benefits of those yolk compounds to females and offspring.     

Energetics of age-specific reproductive effort in female Harp seals, Phoca groenlandica

The theory of reproductive effort is commonly viewed in the perspective of the cost of offspring to the parent. This interpretation predicts that older females make a greater reproductive effort than younger females, for whom the cost of lost future offspring is less. The benefit early-born offspring represent in future generations is greater than that of late-born offspring in most natural populations, so, alternatively, young females should make a greater reproductive effort. These hypotheses were investigated in nursing Harp seals by examining age-specific reproductive effort in terms of energetic maternal investment.
Younger Harp seal females lost weight at the same rate as did older females. Moreover. since younger, growing females tended to start lactation with less blubber than older females. weight loss during 10 days (d) of lactation represented a greater proportion of stored energy for young females. A successfully weaned pup, therefore, constituted a greater reproductive effort for them than for older females, consistent with benefit–oriented predictions from theory.
A model is presented to outline the components of an annual energy budget for female Harp seals in the context of reproductive effort. This model indicates that young females may devote a greater proportion of their annual net energy to reproduction and take a greater risk of lost future reproduction. It also identifies areas of inadequacy of existing data on pinniped energy budgets.     

Reproductive resilience to food shortage in a small heterothermic primate

The massive energetic costs entailed by reproduction in most mammalian females may increase the vulnerability of reproductive success to food shortage. Unexpected events of unfavorable climatic conditions are expected to rise in frequency and intensity as climate changes. The extent to which physiological flexibility allows organisms to maintain reproductive output constant despite energetic bottlenecks has been poorly investigated. In mammals, reproductive resilience is predicted to be maximal during early stages of reproduction, due to the moderate energetic costs of ovulation and gestation relative to lactation. We experimentally tested the consequences of chronic-moderate and short-acute food shortages on the reproductive output of a small seasonally breeding primate, the grey mouse lemur (Microcebus murinus) under thermo-neutral conditions. These two food treatments were respectively designed to simulate the energetic constraints imposed by a lean year (40% caloric restriction over eight months) or by a sudden, severe climatic event occurring shortly before reproduction (80% caloric restriction over a month). Grey mouse lemurs evolved under the harsh, unpredictable climate of the dry forest of Madagascar and should thus display great potential for physiological adjustments to energetic bottlenecks. We assessed the resilience of the early stages of reproduction (mating success, fertility, and gestation) to these contrasted food treatments, and on the later stages (lactation and offspring growth) in response to the chronic food shortage only. Food deprived mouse lemurs managed to maintain constant most reproductive parameters, including oestrus timing, estrogenization level at oestrus, mating success, litter size, and litter mass as well as their overall number of surviving offspring at weaning. However, offspring growth was delayed in food restricted mothers. These results suggest that heterothermic, fattening-prone mammals display important reproductive resilience to energetic bottlenecks. More generally, species living in variable and unpredictable habitats may have evolved a flexible reproductive physiology that helps buffer environmental fluctuations.