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In its initial form, the expensive son hypothesis postulates that sons from male-biased sexually dimorphic species require more food during growth than daughters, which ultimately incur fitness costs for mothers predominantly producing and rearing sons. We first dissect the evolutionary framework in which the expensive son hypothesis is rooted, and we provide a critical reappraisal of its differences from other evolutionary theories proposed in the field of sex allocation. Then, we synthesize the current (and absence of) support for the costs of producing and rearing sons on maternal fitness components (future reproduction and survival). Regarding the consequences in terms of future reproduction, we highlight that species with pronounced sexual size dimorphism display a higher cost of sons than of daughters on subsequent reproductive performance, at least in mammals. However, in most studies, the relative fitness costs of producing and rearing sons and daughters can be due to sex-biased maternal allocation strategies rather than differences in energetic demands of offspring, which constitutes an alternative mechanism to the expensive son hypothesis stricto sensu. We observe that empirical studies investigating the differential costs of sons and daughters on maternal survival in non-human animals remain rare, especially for long-term survival. Indeed, most studies have investigated the influence of offspring sex (or litter sex ratio) at year T on survival at year T + 1, and they rarely provide a support to the expensive son hypothesis. On the contrary, in humans, most studies have focused on the relationship between proportion of sons and maternal lifespan, but these results are inconsistent. Our study highlights new avenues for future research that should provide a comprehensive view of the expensive son hypothesis, by notably disentangling the effects of offspring behaviour from the effect of sex-specific maternal allocation. Moreover, we emphasize that future studies should also embrace the mechanistic side of the expensive son hypothesis, largely neglected so far, by deciphering the physiological pathways linking son's production to maternal health and fitness., (© 2024 The Author(s). Journal of Animal Ecology © 2024 British Ecological Society.)

AbstractIn dimorphic vertebrates where males are larger than females, the energetic costs of producing and rearing sons can exceed those of daughters. In humans, differences in maternal energy intake suggest that sons require 10% and 7% more energy than daughters during pregnancy and lactation, respectively. Due to a trade-off between reproduction and somatic maintenance, having sons is expected to have a more pronounced detrimental impact on a mother's lifespan than having daughters. A limitation of previous studies investigating this hypothesis is that the increased mortality cost of having sons was assumed to affect all mothers equally. Using a dataset from a preindustrial Quebec population monitored over two centuries, we found that the number of sons decreased postmenopausal lifespan only in mothers experiencing high infant mortality. Our study highlights the importance of interindividual variation in environmental conditions and maternal health when studying effects of offspring sex on reproductive costs.

Laboratory studies with rodents indicate that in utero proximity of a female to male foetus can affect female's subsequent reproduction due to elevated testosterone exposure during early development. It remains unknown whether these findings can be generalised to non-laboratory species because the need for caesarean section makes it difficult to determine the intrauterine position outside laboratory conditions. As an alternative, some studies have compared the reproductive performance of individuals born in male-biased litters to those born in female-biased litters. We identified 44 of those studies in 28 viviparous species for a total of 176 relationships between litter sex composition around the time of birth and subsequent reproductive performance (fertility, fecundity, age at first reproduction, interbirth intervals or post-natal survival of offspring). Those relationships are discordant and complex both within and across species. Some factors can mask an actual association between litter sex composition and reproductive performance. Conversely, a part of significant relationships between litter sex composition and reproductive performance likely arises via pathways other than androgen- and oestrogen-transfer between foetuses of different sexes.

Trade-offs between life history traits are expected to occur due to the limited amount of resources that organisms can obtain and share among biological functions, but are of least concern for selection responses in nutrient-rich or benign environments. In domestic animals, selection limits have not yet been reached despite strong selection for higher meat, milk or egg yields. Yet, negative genetic correlations between productivity traits and health or fertility traits have often been reported, supporting the view that trade-offs do occur in the context of nonlimiting resources. The importance of allocation mechanisms in limiting genetic changes can thus be questioned when animals are mostly constrained by their time to acquire and process energy rather than by feed availability. Selection for high productivity traits early in life should promote a fast metabolism with less energy allocated to self-maintenance (contributing to soma preservation and repair). Consequently, the capacity to breed shortly after an intensive period of production or to remain healthy should be compromised. We assessed those predictions in mammalian and avian livestock and related laboratory model species. First, we surveyed studies that compared energy allocation to maintenance between breeds or lines of contrasting productivity but found little support for the occurrence of an energy allocation trade-off. Second, selection experiments for lower feed intake per unit of product (i.e. higher feed efficiency) generally resulted in reduced allocation to maintenance, but this did not entail fitness costs in terms of survival or future reproduction. These findings indicate that the consequences of a particular selection in domestic animals are much more difficult to predict than one could anticipate from the energy allocation framework alone. Future developments to predict the contribution of time constraints and trade-offs to selection limits will be insightful to breed livestock in increasingly challenging environments., Competing Interests: The authors declare no conflict of interest., (© 2021 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.)

Several studies have shown higher costs of rearing sons than daughters in mammals where males are larger than females. These studies typically focus on females by examining how the offspring sex ratio during a single reproductive event affected mothers' subsequent reproduction or survival probability. Here, we examine relationships between offspring sex ratio during single or multiple reproductive events and several survival metrics in mothers and fathers, using data from zoo-housed tigers (Panthera tigris) and ruffed lemurs (Varecia sp.). Our analyses failed to reveal an overall cost of reproduction or a higher cost of sons to mothers. In male ruffed lemurs, the proportion of sons produced during early life (before 10 years old) was negatively correlated with lifespan later in life. In tigers, males with a higher proportion of sons during their lifetime had shorter lifespans. One likely mechanism is the difference in testosterone levels between males: a high concentration of testosterone can increase the proportion of sons and compromise immune function. Our results suggest studies in wild populations should address the outstanding challenge of understanding consequences of sex allocation for males, and open an opportunity to predict lifespan in an applied conservation context., (© 2021 European Society for Evolutionary Biology.)

Sex allocation research has primarily focused on offspring sex-ratio adjustment by mothers. Yet, fathers also benefit from producing more of the sex with greater fitness returns. Here, we review the state-of-the art in the study of male-driven sex allocation and, counter to the current paradigm, we propose that males can adaptively influence offspring sex ratio through a wide variety of mechanisms. This includes differential production and motility of X- versus Y-bearing sperms in mammals, variation in seminal fluid composition in haplo-diploid invertebrates, and epigenetic mechanisms in some fish and lizards exhibiting environmental sex determination. Conflicts of interest between mothers and fathers over offspring sex ratios can emerge, although many more studies are needed in this area. While many studies of sex allocation have focused on adaptive explanations with little attention to mechanisms, and vice versa, the integration of these two topics is essential for understanding male-driven sex allocation., (© 2021 Wiley Periodicals LLC.)

Fisher's principle states that natural selection favours an equal number of male and female births at the population level, unless there are sex differences in rearing costs or sex differences in mortality before the end of the period of parental investment. Sex differences in rearing costs should be more pronounced in low- than in high-resource settings. We, therefore, examined whether human development index and sex differences in child mortality contribute to the natural variation in human sex ratio at birth across the globe. As predicted by Fisher's principle, the proportion of male births increased with both increasing male-biased childhood mortality and level of development of each country. However, these relationships were absent after accounting for spatial autocorrelation in the residuals, which our inference is conditioned on. This work shows how the failure to account for residual spatial autocorrelation can lead to incorrect conclusions regarding support for predictions from sex allocation theory.

Aging, or senescence, is a progressive deterioration of physiological function with age. It leads to age-related declines in reproduction (reproductive senescence) and survival (actuarial senescence) in most organisms. However, senescence patterns can be highly variable across species, populations, and individuals, and the reasons for such variations remain poorly understood. Evolutionary theories predict that increases in reproductive effort in early life should be associated with accelerated senescence, but empirical tests have yielded mixed results. Although in sexually size-dimorphic species offspring of the larger sex (typically males) commonly require more parental resources, these sex differences are not currently incorporated into evolutionary theories of aging. Here, we show that female reproductive senescence varies with both the number and sex ratio of offspring weaned during early life, using data from a long-term study of bighorn sheep. For a given number of offspring, females that weaned more sons than daughters when aged between 2 and 7 y experienced faster senescence in offspring survival in old age. By contrast, analyses of actuarial senescence showed no cost of early-life reproduction. Our results unite two important topics in evolutionary biology: life history and sex allocation. Offspring sex ratio may help explain among-individual variation in senescence rates in other species, including humans., Competing Interests: The authors declare no competing interest.

While all models of sexual selection assume that the development and expression of enlarged secondary sexual traits are costly, males with larger ornaments or weapons generally show greater survival or longevity. These studies have mostly been performed in species with high sexual size dimorphism, subject to intense sexual selection. Here, we examined the relationships between horn growth and several survival metrics in the weakly dimorphic Pyrenean chamois ( Rupicapra pyrenaica ). In this unhunted population living at high density, males and females were able to grow long horns without any apparent costs in terms of longevity. However, we found a negative relationship between horn growth and survival during prime age in males. This association reduces the potential evolutionary consequences of trophy hunting in male chamois. We also found that females with long horns tended to have lower survival at old ages. Our results illustrate the contrasting conclusions that may be drawn when different survival metrics are used in analyses. The ability to detect trade-off between the expression of male secondary sexual traits and survival may depend more on environmental conditions experienced by the population than on the strength of sexual selection., Competing Interests: None declared., (© 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

The impact of early stress on juvenile development has intrigued scientists for decades, but the adaptive significance of such effects remains an ongoing debate. This debate has largely ignored some characteristics of the offspring, such as their sex, despite strong evolutionary and demographic implications of sex-ratio variation. We review recent studies that examine associations between glucocorticoids (GCs), the main class of stress hormones, and offspring sex. Whereas exposure to GCs at around the time of sex determination in fish consistently produces males, the extent and direction of sex-ratio bias in response to stress vary in reptiles, birds, and mammals. We propose proximate and ultimate explanations for most of these trends., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

Environmental conditions during early development, from conception to sexual maturity, can have lasting consequences on fitness components. Although adult life span often accounts for much of the variation in fitness in long-lived animals, we know little about how early environment affects adult life span in the wild, and even less about whether these effects differ between the sexes. Using data collected over 45 years from wild bighorn sheep (Ovis canadensis), we investigated the effects of early environment on adult mortality in both sexes, distinguishing between natural and anthropogenic sources of mortality. We used the average body mass of yearlings (at about 15 months of age) as a yearly index of environmental quality. We first examined sex differences in natural mortality responses to early environment by censoring harvested males in the year they were shot. We then investigated sex differences in the effects of early environment on overall mortality (natural and hunting mortality combined). Finally, we used path analysis to separate the direct influence of early environment from indirect influences, mediated by age at first reproduction, adult mass and horn length. As early environmental conditions improved, natural adult mortality decreased in both sexes, although for males the effect was not statistically supported. Sex differences in the effects of early environment on adult mortality were detected only when natural and hunting mortality were pooled. Males that experienced favourable early environment had longer horns as adults and died earlier because of trophy hunting, which does not mimic natural mortality. Females that experienced favourable early environment started to reproduce earlier and early primiparity was associated with reduced mortality, suggesting a silver-spoon effect. Our results show that early conditions affect males and females differently because of trophy hunting. These findings highlight the importance of considering natural and anthropogenic environmental factors across different life stages to understand sex differences in mortality., (© 2019 The Authors. Journal of Animal Ecology © 2019 British Ecological Society.)

In species with sexual size dimorphism, the offspring of the larger sex usually have greater energy requirements and may lead to greater fitness costs for parents. The effects of offspring sex on maternal longevity, however, have only been tested in humans. Human studies produced mixed results and considerable debate mainly owing to the difficulty of distinguishing the effects of sexual dimorphism from sociocultural factors. To advance this debate, we examined how the relative number of sons influenced maternal longevity in four species of free-living ungulates (Soay sheep Ovis aries; bighorn sheep, Ovis canadensis; red deer, Cervus elaphus; mountain goat, Oreamnos americanus), with high male-biased sexual size dimorphism but without complicating sociocultural variables. We found no evidence for a higher cumulative cost of sons than of daughters on maternal longevity. For a given number of offspring, most females with many sons in all four populations lived longer than females with few sons. The higher cost of sons over daughters on maternal lifespan reported by some human studies may be the exception rather than the rule in long-lived iteroparous species.

We know little about the determinants and demographic consequences of the marked seasonal mass changes exhibited by many northern and alpine mammals. We analysed 43 years of data on individual winter mass loss (the difference between mass in early June and mass in mid-September the previous year) and summer mass gain (the difference between mass in mid-September and in early June of the same year) in adult bighorn sheep (Ovis canadensis). We calculated relative seasonal mass change as a proportion of individual body mass at the start of each season. We first examined the effects of weather and population density on relative changes in body mass. We then assessed the consequences of relative seasonal mass changes on reproduction. Mean April-May temperature was the main driver of relative seasonal mass changes: warm springs reduced both relative winter mass loss and summer mass gain of both sexes, likely partially due to a trade-off between growth rate of plants and duration of access to high-quality forage. Because these effects cancelled each other, spring temperature did not influence mass in mid-September. Mothers that lost relatively more mass during the winter had lambs that gained less mass during summer, likely because these females allocated fewer resources to lactation. Winter survival of lambs increased with their summer mass gain. In males, relative mass loss during winter, which includes the rut, did not influence the probability of siring at least one lamb, possibly indicating that greater mating effort did not necessarily translate into greater reproductive success. Our findings improve our understanding of how weather influences recruitment and underline the importance of cryptic mechanisms behind the effects of climate change on demographic traits., (© 2018 by the Ecological Society of America.)

Can mammalian mothers adaptively control the sex of their offspring? The influential Trivers-Willard hypothesis (TWH) proposes that when maternal condition increases the fitness of sons more than that of daughters, the proportion of sons produced should increase with maternal condition. Studies of mammals, however, often fail to support this hypothesis. This article highlights recent advances, including studies on the assumptions of the TWH and physiological mechanisms for sex-ratio manipulation. Particular emphasis is placed on how factors such as paternal quality, maternal reproductive costs and environmental conditions experienced by mothers early in life can mask/alter the expected relationship between maternal condition and offspring sex ratio or lead to apparent support for the TWH. While there is growing evidence that sex ratio around conception may be maternally and paternally manipulated, a challenge for future studies on sex allocation is to integrate how multiple and potentially opposite selective pressures affect offspring sex ratio., (© 2017 WILEY Periodicals, Inc.)

The internal predictive adaptive response (internal PAR) hypothesis predicts that individuals born in poor conditions should start to reproduce earlier if they are likely to have reduced performance in later life. However, whether this is the case remains unexplored in wild populations. Here, we use longitudinal data from a long-term study of Svalbard reindeer to examine age-related changes in adult female life-history responses to environmental conditions experienced in utero as indexed by rain-on-snow (ROS utero ). We show that females experiencing high ROS utero had reduced reproductive success only from 7 years of age, independent of early reproduction. These individuals were able to maintain the same annual reproductive success between 2 and 6 years as phenotypically superior conspecifics that experienced low ROS utero Young females born after high ROS utero engage in reproductive events at lower body mass (about 2.5 kg less) than those born after low ROS utero The mean fitness of females that experienced poor environmental conditions in early life was comparable with that of females exposed to good environmental conditions in early life. These results are consistent with the idea of internal PAR and suggest that the life-history responses to early-life conditions can buffer the delayed effects of weather on population dynamics., (© 2016 The Author(s).)

Trivers and Willard proposed that offspring sex ratio should vary with maternal condition when condition, meant as maternal capacity to care, has different fitness consequences for sons and daughters. In polygynous and dimorphic species, mothers in good condition should preferentially produce sons, whereas mothers in poor condition should produce more daughters. Despite its logical appeal, support for this hypothesis has been inconsistent. Sex-ratio variation may be influenced by additional factors, such as environmental conditions and previous reproduction, which are often ignored in empirical studies. We analysed 39 years of data on bighorn sheep (Ovis canadensis) that fit all the assumptions of the Trivers-Willard hypothesis. Production of sons increased with maternal condition only for mothers that weaned a son the previous year. This relationship likely reflects a mother's ability to bear the higher reproductive costs of sons. The interaction between maternal condition and previous weaning success on the probability of producing a son was independent of the positive effect of paternal reproductive success. Maternal and paternal effects accounted for similar proportions of the variance in offspring sex. Maternal reproductive history should be considered in addition to current condition in studies of sex allocation., (© 2016 The Author(s).)

Parents should bias sex allocation toward offspring of the sex most likely to provide higher fitness returns. Trivers and Willard proposed that for polygynous mammals, females should adjust sex-ratio at conception or bias allocation of resources toward the most profitable sex, according to their own body condition. However, the possibility that mammalian fathers may influence sex allocation has seldom been considered. Here, we show that the probability of having a son increased from 0.31 to 0.60 with sire reproductive success in wild bighorn sheep (Ovis canadensis). Furthermore, our results suggest that females fertilized by relatively unsuccessful sires allocated more energy during lactation to daughters than to sons, while the opposite occurred for females fertilized by successful sires. The pattern of sex-biased offspring production appears adaptive because paternal reproductive success reduced the fitness of daughters and increased the average annual weaning success of sons, independently of maternal allocation to the offspring. Our results illustrate that sex allocation can be driven by paternal phenotype, with profound influences on the strength of sexual selection and on conflicts of interest between parents., (© 2016 The Author(s). Evolution © 2016 The Society for the Study of Evolution.)

Selective harvest may lead to rapid evolutionary change. For large herbivores, trophy hunting removes males with large horns. That artificial selection, operating in opposition to sexual selection, can lead to undesirable consequences for management and conservation. There have been no comparisons of long-term changes in trophy size under contrasting harvest pressures. We analyzed horn measurements of Stone's rams (Ovis dalli stonei) harvested over 37 years in two large regions of British Columbia, Canada, with marked differences in hunting pressure to identify when selective hunting may cause a long-term decrease in horn growth. Under strong selective harvest, horn growth early in life and the number of males harvested declined by 12% and 45%, respectively, over the study period. Horn shape also changed over time: horn length became shorter for a given base circumference, likely because horn base is not a direct target of hunter selection. In contrast, under relatively lower hunting pressure, there were no detectable temporal trends in early horn growth, number of males harvested, or horn length relative to base circumference. Trophy hunting is an important recreational activity and can generate substantial revenues for conservation. By providing a reproductive advantage to males with smaller horns and reducing the availability of desirable trophies, however, excessive harvest may have the undesirable long-term consequences of reducing both the harvest and the horn size of rams. These consequences can be avoided by limiting offtake.

Empirical evidence for declines in fitness components (survival and reproductive performance) with age has recently accumulated in wild populations, highlighting that the process of senescence is nearly ubiquitous in the living world. Senescence patterns are highly variable among species and current evolutionary theories of ageing propose that such variation can be accounted for by differences in allocation to growth and reproduction during early life. Here, we compiled 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life. Our review brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life. We discuss our results in the light of two closely related theories of ageing-the disposable soma and the antagonistic pleiotropy theories-and propose that the principle of energy allocation roots the ageing process in the evolution of life-history strategies. Finally, we outline research topics that should be investigated in future studies, including the importance of natal environmental conditions in the study of trade-offs between early- and late-life performance and the evolution of sex-differences in ageing patterns., (© 2015 The Author(s) Published by the Royal Society. All rights reserved.)

Male mammals typically have shorter lifespans than females [1]. Sex differences in survival may result, in part, from sex-specific optima in investment in reproduction, with higher male mortality rates from sexual competition selecting for a "live-fast die-young" strategy in this sex [2]. In the wild, lifespan is also influenced by environmental conditions experienced early in life. Poor conditions elevate juvenile mortality, which may selectively remove individuals with a particular phenotype or genotype from a cohort [3], and can alter the subsequent phenotypic condition and fate of those that survive to adulthood [4]. Males and females can respond differently to the same early-life environmental experiences [5, 6], but whether such environmental pressures generate sex differences in lifespan has rarely been considered. We show that sex differences in adult survival and lifespan in cohorts of roe deer (Capreolus capreolus) range from virtually absent in some years to females living 30% longer than males in others. The extent of this sex difference in adult longevity is strongly linked to the level of mortality each cohort experiences as juveniles, with high juvenile mortality generating a strong sex difference in both adult survival and lifespan. In females, high juvenile mortality leads to increased adult survival for those remaining individuals, whereas in males survival is actually reduced. Early environmental conditions and the selective pressures they impose may help to explain variability in sex-specific aging across animal taxa., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

The predictive adaptive response (PAR) hypothesis proposes that animals adjust their physiology and developmental trajectory during early life in anticipation of their future environments. Accordingly, when environmental conditions in early life match environmental conditions during adulthood, individual fitness should be greater. Here, we test this hypothesis in a long-lived mammal, the roe deer, using data from two contrasting populations, intensively monitored for more than 35 years. In the highly productive site, the fitness of female roe deer increased with the quality of environment during adulthood and, contrary to predictions of PAR, individuals born in good conditions always outperformed those born under poor conditions. In the resource-limited site, the fitness of female roe deer born in poor years was better than those born in good conditions in poor years when the animals were adult, but not in good years. Although consistent with predictions of PAR, we showed that this pattern is likely to be a consequence of increased viability selection during the juvenile stage for animals born in poor years. While PARs are often advanced in evolutionary medicine, our findings suggest that detailed biological processes should be investigated before drawing conclusions about the existence of this phenomenon.

There is increasing evidence that environmental conditions experienced early in life can markedly affect an organism's life history, but the pathways by which early environment influences adult phenotype are poorly known. We used long-term data from two roe deer (Capreolus capreolus) populations (Chizé and Trois-Fontaines, France) to investigate the direct and indirect (operating through fawn body mass) effects of environmental conditions during early life on adult body mass. We found that environmental conditions (population size and spring temperatures) around birth influenced body mass of adult females through both direct and indirect effects in both populations. The occurrence of direct effects means that, for a given fawn body mass, adult female mass decreases with adverse conditions in early life. In contrast, we found no evidence for direct effects of early-life conditions on adult body mass of males, suggesting the existence of sex-specific long-term responses of body mass to stressful early conditions. Our results provide evidence that early environmental conditions influence the adult phenotype through persistent effects over the body development in wild mammal populations.

To maximize long-term average reproductive success, individuals can diversify the phenotypes of offspring produced within a reproductive event by displaying the 'coin-flipping' tactic. Wild boar (Sus scrofa scrofa) females have been reported to adopt this tactic. However, whether the magnitude of developmental plasticity within a litter depends on stochasticity in food resources has not been yet investigated. From long-term monitoring, we found that juvenile females produced similar-sized fetuses within a litter independent of food availability. By contrast, adult females adjusted their relative allocation to littermates to the amount of food resources, by providing a similar allocation to all littermates in years of poor food resources but producing highly diversified offspring phenotypes within a litter in years of abundant food resources. By minimizing sibling rivalry, such a plastic reproductive tactic allows adult wild boar females to maximize the number of littermates for a given breeding event.

How populations respond to climate change depends on the interplay between life history, resource availability, and the intensity of the change. Roe deer are income breeders, with high levels of allocation to reproduction, and are hence strongly constrained by the availability of high quality resources during spring. We investigated how recent climate change has influenced demographic processes in two populations of this widespread species. Spring began increasingly earlier over the study, allowing us to identify 2 periods with contrasting onset of spring. Both populations grew more slowly when spring was early. As expected for a long-lived and iteroparous species, adult survival had the greatest potential impact on population growth. Using perturbation analyses, we measured the relative contribution of the demographic parameters to observed variation in population growth, both within and between periods and populations. Within periods, the identity of the critical parameter depended on the variance in growth rate, but variation in recruitment was the main driver of observed demographic change between periods of contrasting spring earliness. Our results indicate that roe deer in forest habitats cannot currently cope with increasingly early springs. We hypothesise that they should shift their distribution to richer, more heterogeneous landscapes to offset energetic requirements during the critical rearing stage., (© 2013 John Wiley & Sons Ltd/CNRS.)