Sex differences in adult lifespan and aging rates of mortality across wild mammals.

In human populations, women consistently outlive men, which suggests profound biological foundations for sex differences in survival. Quantifying whether such sex differences are also pervasive in wild mammals is a crucial challenge in both evolutionary biology and biogerontology. Here, we compile demographic data from 134 mammal populations, encompassing 101 species, to show that the female's median lifespan is on average 18.6% longer than that of conspecific males, whereas in humans the female advantage is on average 7.8%. On the contrary, we do not find any consistent sex differences in aging rates. In addition, sex differences in median adult lifespan and aging rates are both highly variable across species. Our analyses suggest that the magnitude of sex differences in mammalian mortality patterns is likely shaped by local environmental conditions in interaction with the sex-specific costs of sexual selection.

Sex-specific body mass ageing trajectories in adult Asian elephants.

In species with marked sexual dimorphism, the classic prediction is that the sex which undergoes stronger intrasexual competition ages earlier or quicker. However, more recently, alternative hypotheses have been put forward, showing that this association can be disrupted. Here, we utilize a unique, longitudinal data set of a semi-captive population of Asian elephants (Elephas maximus), a species with marked male-biased intrasexual competition, with males being larger and having shorter lifespans, and investigate whether males show earlier and/or faster body mass ageing than females. We found evidence of sex-specific body mass ageing trajectories: adult males gained weight up to the age of 48 years old, followed by a decrease in body mass until natural death. In contrast, adult females gained body mass with age until a body mass decline in the last year of life. Our study shows sex-specific ageing patterns, with an earlier onset of body mass declines in males than females, which is consistent with the predictions of the classical theory of ageing.

The elephant in the family: Costs and benefits of elder siblings on younger offspring life-history trajectory in a matrilineal mammal.

Many mammals grow up with siblings, and interactions between them can influence offspring phenotype and fitness. Among these interactions, sibling competition between different-age offspring should lead to reproductive and survival costs on the younger sibling, while sibling cooperation should improve younger sibling's reproductive potential and survival. However, little is known about the consequences of sibling effects on younger offspring life-history trajectory, especially in long-lived mammals. We take advantage of a large, multigenerational demographic dataset from semi-captive Asian elephants to investigate how the presence and sex of elder siblings influence the sex, survival until 5 years old, body condition, reproductive success (i.e. age at first reproduction and lifetime reproductive success) and long-term survival of subsequent offspring. We find that elder siblings have heterogeneous effects on subsequent offspring life-history traits depending on their presence, their sex and the sex of the subsequent offspring (named focal calf). Overall, the presence of an elder sibling (either sex) strongly increased focal calf long-term survival (either sex) compared to sibling absence. However, elder sisters had higher impact on the focal sibling than elder brothers. Focal females born after a female display higher long-term survival, and decreased age at first reproduction when raised together with an elder sister rather than a brother. Focal males born after a female rather than a male showed lower survival but higher body weight when both were raised together. We did not detect any sibling effects on the sex of the focal calf sex, survival until 5 years old and lifetime reproductive success. Our results highlight the general complexity of sibling effects, but broadly that elder siblings can influence the life-history trajectory of subsequent offspring. We also stress the importance of considering all life stages when evaluating sibling effects on life trajectories.

Denombreux mammifères grandissent en fratrie, et les interactions au sein de lafratrie peuvent influencer le phénotype et la valeur sélective des jeunes.Parmi ces interactions, la compétition entre frères et sœurs d'âges différentspeut entraîner des coûts de reproduction et de survie pour le/la plus jeune,tandis que les interactions coopératives améliorent la reproduction et lasurvie du/de la plus jeune. Cependant, nous avons encore peu de connaissancessur l'influence de la fratrie sur la trajectoire de vie des frères et sœursplus jeunes, en particulier chez les mammifères longévifs. Grâce àun jeu de données démographique multigénérationnel d'éléphants d'Asiesemi-captifs, nous avons pu étudier comment la présence d'un frère aînéou d'une sœur aînée influence le sexe, la survie jusqu'à l'âge de cinqans, la masse corporelle, la reproduction (i.e. l'âge de première reproductionet le succès reproductif sur toute la vie) et la survie à long terme du jeunesuivant. Nousobservons que les frères et sœurs aînés ont des effets hétérogènes sur lestraits d'histoire de vie du jeune suivant et ce, en fonction de leur présence,et du sexe du jeune suivant (appelé focal). Dansl'ensemble, la présence d'un frère aîné oud'une sœur aînée augmente fortement la survie à long terme du jeune focal parrapport à leur absence. Cependant, il est à noter que les sœurs aînées ont unimpact plus important que les frères ainés sur le frère focal. Les femellesfocales présentent une survie à long terme plus élevée et un âge de premièrereproduction plus précoce lorsqu'elles sont élevées avec une sœur aînée plutôtqu'un frère. Les mâles focaux élevés avec une grande sœur plutôt qu'un grandfrère présentent une survie plus faible mais un poids corporel plus élevé. Nousn'avons détecté aucun effet des frères aînés ou sœurs aînées sur le sexe, la survie jusqu'àl'âge de cinq ans et le succès reproducteur sur toute la vie du jeune focal. Nosrésultats mettent en évidence la complexité des effets de la fratrie et, lefait que les frères et sœurs plus âgés peuvent influencer la trajectoire ducycle de vie des jeunes suivant. Nous soulignons également l'importance deconsidérer toutes les étapes de la vie lors de l'évaluation des effets de lafratrie sur les trajectoires de vie.

Maternal age at birth shapes offspring life-history trajectory across generations in long-lived Asian elephants.

Advanced maternal age at birth can have pronounced consequences for offspring health, survival and reproduction. If carried over to the next generation, such fitness effects could have important implications for population dynamics and the evolution of ageing, but these remain poorly understood. While many laboratory studies have investigated maternal age effects, relatively few studies have been conducted in natural populations, and they usually only present a "snapshot" of an offspring's lifetime. In the present study, we focus on how maternal age influences offspring life-history trajectories and performance in a long-lived mammal. We use a multigenerational demographic dataset of semi-captive Asian elephants to investigate maternal age effects on several offspring life-history traits: condition, reproductive success and overall survival. We show that offspring born to older mothers display reduced overall survival but higher reproductive success, and reduced survival of their own progeny. Our results show evidence of a persistent effect of maternal age on fitness across generations in a long-lived mammal. By highlighting transgenerational effects on the fitness of the next generation associated with maternal age, the present study helps increase our understanding of factors contributing to individual variation in ageing rates and fitness.

Early and Adult Social Environments Shape Sex-Specific Actuarial Senescence Patterns in a Cooperative Breeder.

Sociality modulates life-history traits through changes in resource allocation to fitness-related traits. However, how social factors at different stages of the life cycle modulate senescence remains poorly understood. To address this question, we assessed the influence of social environment in both early life and adulthood on actuarial senescence in the Alpine marmot, a cooperative breeder. The influence of helpers on actuarial senescence strongly differed depending on when help was provided and on the sex of the dominant. Being helped when adult slowed down senescence in both sexes. However, the effect of the presence of helpers during the year of birth of a dominant was sex specific. Among dominants helped during adulthood, females born in the presence of helpers senesced slower, whereas males senesced faster. Among dominants without helpers during adulthood, females with helpers at birth senesced faster. Social environment modulates senescence but acts differently between sexes and life stages.

What have humans done for evolutionary biology? Contributions from genes to populations.

Many fundamental concepts in evolutionary biology were discovered using non-human study systems. Humans are poorly suited to key study designs used to advance this field, and are subject to cultural, technological, and medical influences often considered to restrict the pertinence of human studies to other species and general contexts. Whether studies using current and recent human populations provide insights that have broader biological relevance in evolutionary biology is, therefore, frequently questioned. We first surveyed researchers in evolutionary biology and related fields on their opinions regarding whether studies on contemporary humans can advance evolutionary biology. Almost all 442 participants agreed that humans still evolve, but fewer agreed that this occurs through natural selection. Most agreed that human studies made valuable contributions to evolutionary biology, although those less exposed to human studies expressed more negative views. With a series of examples, we discuss strengths and limitations of evolutionary studies on contemporary humans. These show that human studies provide fundamental insights into evolutionary processes, improve understanding of the biology of many other species, and will make valuable contributions to evolutionary biology in the future.

Early and adult social environments have independent effects on individual fitness in a social vertebrate.

Evidence that the social environment at critical stages of life-history shapes individual trajectories is accumulating. Previous studies have identified either current or delayed effects of social environments on fitness components, but no study has yet analysed fitness consequences of social environments at different life stages simultaneously. To fill the gap, we use an extensive dataset collected during a 24-year intensive monitoring of a population of Alpine marmots (Marmota marmota), a long-lived social rodent. We test whether the number of helpers in early life and over the dominance tenure length has an impact on litter size at weaning, juvenile survival, longevity and lifetime reproductive success (LRS) of dominant females. Dominant females, who were born into a group containing many helpers and experiencing a high number of accumulated helpers over dominance tenure length showed an increased LRS through an increased longevity. We provide evidence that in a wild vertebrate, both early and adult social environments influence individual fitness, acting additionally and independently. These findings demonstrate that helpers have both short- and long-term effects on dominant female Alpine marmots and that the social environment at the time of birth can play a key role in shaping individual fitness in social vertebrates.

Early-late life trade-offs and the evolution of ageing in the wild.

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.

How do animals optimize the size-number trade-off when aging? Insights from reproductive senescence patterns in marmots.

We investigated the influence of female age on five reproductive traits and on the offspring size-number trade-off from an extensive data set spanning 20 years of study on free-ranging Alpine marmots. Offspring mass increased with female age, whereas litter size and reproductive allocation remained constant in females up to 10 years of age and declined thereafter. Although reproductive allocation declined, post-weaning juvenile survival and the size-number trade-off did not change markedly throughout a female's lifetime. Senescence of annual reproductive success (i.e., the number of offspring surviving their first hibernation within a given litter) only resulted from senescence of litter size. The data were insufficient to determine whether the decrease in litter size with age was caused by declining litter size at birth, offspring pre-weaning survival, or both. Regardless, our findings demonstrate that marmot females display a size-number trade-off invariant with age, and that their reproductive tactic involves increasing offspring size at the cost of decreasing litter size with increasing age. As a result, reproductive performance remains constant throughout a female's lifetime, despite the deleterious effects of senescence in litter size.

Seasonal variation in molecular and physiological stress markers in Asian elephants.

Free-living species exhibit seasonal variation in various life history traits, including vital rates such as birth and death patterns. Different physiological mechanisms are thought to underlie the expression of life history traits that contribute to lifetime fitness. However, although the broad impacts of seasonality on life history traits and trade-offs is well established in many systems, the exact physiological mechanisms responsible for driving differences within and between individuals are poorly understood. Among them, molecular and physiological stress pathways, such as stress hypothalamic-pituitary-adrenal axis and oxidative stress, have potential to mediate relationships between individual survival, reproduction and environmental seasonality. Here, we determine how different physiological markers of stress including faecal cortisol metabolites (FCMs), heterophils/lymphocytes (H/L) ratio, two markers indicating oxidative balance including a marker of oxidative damage (reactive oxygen metabolites, ROM) and a marker of antioxidant defences (superoxide dismutase, SOD) and body weight vary in a large semi-captive population of Asian elephants (Elephas maximus) exposed to extreme seasonality (e.g. elevated temperatures). Individuals showed higher FCM levels and H/L ratios during cold season, indicating increased stress, and the lowest FCM levels during monsoon season and H/L ratios during hot and dry season, but we found no pattern in oxidative stress (ROM and SOD) levels. Hot season also associated with a decline in body weight. The present study shows how different physiological parameters (FCM levels and H/L ratio), molecular (oxidative stress) and body condition vary with seasonal changes, and how these parameters might allow individuals to adapt to such variations. Our results on an endangered long-lived species are crucial in indicating the most productive timing for conservation efforts, predicting how individuals cope with environmental changes, and allow for a more accurate representation of how animal physiology operates in nature.

Age related variation of health markers in Asian elephants.

Although senescence is often observed in the wild, its underlying mechanistic causes can rarely be studied alongside its consequences, because data on health, molecular and physiological measures of senescence are rare. Documenting how different age-related changes in health accelerate ageing at a mechanistic level is key if we are to better understand the ageing process. Nevertheless, very few studies, particularly on natural populations of long-lived animals, have investigated age-related variation in biological markers of health and sex differences therein. Using blood samples collected from semi-captive Asian elephants, we show that pronounced differences in haematology, blood chemistry, immune, and liver functions among age classes are also evident under natural conditions in this extremely long-lived mammal. We provide strong support that overall health declined with age, with progressive declines in immune and liver functions similarly in both males and females. These changes parallel those mainly observed to-date in humans and laboratory mammals, and suggest a certain ubiquity in the ageing patterns.

Seasonal variation of health in Asian elephants.

Long-lived species are often predicted to be buffered against seasonal variation: longevity means low annual mortality and reproductive rates and annual variability in climate may therefore have a smaller impact on population growth rates of long-lived species in comparison to short-lived ones. However, little is known of the physiological mechanisms underlying such patterns in long-lived species. In this study, we investigated seasonal variation in the health of Asian elephants living in a seasonal monsoon climate. We used two complementary methods: (i) global and (ii) trait-by-trait analyses of seasonal effects on 23 health parameters of 225 individually marked elephants with known age and reproductive and health history, with repeated measures per individual over a 26-month period. The global analysis highlighted the biggest differences in health between the hot and monsoon seasons. Our trait-specific analyses identified the physiological functions underlying such health variation in different ecological settings, including haematological, immunological, muscular, kidney and liver functions, as well as protein balance and electrolytes. Overall, the results suggest that even long-lived, large mammals may experience physiological changes in response to seasonal variation that in extreme circumstances can pose a significant health risk.

Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals.

While it is commonly believed that animals live longer in zoos than in the wild, this assumption has rarely been tested. We compared four survival metrics (longevity, baseline mortality, onset of senescence and rate of senescence) between both sexes of free-ranging and zoo populations of more than 50 mammal species. We found that mammals from zoo populations generally lived longer than their wild counterparts (84% of species). The effect was most notable in species with a faster pace of life (i.e. a short life span, high reproductive rate and high mortality in the wild) because zoos evidently offer protection against a number of relevant conditions like predation, intraspecific competition and diseases. Species with a slower pace of life (i.e. a long life span, low reproduction rate and low mortality in the wild) benefit less from captivity in terms of longevity; in such species, there is probably less potential for a reduction in mortality. These findings provide a first general explanation about the different magnitude of zoo environment benefits among mammalian species, and thereby highlight the effort that is needed to improve captive conditions for slow-living species that are particularly susceptible to extinction in the wild.

Does tooth wear influence ageing? A comparative study across large herbivores.

We test whether the intensity of tooth wear influences the strength of actuarial senescence across species of large herbivores. We collected from the literature data on tooth wear in the wild (measured as the slope of the regression of log-transformed M1 crown height on age), longevity (measured as the age at which 90% of individuals are dead) and two metrics of actuarial senescence in captive populations (rate of senescence between 6 and 12 years of age and Gompertz rate of senescence). Between-species differences and variation in tooth height accounted for most of the observed variation in tooth wear among large herbivores: tooth height and tooth wear were positively correlated. In contrast, tooth wear was little influenced by sex, body mass, or taxonomy. No marked between-sex differences in longevity occurred. Males senesced faster than females when tooth wear was low (for both senescence metrics), while between-sex differences in actuarial senescence when tooth wear was high depended on the metric used to measure actuarial senescence. While longevity was mostly independent of the intensity of tooth wear, we found general support for a positive relationship between both measures of actuarial senescence and tooth wear. These patterns were consistent whether hypsodonty was controlled for or not. Although varying according to sex and to the metric used for assessing actuarial senescence, our findings suggest overall that tooth wear could be positively associated with actuarial senescence among large herbivores. Further longitudinal studies focusing on changes within individuals will be required to test whether a mechanistic link between tooth wear and actuarial senescence occurs in large herbivores.