Survival improvements of marine mammals in zoological institutions mirror historical advances in human longevity.

An intense public debate has fuelled governmental bans on marine mammals held in zoological institutions. The debate rests on the assumption that survival in zoological institutions has been and remains lower than in the wild, albeit the scientific evidence in support of this notion is equivocal. Here, we used statistical methods previously applied to assess historical improvements in human lifespan and data on 8864 individuals of four marine mammal species (harbour seal, Phoca vitulina; California sea lion, Zalophus californianus; polar bear, Ursus maritimus; common bottlenose dolphin, Tursiops truncatus) held in zoos from 1829 to 2020. We found that life expectancy increased up to 3.40 times, and first-year mortality declined up to 31%, during the last century in zoos. Moreover, the life expectancy of animals in zoos is currently 1.65-3.55 times longer than their wild counterparts. Like humans, these improvements have occurred concurrently with advances in management practices, crucial for population welfare. Science-based decisions will help effective legislative changes and ensure better implementation of animal care.

Species delineation and genetic structure of two Chaerephon species (C. pusillus and C. leucogaster) on Madagascar and the Comoro archipelago.

Cryptic species diversity is known to be common in bats but remains challenging to study in these mammals, whose natural history traits render their sampling and monitoring challenging. For these animals, indirect genetic approaches provide a powerful tool to gain insight into the evolutionary history and ecology of cryptic bat species. The speciation history of the polyphyletic Chaerephon pumilus species group (Molossidae) is poorly understood, including those found on western Indian Ocean islands. Two species in this complex have been identified in the Comoros: C. pusillus and C. leucogaster. Here, we aim to genetically characterize these two species and investigate their spatial population genetic structure. Analyzing five nuclear microsatellite markers from 200 individuals and one mitochondrial DNA gene (Cyt-b) from 161 (out of the 200) individuals sampled on Madagascar and the Comoros, our findings indicated that these species are genetically differentiated. We observed mitonuclear discordance in numerous individuals (33% of the 161 mtDNA-sequenced individuals). Based on ABC analyses, we found that this pattern could potentially be the result of asymmetric introgressive hybridization from C. leucogaster to C. pusillus and calls for further studies on the demographic history of these species. Moreover, at the intra-specific level, analyses of the microsatellite loci suggested the evidence of a more pronounced, although weak, geographically based genetic structure in C. pusillus than in C. leucogaster. Altogether, our findings provide preliminary insights into the eco-evolutionary aspects of this species complex and warrant further research to understand hybridization dynamics and mechanisms responsible for mitonuclear discordance.

Sex-specific actuarial and reproductive senescence in zoo-housed tiger (Panthera tigris): The importance of sub-species for conservation.

A fifth of all known species are currently classified as threatened in the wild: the rate of biodiversity loss is rapid, continuous, and mostly due to anthropogenic activities. To slow down this decline, the accurate estimation of demographic parameters for threatened species is critical. With this aim, zoo institutions play an important role, giving access to data on zoo-housed animals, which aids researchers working on species life-history traits and intrinsic factors influencing the fitness of both sexes, such as age. While tigers (Panthera tigris) are particularly threatened in their natural environment, few of their demographic parameters have been determined because of their solitary and elusive nature as well as low population density. Using individual-based information for more than 9200 tigers (from 1938 to 2018) recorded in the International Tiger Studbook 2018, we aimed to determine sub-species and sex-specific variability of survival and reproductive parameters with age. No significant sex-difference in actuarial senescence (i.e., decline of survival probabilities with age) was observed but males tended to have a higher juvenile mortality and a faster senescence than females. Reproductive senescence (i.e., decline of reproductive parameters with age) was more pronounced in females than males. Moreover, we observed sub-species-specific variation in mortality and reproductive patterns, pointing out the necessity to consider them independently for conservation goals. Our findings can provide meaningful improvements to the husbandry of zoo-housed tigers, emphasizing the importance of adult breeding females of 7-9 years-old to control zoo-housed population size, but also providing accurate demographic estimates, crucial to set up effective conservation plans.

Lifespan decreases with proportion of sons in males but not females of zoo-housed tigers and lemurs.

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.

Variation in the ontogenetic allometry of horn length in bovids along a body mass continuum.

Allometric relationships describe the proportional covariation between morphological, physiological, or life-history traits and the size of the organisms. Evolutionary allometries estimated among species are expected to result from species differences in ontogenetic allometry, but it remains uncertain whether ontogenetic allometric parameters and particularly the ontogenetic slope can evolve. In bovids, the nonlinear evolutionary allometry between horn length and body mass in males suggests systematic changes in ontogenetic allometry with increasing species body mass. To test this hypothesis, we estimated ontogenetic allometry between horn length and body mass in males and females of 19 bovid species ranging from ca. 5 to 700 kg. Ontogenetic allometry changed systematically with species body mass from steep ontogenetic allometries over a short period of horn growth in small species to shallow allometry with the growth period of horns matching the period of body mass increase in the largest species. Intermediate species displayed steep allometry over long period of horn growth. Females tended to display shallower ontogenetic allometry with longer horn growth compared to males, but these differences were weak and highly variable. These findings show that ontogenetic allometric slope evolved across species possibly as a response to size-related changes in the selection pressures acting on horn length and body mass.

Pathogens Shape Sex Differences in Mammalian Aging.

Understanding the origin of sex differences in lifespan and aging patterns remains a salient challenge in both biogerontology and evolutionary biology. Different factors have been studied but the potential influence of pathogens has never been investigated. Sex differences, especially in hormones and resource allocation, generate a differential response to pathogens and thereby shape sex differences in lifespan or aging. We provide an integrative framework linking host pathogenic environment with both sex-specific selections on immune performance and mortality trajectories. We propose future directions to fill existing knowledge gaps about mechanisms that link sex differences, not only to exposition and sensitivity to pathogens, but also to mortality patterns, whilst emphasizing the urgent need to consider the role of sex in medicine.

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.

Variation in actuarial senescence does not reflect life span variation across mammals.

The concept of actuarial senescence (defined here as the increase in mortality hazards with age) is often confounded with life span duration, which obscures the relative role of age-dependent and age-independent processes in shaping the variation in life span. We use the opportunity afforded by the Species360 database, a collection of individual life span records in captivity, to analyze age-specific mortality patterns in relation to variation in life span. We report evidence of actuarial senescence across 96 mammal species. We identify the life stage (juvenile, prime-age, or senescent) that contributes the most to the observed variation in life span across species. Actuarial senescence only accounted for 35%-50% of the variance in life span across species, depending on the body mass category. We computed the sensitivity and elasticity of life span to five parameters that represent the three stages of the age-specific mortality curve-namely, the duration of the juvenile stage, the mean juvenile mortality, the prime-age (i.e., minimum) adult mortality, the age at the onset of actuarial senescence, and the rate of actuarial senescence. Next, we computed the between-species variance in these five parameters. Combining the two steps, we computed the relative contribution of each of the five parameters to the variance in life span across species. Variation in life span was increasingly driven by the intensity of actuarial senescence and decreasingly driven by prime-age adult mortality from small to large species because of changes in the elasticity of life span to these parameters, even if all the adult survival parameters consistently exhibited a canalization pattern of weaker variability among long-lived species than among short-lived ones. Our work unambiguously demonstrates that life span cannot be used to measure the strength of actuarial senescence, because a substantial and variable proportion of life span variation across mammals is not related to actuarial senescence metrics.

Maternal reproductive senescence shapes the fitness consequences of the parental age difference in ruffed lemurs.

In humans, pronounced age differences between parents have deleterious fitness consequences. In particular, the number of children is lower when mothers are much older than fathers. However, previous analyses failed to disentangle the influence of differential parental age per se from a direct age effect of each parent. In this study, we analyse the fitness consequences of both parental age and parental age differences on litter size and offspring survival in two closely related species of lemurs living in captivity. As captive lemurs do not choose their reproductive partner, we were able to measure litter size and offspring survival across breeding pairs showing a wide range of parental age differences. However, we demonstrated that the effect of the parental age difference on litter size was fully accounted for by female reproductive senescence because females mating with much younger males were old females. On the other hand, both parental age difference and female reproductive senescence influenced offspring survival. Our results emphasize the importance of teasing apart the effect of parental reproductive senescence when investigating the health and fitness consequences of parental age differences and also provide new insights for conservation programmes of endangered species.

High reproductive effort is associated with decreasing mortality late in life in captive ruffed lemurs.

Evolutionary theories of senescence predict that a high allocation to reproduction during early life should have long-term deleterious consequences on future reproduction or survival because individuals have to face an energy allocation trade-off between reproductive effort and the maintenance of body condition. Using a high-quality dataset from 1,721 red ruffed lemurs (RRL, Varecia rubra) and 3,637 black and white ruffed lemurs (BWRM, V. variegata) living in captivity, we tested the existence of a trade-off between reproductive effort and late-life survival after accounting for possible confounding effects of natal environmental conditions. We report clear evidence of actuarial senescence (i.e., the decline of annual survival with increasing age) in both sexes and for both species of ruffed lemurs. RRL had a lower baseline mortality and senesced faster than BWRL, resulting in similar distributions of longevities for both species. No between-sex difference was observed in any species. Lastly, a higher reproductive effort was positively associated with an increase of survival late in life, and thereby an increased longevity. These findings indicate that individual quality rather than trade-off drives the association between reproductive success and survival pattern among individual lemurs of both species in the protected environment provided by zoos. Lemurs are among the world's highest conservation priorities and better understanding factors influencing their longevity and actuarial senescence patterns should improve their conservation.

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 sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants.

In most mammals, both sexes display different survival patterns, often involving faster senescence in males. Being under intense sexual competition to secure mating opportunities, males of polygynous species allocate resources to costly behaviors and conspicuous sexual traits, which might explain these observed differences in longevity and senescence patterns. However, comparative studies performed to date have led to conflicting results. We aimed to resolve this problem by first reviewing case studies of the relationship between the strength of sexual selection and age-specific survival metrics. Then, we performed a comprehensive comparative analysis to test whether such relationships exist among species of captive ruminants. We found that the strength of sexual selection negatively influenced the onset of actuarial senescence in males, with males senescing earlier in polygynous than in monogamous species, which led to reduced male longevity in polygynous species. Moreover, males of territorial species senesced earlier but slower, and have a shorter longevity than males of species displaying other mating tactics. We detected little influence of the strength of sexual selection on the rate of actuarial senescence. Our findings demonstrate that the onset of actuarial senescence, rather than its rate, is a side effect of physiological mechanisms linked to sexual selection, and potentially accounts for observed differences in longevity.

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.

Males do not senesce faster in large herbivores with highly seasonal rut.

Patterns of actuarial senescence vary among long-lived species. A proposed explanation of the evolution of species-specific senescence patterns is that increased levels of energy allocation to intra-male competition decrease the amount of energy available for somatic maintenance, leading to earlier or faster actuarial senescence. Previous studies did not provide support for such relationships, but did not focus on the intensity of allocation likely to shape inter-specific variation in actuarial senescence in males. Here, by analyzing data from 56 species of captive large herbivores, we tested whether actuarial senescence is more pronounced in species displaying a well-defined 'rut' period than in species with year-round reproduction. Using an original quantitative metric of the annual duration of reproductive activity, we demonstrated that the length of the mating season has no detectable effect on actuarial senescence. On the other hand, both diet and body mass are important factors shaping actuarial senescence patterns in male captive herbivores.