Long-lasting effects of the presence of male siblings in utero on subsequent reproductive performance.

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.

Polyphenism predicts actuarial senescence and lifespan in tiger salamanders.

Actuarial senescence (called 'senescence' hereafter) often shows broad variation at the intraspecific level. Phenotypic plasticity likely plays a central role in among-individual heterogeneity in senescence rate (i.e. the rate of increase in mortality with age), although our knowledge on this subject is still very fragmentary. Polyphenism-the unique sub-type of phenotypic plasticity where several discrete phenotypes are produced by the same genotype-may provide excellent study systems to investigate if and how plasticity affects the rate of senescence in nature. In this study, we investigated whether facultative paedomorphosis influences the rate of senescence in a salamander, Ambystoma mavortium nebulosum. Facultative paedomorphosis, a unique form of polyphenism found in dozens of urodele species worldwide, leads to the production of two discrete, environmentally induced phenotypes: metamorphic and paedomorphic individuals. We leveraged an extensive set of capture-recapture data (8948 individuals, 24 years of monitoring) that were analysed using multistate capture-recapture models and Bayesian age-dependent survival models. Multistate models revealed that paedomorphosis was the most common developmental pathway used by salamanders in our study system. Bayesian age-dependent survival models then showed that paedomorphs have accelerated senescence in both sexes and shorter adult lifespan (in females only) compared to metamorphs. In paedomorphs, senescence rate and adult lifespan also varied among ponds and individuals. Females with good body condition and high lifetime reproductive success had slower senescence and longer lifespan. Late-breeding females also lived longer but showed a senescence rate similar to that of early-breeding females. Moreover, males with good condition had longer lifespan than males with poor body condition, although they had similar senescence rates. In addition, late-breeding males lived longer but, unexpectedly, had higher senescence than early-breeding males. Overall, our work provides one of the few empirical cases suggesting that environmentally cued polyphenism could affect the senescence of a vertebrate in nature, thus providing insights on the ecological and evolutionary consequences of developmental plasticity on ageing.

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.

Decline in telomere length with increasing age across nonhuman vertebrates: A meta-analysis.

The prediction that telomere length (TL) shortens with increasing age is a major element in considering the role of telomeres as a key player in evolution. While telomere attrition is found in humans both in vitro and in vivo, the increasing number of studies reporting diverse age-specific patterns of TL challenges the hypothesis of a universal decline of TL with increasing age. Here, we performed a meta-analysis to estimate the relationship between TL and age across 175 estimates encompassing 98 species of vertebrates. We found that, on average, TL does decline with increasing age during adulthood. However, this decline was weak and variable across vertebrate classes, and we also found evidence for a publication bias that might weaken our current evidence of decreasing TL with increasing age. We found no evidence for a faster decline in TL with increasing age when considering the juvenile stage (from birth to age at first reproduction) compared to the adult stage. Heterogeneity in TL ageing rates was explained by the method used to measure telomeres: detectable TL declines with increasing age were found only among studies using TRF with in-gel hybridisation and qFISH methods, but not in studies using qPCR and Southern blot-based TRF methods. While we confirmed that TL declines with increasing age in most adult vertebrates, our results identify an influence of telomere measurement methodology, which highlights the need to examine more thoroughly the effect of the method of measurement on TL estimates.

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.

The kinship matrix: inferring the kinship structure of a population from its demography.

The familial structure of a population and the relatedness of its individuals are determined by its demography. There is, however, no general method to infer kinship directly from the life cycle of a structured population. Yet, this question is central to fields such as ecology, evolution and conservation, especially in contexts where there is a strong interdependence between familial structure and population dynamics. Here, we give a general formula to compute, from any matrix population model, the expected number of arbitrary kin (sisters, nieces, cousins, etc) of a focal individual ego, structured by the class of ego and of its kin. Central to our approach are classic but little-used tools known as genealogical matrices. Our method can be used to obtain both individual-based and population-wide metrics of kinship, as we illustrate. It also makes it possible to analyse the sensitivity of the kinship structure to the traits implemented in the model.

Sex differences in adult lifespan and aging rate across mammals: A test of the 'Mother Curse hypothesis'.

In many animal species, including humans, males have shorter lifespan and show faster survival aging than females. This differential increase in mortality between sexes could result from the accumulation of deleterious mutations in the mitochondrial genome of males due to the maternal mode of mtDNA inheritance. To date, empirical evidence supporting the existence of this mechanism - called the Mother Curse hypothesis - remains largely limited to a few study cases in humans and Drosophila. In this study, we tested whether the Mother Curse hypothesis accounts for sex differences in lifespan and aging rate across 128 populations of mammals (60 and 68 populations studied in wild and captive conditions, respectively) encompassing 104 species. We found that adult lifespan decreases with increasing mtDNA neutral substitution rate in both sexes in a similar way in the wild - but not in captivity. Moreover, the aging rate marginally increased with neutral substitution rate in males and females in the wild. Overall, these results indicate that the Mother Curse hypothesis is not supported across mammals. We further discuss the implication of these findings for our understanding of the evolution of sex differences in mortality and aging.

Sex-related differences in aging rate are associated with sex chromosome system in amphibians.

Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture-recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the "unguarded X/Z effect") or repeat-rich Y/W chromosome (the "toxic Y/W effect") could accelerate aging in the heterogametic sex in some vertebrate clades.

Is degree of sociality associated with reproductive senescence? A comparative analysis across birds and mammals.

Our understanding on how widespread reproductive senescence is in the wild and how the onset and rate of reproductive senescence vary among species in relation to life histories and lifestyles is currently limited. More specifically, whether the species-specific degree of sociality is linked to the occurrence, onset and rate of reproductive senescence remains unknown. Here, we investigate these questions using phylogenetic comparative analyses across 36 bird and 101 mammal species encompassing a wide array of life histories, lifestyles and social traits. We found that female reproductive senescence: (i) is widespread and occurs with similar frequency (about two-thirds) in birds and mammals; (ii) occurs later in life and is slower in birds than in similar-sized mammals; (iii) occurs later in life and is slower with an increasingly slower pace of life in both vertebrate classes; and (iv) is only weakly associated, if any, with the degree of sociality in both classes after accounting for the effect of body size and pace of life. However, when removing the effect of species differences in pace of life, a higher degree of sociality was associated with later and weaker reproductive senescence in females, which suggests that the degree of sociality is either indirectly related to reproductive senescence via the pace of life or simply a direct outcome of the pace of life. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Female reproductive senescence across mammals: A high diversity of patterns modulated by life history and mating traits.

Senescence patterns are highly variable across the animal kingdom. However, while empirical evidence of actuarial senescence in vertebrates is accumulating in the wild and life history correlates of actuarial senescence are increasingly identified, both the extent and variation of reproductive senescence across species remain poorly studied. Here, we performed the first large-scale analysis of female reproductive senescence across 101 mammalian species that encompassed a wide range of Orders. We found evidence of reproductive senescence in 68.31 % of the species, which demonstrates that reproductive senescence is pervasive in mammals. As expected from allometric rules, the onset of reproductive senescence occurs later and the rate of reproductive senescence decreases with increasing body mass and delayed age at first reproduction. Moreover, for a given pace of life, females displaying a high level of multiple mating and/or with induced ovulation senesce earlier than females displaying a low level of multiple mating and/or with spontaneous ovulation. These results suggest that both female mating behavior and reproductive physiology shape the diversity of reproductive senescence patterns across mammals. We propose future avenues of research regarding the role played by environmental conditions or reproductive features (e.g. type of placentation) on the evolution of reproductive senescence.

No sex differences in adult telomere length across vertebrates: a meta-analysis.

In many mammalian species, females live on average longer than males. In humans, women have consistently longer telomeres than men, and this has led to speculation that sex differences in telomere length (TL) could play a role in sex differences in longevity. To address the generality and drivers of patterns of sex differences in TL across vertebrates, we performed meta-analyses across 51 species. We tested two main evolutionary hypotheses proposed to explain sex differences in TL, namely the heterogametic sex disadvantage and the sexual selection hypotheses. We found no support for consistent sex differences in TL between males and females among mammal, bird, fish and reptile species. This absence of sex differences in TL across different classes of vertebrates does not support the heterogametic sex disadvantage hypothesis. Likewise, the absence of any negative effect of sexual size dimorphism on male TL suggests that sexual selection is not likely to mediate the magnitude of sex differences in TL across vertebrates. Finally, the comparative analyses we conducted did not detect any association between sex differences in TL and sex differences in longevity, which does not support the idea that sex differences in TL could explain the observed sex differences in longevity.

Causes and consequences of variation in offspring body mass: meta-analyses in birds and mammals.

Early survival is highly variable and strongly influences observed population growth rates in most vertebrate populations. One of the major potential drivers of survival variation among juveniles is body mass. Heavy juveniles are better fed and have greater body reserves, and are thus assumed to survive better than light individuals. In spite of this, some studies have failed to detect an influence of body mass on offspring survival, questioning whether offspring body mass does indeed consistently influence juvenile survival, or whether this occurs in particular species/environments. Furthermore, the causes for variation in offspring mass are poorly understood, although maternal mass has often been reported to play a crucial role. To understand why offspring differ in body mass, and how this influences juvenile survival, we performed phylogenetically corrected meta-analyses of both the relationship between offspring body mass and offspring survival in birds and mammals and the relationship between maternal mass and offspring mass in mammals. We found strong support for an overall positive effect of offspring body mass on survival, with a more pronounced influence in mammals than in birds. An increase of one standard deviation of body mass increased the odds of offspring survival by 71% in mammals and by 44% in birds. A cost of being too fat in birds in terms of flight performance might explain why body mass is a less reliable predictor of offspring survival in birds. We then looked for moderators explaining the among-study differences reported in the intensity of this relationship. Surprisingly, sex did not influence the intensity of the offspring mass-survival relationship and phylogeny only accounted for a small proportion of observed variation in the intensity of that relationship. Among the potential factors that might affect the relationship between mass and survival in juveniles, only environmental conditions was influential in mammals. Offspring survival was most strongly influenced by body mass in captive populations and wild populations in the absence of predation. We also found support for the expected positive effect of maternal mass on offspring mass in mammals (rpearson = 0.387). As body mass is a strong predictor of early survival, we expected heavier mothers to allocate more to their offspring, leading them to be heavier and so to have a higher survival. However, none of the potential factors we tested for variation in the maternal mass-offspring mass relationship had a detectable influence. Further studies should focus on linking these two relationships to determine whether a strong effect of offspring size on early survival is associated with a high correlation coefficient between maternal mass and offspring mass.

The 'Evo-Demo' Implications of Condition-Dependent Mortality.

Animals in the wild die from a variety of different mortality sources, including predation, disease, and starvation. Different mortality sources selectively remove individuals with different body condition in different ways, and this variation in the condition dependence of mortality has evolutionary and demographic implications. Subsequent population dynamics are influenced by the strength of condition-dependent mortality during specific periods, with population growth impacted in different ways in short- versus long-lived species. The evolution of lifespan is strongly influenced by condition-dependent mortality, with strikingly different outcomes expected in senescence rates when the relationship between condition and mortality is altered. A coupling of field and laboratory studies is now required to further reveal the evolutionary implications of condition-dependent mortality.