Jean-François Lemaître

French National Centre for Scientific Research | CNRS · Laboratoire de Biométrie et Biologie Évolutive (LBBE)

Significance In human populations, women live longer than men. While it is commonly assumed that this pattern of long-lived females vs. short-lived males constitutes the rule in mammals, the magnitude of the sex differences in lifespan and increase of mortality rate with advancing age remain to be quantified. Here, we demonstrate that, in the wild,...

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 respo...

Ageing and sexual selection are intimately linked. There is by now compelling evidence from studies performed across diverse organisms that males allocating resources to mating competition incur substantial physiological costs, ultimately increasing ageing. However, although insightful, we argue here that to date these studies cover only part of th...

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,...

The hygiene hypothesis, according to which the recent reduction of exposure to infectious agents in the human species would be the origin of various diseases, including autoimmune diseases and cancer, has often been proposed but not properly tested on animals. Here, we evaluated the relevance of this hypothesis to cancer risk in mammals in an origi...

Changes in the risk of exposure to infectious disease agents can be tracked through variations in antibody prevalence in vertebrate host populations. However, information on the temporal dynamics of the immune status of individuals is critical. If antibody levels persist a long time after exposure to an infectious agent, they could enable the effic...

Using DNA methylation profiles (n = 15,456) from 348 mammalian species, we constructed phyloepigenetic trees that bear marked similarities to traditional phylogenetic ones. Using unsupervised clustering across all samples, we identified 55 distinct cytosine modules, of which 30 are related to traits such as maximum life span, adult weight, age, sex...

Using DNA methylation profiles (n = 15,456) from 348 mammalian species, we constructed phyloepigenetic trees that bear marked similarities to traditional phylogenetic ones. Using unsupervised clustering across all samples, we identified 55 distinct cytosine modules, of which 30 are related to traits such as maximum life span, adult weight, age, sex...

Aging, often considered a result of random cellular damage, can be accurately estimated using DNA methylation profiles, the foundation of pan-tissue epigenetic clocks. Here, we demonstrate the development of universal pan-mammalian clocks, using 11,754 methylation arrays from our Mammalian Methylation Consortium, which encompass 59 tissue types acr...

Lifespan differences between sexes is a puzzling question in human and evolutionary biology. Sex chromosomes have been proposed as playing a central role, and the Y male chromosome has been suspected of having a toxic genomic impact in this trait. As Y chromosomes are typically enriched in transposable elements (TE), this hypothesis suggests that i...

Reproduction is a central activity for all living organisms but is also associated with a diversity of costs that are detrimental for survival. Until recently, the cost of cancer as a selective force has been poorly considered. Considering 191 mammal species, we found cancer mortality was more likely to be detected in species having large, rather t...

Environmental fluctuations force animals to adjust glucocorticoids (GCs) secretion and release to current conditions. GCs are a widely used proxy of an individual stress level. While short-term elevation in GCs is arguably beneficial for fitness components, previous studies have documented that the relationship between long-term baseline GCs elevat...

It is now broadly admitted that female reproductive senescence -a decline in reproductive performance with increasing age -occurs in most species, at least among birds and mammals.Although information is more limited, male reproductive senescence has been regularly inferred from the decline in the size or performance of phenotypic traits that under...

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 supportin...

We tested independently the influences of increasing temperature and decreasing moisture on life history and physiological traits in the arthropod Armadillidium vulgare. Both increasing temperature and decreasing moisture led reproductive success to decrease. While the density of immune cells decreased and the β-galactosidase activity increased wit...

Living in variable and unpredictable environments, organisms face recurrent stressful situations. The endocrine stress response, which includes the secretion of glucocorticoids, helps organisms to cope with these perturbations. Although short-term elevations of glucocorticoid levels are often associated with immediate beneficial consequences for in...

Actuarial senescence, the increase in adult mortality risk with increasing age, is a widespread phenomenon across the animal kingdom. Although between-species variation in the rate of increase in mortality as organisms age (i.e. ageing rate) is now well documented, the occurrence of variation in ageing rate within a given species remains much more...

We tested independently the influences of increasing temperature and decreasing moisture on life history and physiological traits in the arthropod Armadillidium vulgare. Both increasing temperature and decreasing moisture led individual body mass and reproductive success to decrease. While immune cells density decreased and β-galactosidase activity...

Environmental fluctuations force animals to adjust glucocorticoids (GCs) secretion and release to current conditions. GCs are a widely used proxy of an individual stress level. While short-term elevation in GCs is arguably beneficial for fitness components, previous studies have documented that the relationship between long-term baseline GCs elevat...

In polygynous vertebrates, males must allocate energy to growing the secondary sexual characteristics, such as ornaments or weapons, that they require to attract and defend potential mates, impacting body condition and potentially entailing fitness costs. We investigated sex differences in over winter body mass change across five intensively monito...

Habitat anthropization is a major driver of global biodiversity decline. Although most species are negatively affected, some benefit from anthropogenic habitat modifications by showing intriguing life-history responses. For instance, increased recruitment through higher allocation to reproduction or improved performance during early-life stages cou...

Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 population...

Reproduction is one of the most energetically demanding life-history stages. As a result, breeding individuals often experience trade-offs, where energy is diverted away from maintenance (cell repair, immune function) toward reproduction. While it is increasingly acknowledged that oncogenic processes are omnipresent, evolving and opportunistic enti...

Recent developments in telomere and cancer evolutionary ecology demonstrate a very complex relationship between the need of tissue repair and controlling the emergence of abnormally proliferating cells. The trade‐off is balanced by natural and sexual selection and mediated via both intrinsic and environmental factors. We explore the effects of telo...

In animals, males and females can display markedly different longevity (also called sex gaps in longevity, SGL). Sex chromosomes contribute to establishing these SGLs. X-hemizygosity and toxicity of the Y chromosomes are two mechanisms that have been suggested to reduce male longevity (Z-hemizygosity and W toxicity in females in ZW systems). In pla...

Living in variable and unpredictable environments, organisms face recurrent stressful situations. The endocrine stress response, which includes the secretion of glucocorticoids, helps organisms to cope with these perturbations. Although short-term elevations of glucocorticoid levels are often associated with immediate beneficial consequences for in...

DNA methylation-based biomarkers of aging (epigenetic clocks) promise to lead to new insights into evolutionary biology of ageing. Relatively little is known about how the natural environment affects epigenetic aging effects in wild species. In this study, we took advantage of a unique long-term (>40 years) longitudinal monitoring of individual roe...

Cancer is a ubiquitous disease of metazoans, predicted to disproportionately affect larger, long-lived organisms owing to their greater number of cell divisions, and thus increased probability of somatic mutations1,2. While elevated cancer risk with larger body size and/or longevity has been documented within species3,4,5, Peto’s paradox indicates...

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 influences 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)...

Significance Using long-term demographic studies, we showed that warmer temperatures are associated with increased senescence rates and decreased lifespans in four amphibian species that are widely distributed across two continents (North America and Europe). Our study highlights the role of changing climatic conditions in the aging of ectotherms i...

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 hig...

Little is known about the effects of environmental variation on allometric relationships of condition‐dependent traits, especially in wild populations. We estimated sex‐specific static allometry between horn length and body mass in four populations of mountain ungulates that experienced periods of contrasting density over the course of the study. T...

In animals, males and females can display markedly different longevity (also called sex gap in longevity, SGLs). Recent work has revealed that sex chromosomes contribute to establishing these SGLs. X-hemizygosity and toxicity of the Y chromosomes are two mechanisms that have been suggested to reduce male longevity (Z-hemizygosity and W toxicity in...

Comparative demographic analyses aim to identify axes of variation in vital rates and the factors that determine the position of species along these axes. These analyses can be performed using different primary data sets, with marked heterogeneity in data quality and structure. Whether the outcome of demographic comparative analyses depends on the...

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 dec...

Body size often differs between the sexes (leading to sexual size dimorphism, SSD), as a consequence of differential responses by males and females to selection pressures. Adult sex ratio (the proportion of males in the adult population, ASR) should influence SSD because ASR relates to both the number of competitors and available mates, which shape...

Maximum lifespan of a species is the oldest that individuals can survive, reflecting the genetic limit of longevity in an ideal environment. Here we report methylation-based models that accurately predict maximum lifespan (r=0.89), gestational time (r=0.96), and age at sexual maturity (r=0.87), using cytosine methylation patterns collected from ove...

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 senesce...

In vertebrates, offspring survival often decreases with increasing maternal age. While many studies have reported a decline in fitness‐related traits of offspring with increasing maternal age, the study of senescence in maternal effect through age‐specific changes in offspring physiological condition is still at its infancy. We assessed the influen...

While evidence that telomere length is associated with health and mortality in humans and birds is accumulating, a large body of research is currently seeking to identify factors that modulate telomere dynamics. We tested the hypothesis that high levels of glucocorticoids in individuals under environmental stress should accelerate telomere shorteni...

ABSTRACT Aging is often perceived as a degenerative process caused by random accrual of cellular damage over time. In spite of this, age can be accurately estimated by epigenetic clocks based on DNA methylation profiles from almost any tissue of the body. Since such pan-tissue epigenetic clocks have been successfully developed for several different...

A large part of the diversity of longevity and actuarial senescence (i.e., the progressive decline of survival probabilities with age) across vertebrates can be related to body size, phylogeny, and the species’ position on the slow-fast continuum of life histories. However, differences in mortality patterns between ecologically similar species, suc...

Aging evolutionary theories predict that patterns of actuarial and reproductive senescence should be aligned, with a common onset of senescence set at the age of first reproduction. However, a few empirical studies reported asynchrony between actuarial and reproductive senescence. This asynchrony is expected to be particularly pronounced in organis...

Sex chromosomes are typically comprised of a non-recombining region and a recombining pseudoautosomal region. Accurately quantifying the relative size of these regions is critical for sex-chromosome biology both from a functional and evolutionary perspective. The evolution of the pseudoautosomal boundary (PAB) is well documented in haplorrhines (ap...

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 vertebra...

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 senesce...

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 senesce...

DNA methylation-based biomarkers of aging (epigenetic clocks) promise to lead to new insights in the evolutionary biology of ageing. Relatively little is known about how the natural environment affects epigenetic aging effects in wild species. In this study, we took advantage of a unique long-term (>40 years) longitudinal monitoring of individual r...

There is a great deal of debate on the question of whether or not we know what ageing is (Ref. Cohen et al). Here, we consider what we believe to be the especially confused and confusing case of the ageing of the human immune system, commonly referred to as "immunosenescence". But what exactly is meant by this term? It has been used loosely in the...

Actuarial senescence (i.e., the age-specific increase in mortality rate) is pervasive across mammalian species, but our current understanding of the diversity of forms that actuarial senescence displays across species remains limited. Although several mathematical models have been proposed to model actuarial senescence, there is still no consensus...

Objectif L’espérance de vie des patients atteints du syndrome de Klinefelter est en moyenne diminuée de 2,1 ans par rapport aux sujets 46,XY eux-mêmes vivant moins longtemps que les sujets 46,XX. L’objectif était de tester l’hypothèse du rôle du chromosome Y dans la longévité par son action sur l’expression des gènes. Matériel et méthodes Dix neuf...

At a recent symposium on aging biology, a debate was held as to whether or not we know what biological aging is. Most of the participants were struck not only by the lack of consensus on this core question, but also on many basic tenets of the field. Accordingly, we undertook a systematic survey of our 71 participants on key questions that were rai...

Reproductive senescence is the decrease of reproductive performance with increasing age and can potentially include trans‐generational effects as the offspring produced by old parents might have a lower fitness than those produced by young parents. This negative effect may be caused either by the age of the father, mother, or the interaction betwee...

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 p...

Over the last few decades, comparative biology of aging has aimed to identify factors responsible for the huge variability in lifespan observed across the animal kingdom. While these studies have undeniably improved our understanding of the complex processes that shape lifespan, we argue that time has now come to focus on specific aging metrics (e....

Senescence, the decline of physiological parameters with increasing age, is a quasi-ubiquitous phenomenon in the living world. The observed patterns of senescence, however, can markedly differ across species and populations, between sexes, and even among individuals. To identify the drivers of this variation in senescence, experimental approaches a...

1. Senescence-the decline in age-specific contribution to fitness with increasing age-has been widely investigated in evolutionary ecology. A tremendous amount of detailed empirical analyses have now revealed the widespread occurrence of demographic senescence (i.e. both actuarial and reproductive senescence) and have started to identify factors (e...

Patterns of actuarial senescence can be highly variable among species. Previous comparative analyses revealed that both age at the onset of senescence and rates of senescence are linked to position of a species along the fast–slow life‐history continuum. As there are few long‐term datasets of wild populations with known‐age individuals, intraspecif...

Why a postfertile stage has evolved in females of some species has puzzled evolutionary biologists for over 50 years. We propose that existing adaptive explanations have underestimated in their formulation an important parameter operating both at the specific and the individual levels: the balance between cancer risks and cancer defenses. During th...

Understanding how wild animals adapt to perturbations and their consequences for life history traits and population dynamics is a current focus of attention in ecology and conservation biology. Here, we analysed variation in the neutrophil to lymphocyte ratio (N:L ratio), a proxy of stress level, in wild roe deer Capreolus capreolus from three popu...

Several non-human mammalian species provide grandparental care but remain fertile until death, unlike our species. This might call into question the 'grandmother hypothesis' that the ability to provide grandparental care, associated with an increase in the cost of breeding with age, promote the early cessation of reproduction. Here, we analyse indi...

Deterioration of the immune system with age increases winter mortality in Soay sheep

The concept of actuarial senescence (defined here as the increase in mortality hazard 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 lif...

Actuarial senescence has been viewed for a long time as an inevitable and uniform process. However, the work on senescence has mainly focused on endotherms with deterministic growth and low regeneration capacity during the adult stage, leading to a strong taxonomic bias in the study of aging. Recent studies have highlighted that senescence could in...