Publications by authors named "Jean-Michel Gaillard"

147 Publications

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

Philos Trans R Soc Lond B Biol Sci 2021 Apr 8;376(1823):20190744. Epub 2021 Mar 8.

Laboratoire de Biométrie et Biologie Évolutive, CNRS, Université Lyon, Villeurbanne, France.

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?'
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http://dx.doi.org/10.1098/rstb.2019.0744DOI Listing
April 2021

Maternal effects shape offspring physiological condition but do not senesce in a wild mammal.

J Evol Biol 2021 Apr 3;34(4):661-670. Epub 2021 Mar 3.

Laboratoire de Biométrie et Biologie 8 Evolutive UMR5558, Université de Lyon, Université Lyon 1, CNRS, Villeurbanne, France.

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 influence of maternal age and body mass on offspring physiological condition in two populations of roe deer (Capreolus capreolus) subjected to markedly different environmental conditions. We measured seven markers to index body condition and characterize the immune profile in 86 fawns which became recently independent of their known-aged mothers. We did not find striking effects of maternal age on offspring physiological condition measured at 8 months of age. This absence of evidence for senescence in maternal effects is likely due to the strong viability selection observed in the very first months of life in this species. Offspring physiological condition was, on the other hand, positively influenced by maternal body mass. Between-population differences in environmental conditions experienced by fawns also influenced their average body condition and immune phenotype. Fawns facing food limitation displayed lower values in some markers of body condition (body mass and haemoglobin levels) than those living in good quality habitat. They also allocated preferentially to humoral immunity, contrary to those living in good conditions, which allocated more to cellular response. These results shed a new light on the eco-physiological pathways mediating the relationship between mother's mass and offspring condition.
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http://dx.doi.org/10.1111/jeb.13768DOI Listing
April 2021

Can we use a functional trait to construct a generalized model for ungulate populations?

Ecology 2021 Apr 3;102(4):e03289. Epub 2021 Mar 3.

Department of Zoology, University of Oxford, Tinbergen Building, South Parks Road, Oxford, OX1 3PS, United Kingdom.

Ecologists have long desired predictive models that allow inference on population dynamics, where detailed demographic data are unavailable. Integral projection models (IPMs) allow both demographic and phenotypic outcomes at the level of the population to be predicted from the distribution of a functional trait, like body mass. In species where body mass markedly influences demographic rates, as is the rule among mammals, then IPMs provide not only opportunity to assess the population responses to a given environment, but also improve our understanding of the complex interplay between traits and demographic outcomes. Here, we develop a body-mass-based approach to constructing generalized, predictive IPMs for species of ungulates covering a broad range of body size (25-400 kg). Despite our best efforts, we found that a reliable and general, functional, trait-based model for ungulates was unattainable even after accounting for among-species variation in both age at first reproduction and litter size. We attribute this to the diversity of reproductive tactics among similar-sized species of ungulates, and to the interplay between density-dependent and environmental factors that shape demographic parameters independent of mass at the local scale. These processes thus drive population dynamics and cannot be ignored. Environmental context generally matters in population ecology, and our study shows this may be the case for functional traits in vertebrate populations.
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http://dx.doi.org/10.1002/ecy.3289DOI Listing
April 2021

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

R Soc Open Sci 2020 Nov 11;7(11):200548. Epub 2020 Nov 11.

Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive, UMR5558, F-69622 Villeurbanne, France.

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.
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http://dx.doi.org/10.1098/rsos.200548DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7735339PMC
November 2020

Short-term telomere dynamics is associated with glucocorticoid levels in wild populations of roe deer.

Comp Biochem Physiol A Mol Integr Physiol 2021 02 2;252:110836. Epub 2020 Nov 2.

Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558, F-69622 Villeurbanne, France; Université de Lyon, VetAgro Sup, Marcy-l'Etoile, France.

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 shortening in two wild populations of roe deer (Capreolus capreolus) living in different ecological contexts. From two consecutive annual sampling sessions, we found that individuals with faster rates of telomere shortening had higher concentrations of fecal glucocorticoid metabolites, suggesting a functional link between glucocorticoid levels and telomere attrition rate. This relationship was consistent for both sexes and populations. This finding paves the way for further studies of the fitness consequences of exposure to environmental stressors in wild vertebrates.
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http://dx.doi.org/10.1016/j.cbpa.2020.110836DOI Listing
February 2021

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

Mech Ageing Dev 2020 12 5;192:111377. Epub 2020 Oct 5.

Univ Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Évolutive UMR 5558, F-69622, Villeurbanne, France.

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.
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http://dx.doi.org/10.1016/j.mad.2020.111377DOI Listing
December 2020

The hidden ageing costs of sperm competition.

Ecol Lett 2020 Nov 9;23(11):1573-1588. Epub 2020 Sep 9.

Evolutionary Biology, Bielefeld University, Konsequenz 45, Bielefeld, 33615, Germany.

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 the relationship linking sexual selection and ageing. Crucially, allocation to traits important in post-copulatory sexual selection, that is sperm competition, has been largely ignored. As we demonstrate, such allocation could potentially explain much diversity in male and female ageing patterns observed both within and among species. We first review how allocation to sperm competition traits such as sperm and seminal fluid production depends on the quality of resources available to males and can be associated with a wide range of deleterious effects affecting both somatic tissues and the germline, and thus modulate ageing in both survival and reproductive terms. We further hypothesise that common biological features such as plasticity, prudent sperm allocation and seasonality of ejaculate traits might have evolved as counter-adaptations to limit the ageing costs of sperm competition. Finally, we discuss the implications of these emerging ageing costs of sperm competition for current research on the evolutionary ecology of ageing.
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http://dx.doi.org/10.1111/ele.13593DOI Listing
November 2020

Competition for safe real estate, not food, drives density-dependent juvenile survival in a large herbivore.

Ecol Evol 2020 Jun 9;10(12):5464-5475. Epub 2020 Jun 9.

Laboratoire Biométrie & Biologie Évolutive CNRSUMR-CNRS 5558 University Claude Bernard - Lyon I Villeurbanne Cedex France.

Density-dependent competition for food reduces vital rates, with juvenile survival often the first to decline. A clear prediction of food-based, density-dependent competition for large herbivores is decreasing juvenile survival with increasing density. However, competition for enemy-free space could also be a significant mechanism for density dependence in territorial species. How juvenile survival is predicted to change across density depends critically on the nature of predator-prey dynamics and spatial overlap among predator and prey, especially in multiple-predator systems. Here, we used a management experiment that reduced densities of a generalist predator, coyotes, and specialist predator, mountain lions, over a 5-year period to test for spatial density dependence mediated by predation on juvenile mule deer in Idaho, USA. We tested the spatial density-dependence hypothesis by tracking the fate of 251 juvenile mule deer, estimating cause-specific mortality, and testing responses to changes in deer density and predator abundance. Overall juvenile mortality did not increase with deer density, but generalist coyote-caused mortality did, but not when coyote density was reduced experimentally. Mountain lion-caused mortality did not change with deer density in the reference area in contradiction of the food-based competition hypothesis, but declined in the treatment area, opposite to the pattern of coyotes. These observations clearly reject the food-based density-dependence hypothesis for juvenile mule deer. Instead, our results provide support for the spatial density-dependence hypothesis that competition for enemy-free space increases predation by generalist predators on juvenile large herbivores.
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http://dx.doi.org/10.1002/ece3.6289DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7319175PMC
June 2020

Reproductive senescence and parental effects in an indeterminate grower.

J Evol Biol 2020 09 31;33(9):1256-1264. Epub 2020 Jul 31.

Laboratoire Ecologie et Biologie des Interactions, UMR CNRS 7267, Université de Poitiers, Poitiers Cedex 9, France.

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 between the ages of both parents. Using the common woodlouse Armadillidium vulgare, an indeterminate grower, as a biological model, we tested for the existence of a deleterious effect of parental age on fitness components. Contrary to previous findings reported from vertebrate studies, old parents produced both a higher number and larger offspring than young parents. However, their offspring had lower fitness components (by surviving less, producing a smaller number of clutches or not reproducing at all) than offspring born to young parents. Our findings strongly support the existence of trans-generational senescence in woodlice and contradict the belief that old individuals in indeterminate growers contribute the most to recruitment and correspond thereby to the key life stage for population dynamics. Our work also provides rare evidence that the trans-generational effect of senescence can be stronger than direct reproductive senescence in indeterminate growers.
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http://dx.doi.org/10.1111/jeb.13667DOI Listing
September 2020

Pathogens Shape Sex Differences in Mammalian Aging.

Trends Parasitol 2020 08 7;36(8):668-676. Epub 2020 May 7.

Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR5558, F-69622, Villeurbanne, France; LabEx ECOFECT, Université de Lyon, F-69000, Lyon, France.

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.
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http://dx.doi.org/10.1016/j.pt.2020.05.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7203054PMC
August 2020

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

Ecol Evol 2020 May 27;10(9):4104-4114. Epub 2020 Mar 27.

Department of Biology Centre for Biodiversity Dynamics NTNU Norwegian University of Science and Technology Trondheim Norway.

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.
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http://dx.doi.org/10.1002/ece3.6181DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7244813PMC
May 2020

Evolutionary Pathways to Communal and Cooperative Breeding in Carnivores.

Am Nat 2020 06 6;195(6):1037-1055. Epub 2020 May 6.

In animal societies, individuals can cooperate in a variety of tasks, including rearing young. Such cooperation is observed in complex social systems, including communal and cooperative breeding. In mammals, both these social systems are characterized by delayed dispersal and alloparenting, whereas only cooperative breeding involves reproductive suppression. While the evolution of communal breeding has been linked to direct fitness benefits of alloparenting, the direct fitness cost of reproductive suppression has led to the hypothesis that the evolution of cooperative breeding is driven by indirect fitness benefits accrued through raising the offspring of related individuals. To decipher between the evolutionary scenarios leading to communal and cooperative breeding in carnivores, we investigated the coevolution among delayed dispersal, reproductive suppression, and alloparenting. We reconstructed ancestral states and transition rates between these traits. We found that cooperative breeding and communal breeding evolved along separate pathways, with delayed dispersal as the first step for both. The three traits coevolved, enhancing and stabilizing one another, which resulted in cooperative social systems as opposed to intermediate configurations being stable. These findings promote the key role of coevolution among traits to stabilize cooperative social systems and highlight the specificities of evolutionary patterns of sociality in carnivores.
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http://dx.doi.org/10.1086/708639DOI Listing
June 2020

The Demographic Buffering Hypothesis: Evidence and Challenges.

Trends Ecol Evol 2020 06 24;35(6):523-538. Epub 2020 Mar 24.

Department of Biology, Centre for Biodiversity Dynamics, NTNU, Norwegian University of Science and Technology, 7491 Trondheim, Norway.

In (st)age-structured populations, the long-run population growth rate is negatively affected by temporal variation in vital rates. In most cases, natural selection should minimize temporal variation in the vital rates to which the long-run population growth is most sensitive, resulting in demographic buffering. By reviewing empirical studies on demographic buffering in wild populations, we found overall support for this hypothesis. However, we also identified issues when testing for demographic buffering. In particular, solving scaling problems for decomposing, measuring, and comparing stochastic variation in vital rates and accounting for density dependence are required in future tests of demographic buffering. In the current context of climate change, demographic buffering may mitigate the negative impact of environmental variation and help populations to persist in an increasingly variable environment.
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http://dx.doi.org/10.1016/j.tree.2020.02.004DOI Listing
June 2020

Large-scale variation in birth timing and synchrony of a large herbivore along the latitudinal and altitudinal gradients.

J Anim Ecol 2020 08 25;89(8):1906-1917. Epub 2020 Jun 25.

Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland.

Hopkins' Bioclimatic Law predicts geographical patterns in phenological timing by establishing a correspondence between latitudinal and altitudinal gradients. First proposed for key phenological events of plants, such as leaf sprouting or flowering dates, this law has rarely been used to assess the geographical equivalence of key life-history traits of mammals. We hypothesize that (H1) parturition dates of European roe deer Capreolus capreolus are delayed and more synchronized at higher latitudes and altitudes, (H2) parturition timing varies along latitudinal and altitudinal gradients in a way that matches the Hopkins' Bioclimatic Law and (H3) females adjust parturition timing to match the period of high energy demand with peak resource availability. We used parturition dates of 7,444 European roe deer from Switzerland to assess altitudinal variation in birth timing and synchrony from 288 to 2,366 m a.s.l. We then performed a literature survey to compare altitudinal results with those from different populations along the species' latitudinal range of distribution. Finally, we performed spatial analysis combining our highly resolved altitudinal data on parturition dates with plant phenology data. As expected, parturition dates were delayed with increasing latitude and altitude. This delay matched the Bioclimatic Law, as the effect of 1º increase in latitude was similar to 120 m increase in altitude. However, while parturitions were more synchronized with increasing altitude, we did not detect any trend along the latitudinal gradient. Finally, plant phenology explained altitudinal variation in parturition timing better than a linear effect of altitude. Our findings clearly demonstrate the ability of a large herbivore to match parturition timing with phenological conditions across the altitudinal gradient, even at the smallest spatial scales.
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http://dx.doi.org/10.1111/1365-2656.13251DOI Listing
August 2020

How does increasing mast seeding frequency affect population dynamics of seed consumers? Wild boar as a case study.

Ecol Appl 2020 09 21;30(6):e02134. Epub 2020 May 21.

Department of Biology, Centre for Biodiversity Dynamics, Norwegian University of Science and Technology, Trondheim, 7491, Norway.

Mast seeding in temperate oak populations shapes the dynamics of seed consumers and numerous communities. Mast seeding responds positively to warm spring temperatures and is therefore expected to increase under global warming. We investigated the potential effects of changes in oak mast seeding on wild boar population dynamics, a widespread and abundant consumer species. Using long-term monitoring data, we showed that abundant acorn production enhances the proportion of breeding females. With a body-mass-structured population model and a fixed hunting rate of 0.424, we showed that high acorn production over time would lead to an average wild boar population growth rate of 1.197 whereas non-acorn production would lead to a stable population. Finally, using climate projections and a mechanistic model linking weather data to oak reproduction, we predicted that mast seeding frequency might increase over the next century, which would lead to increase in both wild boar population size and the magnitude of its temporal variation. Our study provides rare evidence that some species could greatly benefit from global warming thanks to higher food availability and therefore highlights the importance of investigating the cascading effects of changing weather conditions on the dynamics of wild animal populations to reliably assess the effects of climate change.
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http://dx.doi.org/10.1002/eap.2134DOI Listing
September 2020

Grow fast at no cost: no evidence for a mortality cost for fast early-life growth in a hunted wild boar population.

Oecologia 2020 Apr 2;192(4):999-1012. Epub 2020 Apr 2.

Centre for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology, 7491, Trondheim, Norway.

From current theories on life-history evolution, fast early-life growth to reach early reproduction in heavily hunted populations should be favored despite the possible occurrence of mortality costs later on. However, fast growth may also be associated with better individual quality and thereby lower mortality, obscuring a clear trade-off between early-life growth and survival. Moreover, fast early-life growth can be associated with sex-specific mortality costs related to resource acquisition and allocation throughout an individual's lifetime. In this study, we explore how individual growth early in life affects age-specific mortality of both sexes in a heavily hunted population. Using longitudinal data from an intensively hunted population of wild boar (Sus scrofa), and capture-mark-recapture-recovery models, we first estimated age-specific overall mortality and expressed it as a function of early-life growth rate. Overall mortality models showed that faster-growing males experienced lower mortality at all ages. Female overall mortality was not strongly related to early-life growth rate. We then split overall mortality into its two components (i.e., non-hunting mortality vs. hunting mortality) to explore the relationship between growth early in life and mortality from each cause. Faster-growing males experienced lower non-hunting mortality as subadults and lower hunting mortality marginal on age. Females of all age classes did not display a strong association between their early-life growth rate and either mortality type. Our study does not provide evidence for a clear trade-off between early-life growth and mortality.
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http://dx.doi.org/10.1007/s00442-020-04633-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7165149PMC
April 2020

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

Proc Natl Acad Sci U S A 2020 04 23;117(15):8546-8553. Epub 2020 Mar 23.

Laboratoire de Biométrie et Biologie Évolutive UMR 5558, CNRS, Université Lyon 1, F-69622 Villeurbanne, France.

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.
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http://dx.doi.org/10.1073/pnas.1911999117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7165438PMC
April 2020

Stay home, stay safe-Site familiarity reduces predation risk in a large herbivore in two contrasting study sites.

J Anim Ecol 2020 06 4;89(6):1329-1339. Epub 2020 Apr 4.

Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.

Restricting movements to familiar areas should increase individual fitness as it provides animals with information about the spatial distribution of resources and predation risk. While the benefits of familiarity for locating resources have been reported previously, the potential value of familiarity for predation avoidance has been accorded less attention. It has been suggested that familiarity should be beneficial for anti-predator behaviour when direct cues of predation risk are unclear and do not allow prey to identify well-defined spatial refuges. However, to our knowledge, this hypothesis has yet to be tested. Here, we assessed how site familiarity, measured as the intensity of use of a given location, is associated with the probability of roe deer Capreolus capreolus being killed by two predators with contrasting hunting tactics, the Eurasian lynx Lynx lynx and human hunters. While risk of human hunting was confined to open habitats, risk of lynx predation was more diffuse, with no clear refuge areas. We estimated cause-specific mortality rates in a competing risk framework for 212 GPS-collared roe deer in two ecologically distinct areas of Central Europe to test the hypothesis that the daily risk of being killed by lynx or hunters should be lower in areas of high familiarity. We found strong evidence that site familiarity reduces the risk of being predated by lynx, whereas the evidence that the risk of being hunted is linked to site familiarity was weak. We suggest that local knowledge about small-scale differences in predation risk and information about efficient escape routes affect an individual's ability to avoid or escape an attack by an ambush predator. Our study emphasizes the role of site familiarity in determining the susceptibility of prey to predation. Further research will be required to understand better how a cognitive map of individual spatial information is beneficial for avoiding predation in the arms race that drives the predator-prey shell game.
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http://dx.doi.org/10.1111/1365-2656.13202DOI Listing
June 2020

A new Editor team.

J Anim Ecol 2020 01;89(1):4-5

British Ecological Society, London, UK.

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http://dx.doi.org/10.1111/1365-2656.13165DOI Listing
January 2020

Life-history strategy varies with the strength of competition in a food-limited ungulate population.

Ecol Lett 2020 May 23;23(5):811-820. Epub 2020 Feb 23.

Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK.

Fluctuating population density in stochastic environments can contribute to maintain life-history variation within populations via density-dependent selection. We used individual-based data from a population of Soay sheep to examine variation in life-history strategies at high and low population density. We incorporated life-history trade-offs among survival, reproduction and body mass growth into structured population models and found support for the prediction that different life-history strategies are optimal at low and high population densities. Shorter generation times and lower asymptotic body mass were selected for in high-density environments even though heavier individuals had higher probabilities to survive and reproduce. In contrast, greater asymptotic body mass and longer generation times were optimal at low population density. If populations fluctuate between high density when resources are scarce, and low densities when they are abundant, the variation in density will generate fluctuating selection for different life-history strategies, that could act to maintain life-history variation.
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http://dx.doi.org/10.1111/ele.13470DOI Listing
May 2020

Skewed distributions of lifetime reproductive success: beyond mean and variance.

Ecol Lett 2020 Apr 11;23(4):748-756. Epub 2020 Feb 11.

Laboratoire de Biométrie et Biologie Evolutive, CNRS, UMR 5558, Université Lyon 1, F-69622, Villeurbanne, France.

Lifetime reproductive performance is quantified here by the LRS (lifetime reproductive success), the random number of offspring an individual produces over its lifetime. Many field studies find that distributions of LRS among individuals are non-normal, zero-inflated and highly skewed. These results beg the question, what is the distribution of LRS predicted by demographic models when the only source of randomness is demographic stochasticity? Here we present the first exact analysis of the probability distribution of LRS for species described by age + stage models; our analysis starts with estimated vital rates. We illustrate with three examples: the Hadza, human hunter-foragers (age-only), the evergreen tree Tsuga canadensis (stage-only) and Roe deer, Capreolus capreolus (age + stage). For each we obtain the exact distribution of LRS, but also calculate and discuss the first three moments. Our results point to important questions about how such LRS distributions affect natural selection, and life history evolution.
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http://dx.doi.org/10.1111/ele.13467DOI Listing
April 2020

An aging phenotype in the wild.

Science 2019 09;365(6459):1244-1245

Claude Bernard Lyon 1, Université de Lyon, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558, F-69622 Villeurbanne, France.

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http://dx.doi.org/10.1126/science.aay9493DOI Listing
September 2019

Flower phenology as a disruptor of the fruiting dynamics in temperate oak species.

New Phytol 2020 02 30;225(3):1181-1192. Epub 2019 Oct 30.

Laboratoire de Biométrie et Biologie Évolutive, UMR 5558, Université de Lyon, Université Lyon 1, CNRS, F-69622, Villeurbanne, France.

Many perennial plants display masting, that is, fruiting with strong interannual variations, irregular and synchronized between trees within the population. Here, we tested the hypothesis that the early flower phenology in temperate oak species promotes stochasticity into their fruiting dynamics, which could play a major role in tree reproductive success. From a large field monitoring network, we compared the pollen phenology between temperate and Mediterranean oak species. Then, focusing on temperate oak species, we explored the influence of the weather around the time of budburst and flowering on seed production, and simulated with a mechanistic model the consequences that an evolutionary shifting of flower phenology would have on fruiting dynamics. Temperate oak species release pollen earlier in the season than do Mediterranean oak species. Such early flowering in temperate oak species results in pollen often being released during unfavorable weather conditions and frequently results in reproductive failure. If pollen release were delayed as a result of natural selection, fruiting dynamics would exhibit much reduced stochastic variation. We propose that early flower phenology might be adaptive by making mast-seeding years rare and unpredictable, which would greatly help in controlling the dynamics of seed consumers.
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http://dx.doi.org/10.1111/nph.16224DOI Listing
February 2020

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

PLoS Biol 2019 09 13;17(9):e3000432. Epub 2019 Sep 13.

Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Évolutive UMR5558, Villeurbanne, France.

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.
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http://dx.doi.org/10.1371/journal.pbio.3000432DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6760812PMC
September 2019

Data gaps and opportunities for comparative and conservation biology.

Proc Natl Acad Sci U S A 2019 05 19;116(19):9658-9664. Epub 2019 Apr 19.

Interdisciplinary Center on Population Dynamics, University of Southern Denmark, 5230 Odense M, Denmark;

Biodiversity loss is a major challenge. Over the past century, the average rate of vertebrate extinction has been about 100-fold higher than the estimated background rate and population declines continue to increase globally. Birth and death rates determine the pace of population increase or decline, thus driving the expansion or extinction of a species. Design of species conservation policies hence depends on demographic data (e.g., for extinction risk assessments or estimation of harvesting quotas). However, an overview of the accessible data, even for better known taxa, is lacking. Here, we present the Demographic Species Knowledge Index, which classifies the available information for 32,144 (97%) of extant described mammals, birds, reptiles, and amphibians. We show that only 1.3% of the tetrapod species have comprehensive information on birth and death rates. We found no demographic measures, not even crude ones such as maximum life span or typical litter/clutch size, for 65% of threatened tetrapods. More field studies are needed; however, some progress can be made by digitalizing existing knowledge, by imputing data from related species with similar life histories, and by using information from captive populations. We show that data from zoos and aquariums in the Species360 network can significantly improve knowledge for an almost eightfold gain. Assessing the landscape of limited demographic knowledge is essential to prioritize ways to fill data gaps. Such information is urgently needed to implement management strategies to conserve at-risk taxa and to discover new unifying concepts and evolutionary relationships across thousands of tetrapod species.
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http://dx.doi.org/10.1073/pnas.1816367116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6511006PMC
May 2019

Goodbye and farewell to print.

J Anim Ecol 2019 01;88(1):4-7

British Ecological Society, London, UK.

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http://dx.doi.org/10.1111/1365-2656.12940DOI Listing
January 2019

The diversity of population responses to environmental change.

Ecol Lett 2019 Feb 9;22(2):342-353. Epub 2018 Dec 9.

Université Lyon 1, CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622, Villeurbanne, France.

The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.
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http://dx.doi.org/10.1111/ele.13195DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6378614PMC
February 2019

Pollen limitation as a main driver of fruiting dynamics in oak populations.

Ecol Lett 2019 Jan 15;22(1):98-107. Epub 2018 Oct 15.

Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, F-69622, Villeurbanne, France.

In many perennial wind-pollinated plants, the dynamics of seed production is commonly known to be highly fluctuating from year to year and synchronised among individuals within populations. The proximate causes of such seeding dynamics, called masting, are still poorly understood in oak species that are widespread in the northern hemisphere, and whose fruiting dynamics dramatically impacts forest regeneration and biodiversity. Combining long-term surveys of oak airborne pollen amount and acorn production over large-scale field networks in temperate areas, and a mechanistic modelling approach, we found that the pollen dynamics is the key driver of oak masting. Mechanisms at play involved both internal resource allocation to pollen production synchronised among trees and spring weather conditions affecting the amount of airborne pollen available for reproduction. The sensitivity of airborne pollen to weather conditions might make oak masting and its ecological consequences highly sensitive to climate change.
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http://dx.doi.org/10.1111/ele.13171DOI Listing
January 2019

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

Proc Biol Sci 2018 09 12;285(1886). Epub 2018 Sep 12.

Université de Lyon, F-69000, Lyon; Université Lyon 1; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne, France.

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 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.
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http://dx.doi.org/10.1098/rspb.2018.1479DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6158536PMC
September 2018

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

Am Nat 2018 10 23;192(4):525-536. Epub 2018 Aug 23.

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.
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http://dx.doi.org/10.1086/699513DOI Listing
October 2018