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.

Disease outbreaks select for mate choice and coat color in wolves.

We know much about pathogen evolution and the emergence of new disease strains, but less about host resistance and how it is signaled to other individuals and subsequently maintained. The cline in frequency of black-coated wolves (Canis lupus) across North America is hypothesized to result from a relationship with canine distemper virus (CDV) outbreaks. We tested this hypothesis using cross-sectional data from wolf populations across North America that vary in the prevalence of CDV and the allele that makes coats black, longitudinal data from Yellowstone National Park, and modeling. We found that the frequency of CDV outbreaks generates fluctuating selection that results in heterozygote advantage that in turn affects the frequency of the black allele, optimal mating behavior, and black wolf cline across the continent.

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.

Modeling the demography of species providing extended parental care: A capture-recapture multievent model with a case study on polar bears (Ursus maritimus).

In species providing extended parental care, one or both parents care for altricial young over a period including more than one breeding season. We expect large parental investment and long-term dependency within family units to cause high variability in life trajectories among individuals with complex consequences at the population level. So far, models for estimating demographic parameters in free-ranging animal populations mostly ignore extended parental care, thereby limiting our understanding of its consequences on parents and offspring life histories.We designed a capture-recapture multievent model for studying the demography of species providing extended parental care. It handles statistical multiple-year dependency among individual demographic parameters grouped within family units, variable litter size, and uncertainty on the timing at offspring independence. It allows for the evaluation of trade-offs among demographic parameters, the influence of past reproductive history on the caring parent's survival status, breeding probability, and litter size probability, while accounting for imperfect detection of family units. We assess the model performance using simulated data and illustrate its use with a long-term dataset collected on the Svalbard polar bears (Ursus maritimus).Our model performed well in terms of bias and mean square error and in estimating demographic parameters in all simulated scenarios, both when offspring departure probability from the family unit occurred at a constant rate or varied during the field season depending on the date of capture. For the polar bear case study, we provide estimates of adult and dependent offspring survival rates, breeding probability, and litter size probability. Results showed that the outcome of the previous reproduction influenced breeding probability.Overall, our results show the importance of accounting for i) the multiple-year statistical dependency within family units, ii) uncertainty on the timing at offspring independence, and iii) past reproductive history of the caring parent. If ignored, estimates obtained for breeding probability, litter size, and survival can be biased. This is of interest in terms of conservation because species providing extended parental care are often long-living mammals vulnerable or threatened with extinction.

A meta-analysis of genome-wide association studies identifies multiple longevity genes.

Human longevity is heritable, but genome-wide association (GWA) studies have had limited success. Here, we perform two meta-analyses of GWA studies of a rigorous longevity phenotype definition including 11,262/3484 cases surviving at or beyond the age corresponding to the 90th/99th survival percentile, respectively, and 25,483 controls whose age at death or at last contact was at or below the age corresponding to the 60th survival percentile. Consistent with previous reports, rs429358 (apolipoprotein E (ApoE) ε4) is associated with lower odds of surviving to the 90th and 99th percentile age, while rs7412 (ApoE ε2) shows the opposite. Moreover, rs7676745, located near GPR78, associates with lower odds of surviving to the 90th percentile age. Gene-level association analysis reveals a role for tissue-specific expression of multiple genes in longevity. Finally, genetic correlation of the longevity GWA results with that of several disease-related phenotypes points to a shared genetic architecture between health and longevity.

How many cubs can a mum nurse? Maternal age and size influence litter size in polar bears.

Life-history theory predicts that females' age and size affect the level of maternal investment in current reproduction, balanced against the future reproductive effort, maintenance and survival. Using long-term (30 years) individual data on 193 female polar bears ( Ursus maritimus), we assessed age- and size-specific variation on litter size. Litter size varied with maternal age, younger females had higher chances of losing a cub during their first months of life. Results suggest an improvement in reproductive abilities early in life due to experience with subsequent reproductive senescence. Litter size increased with maternal size, indicating that size may reflect individual quality. We also found an optimum in the probability of having twins, suggesting stabilizing selection on female body size. Heterogeneity was observed among the largest females, suggesting that large size comes at a cost.

Frailty and Associated Factors among Centenarians in the 5-COOP Countries.

BACKGROUND: The global number of centenarians is still strongly growing and information about the health and healthcare needs of this segment of the population is needed. This study aimed to estimate the prevalence of frailty among centenarians included in a multinational study and to investigate associated factors. METHODS: The 5-COOP study is a cross-sectional survey including 1,253 centenarians in 5 countries (Japan, France, Switzerland, Denmark, and Sweden). Data were collected using a standardized questionnaire during a face-to-face interview (73.3%), telephone interview (14.5%), or by postal questionnaire (12.2%). The 5 dimensions of the frailty phenotype (weight loss, fatigue, weakness, slow walking speed, and low level of physical activity) were assessed by using self-reported data. Factors associated with frailty criteria were investigated by using multivariate regression models. RESULTS: Almost 95% of the participants had at least 1 frailty criterion. The overall prevalence of frailty (3 criteria or more) was 64.7% (from 51.5% in Sweden to 77.6% in Switzerland), and 32.2% of the participants had 4 or 5 criteria. The most frequent criteria were weakness (84.2%), slow walking speed (77.6%), and low level of physical activity (72.5%), followed by fatigue (43.8%) and weight loss (23.8%). Factors associated with frailty included data collection modes, country of residence, gender, living in institution, depression, dementia, disability, falls, and sensory impairments. CONCLUSIONS: This study shows that reaching 100 years of age rarely goes without frailty and sheds light on factors associated with frailty at a very old age.

Worldwide demography of centenarians.

The global number of centenarians should strongly increase during the 21 st century. According to the Population Division of the United Nations it should reach more than 25 million people in 2100. To better understand the dynamics of the emergence and growth of the centenarian population, we focused on four European countries having long chronological series and high quality data about centenarians, Denmark, France, Sweden, and Switzerland, and Japan which has had the highest life expectancy at birth for several years. we analysed the emergence of the centenarian populations and their pace of growth in the wider context of the adult longevity revolution, as well as the trends in mortality level among these new populations. We found that out of the 5 countries studied, the decrease in mortality at age 100 for females who are leading the adult longevity revolution, seems to be interrupted in 4 countries, including in Japan. These results are in favour of the scenario of "compression of mortality", possibly limiting the future number of centenarians. However, previous studies have shown that demographic transitions are not linear and, after periods of interruption, trends can resume towards an always greater longevity.

Unsuccessful dispersal affects life history characteristics of natal populations: The role of dispersal related variation in vital rates.

Individuals that disperse from one habitat to another has consequences for individual fitness, population dynamics and gene flow. The fitness benefits accrued in the new habitat are traded off against costs associated with dispersal. Most studies focus on costs at settlement and effects on settlement populations; the influence of dispersal to natal populations is assessed by monitoring change in numbers due to emigration. However, the extent to which natal populations are affected when individuals that invest in dispersal fail to disperse/emigrate is unclear. Here, we use an Integral Projection Model (IPM) to assess how developing into a disperser affects natal population structure and growth. We do so using the bulb mite (Rhizoglyphus robini) as a study system. Bulb mites, in unfavourable environments, develop into a dispersal (deutonymph) stage during ontogeny; these individuals are called dispersers with individuals not developing into this stage called non-dispersers. We varied disperser expression and parameterised IPMs to describe three simulations of successful and unsuccessful dispersal: (i) 'no dispersal' - dispersal stage is excluded and demographic data are from non-disperser individuals; (ii) 'false dispersal' - dispersal stage included and demographic data from non-disperser individuals are used; (iii) 'true dispersal' - dispersal stage included and demographic data are from individuals that go through the dispersal stage and from non-disperser individuals. We found that the type of dispersal simulation (no dispersal < false dispersal < true dispersal) and disperser expression increases generation time and reduces lifetime reproductive success and population growth rate. Our findings show that disperser individuals that fail to leave, can change the structure and growth of natal populations.

Age-specific cost of first reproduction in female southern elephant seals.

When to commence breeding is a crucial life-history decision that may be the most important determinant of an individual's lifetime reproductive output and can have major consequences on population dynamics. The age at which individuals first reproduce is an important factor influencing the intensity of potential costs (e.g. reduced survival) involved in the first breeding event. However, quantifying age-related variation in the cost of first reproduction in wild animals remains challenging because of the difficulty in reliably recording the first breeding event. Here, using a multi-event capture-recapture model that accounts for both imperfect detection and uncertainty in the breeding status on an 18-year dataset involving 6637 individuals, we estimated age and state-specific survival of female elephant seals (Mirounga leonina) in the declining Macquarie Island population. We detected a clear cost of first reproduction on survival. This cost was higher for both younger first-time breeders and older first-time breeders compared with females recruiting at age four, the overall mean age at first reproduction. Neither earlier primiparity nor delaying primiparity appear to confer any evolutionary advantage, rather the optimal strategy seems to be to start breeding at a single age, 4 years.

Density-dependent intraspecific aggression regulates survival in northern Yellowstone wolves (Canis lupus).

Understanding the population dynamics of top-predators is essential to assess their impact on ecosystems and to guide their management. Key to this understanding is identifying the mechanisms regulating vital rates. Determining the influence of density on survival is necessary to understand the extent to which human-caused mortality is compensatory or additive. In wolves (Canis lupus), empirical evidence for density-dependent survival is lacking. Dispersal is considered the principal way in which wolves adjust their numbers to prey supply or compensate for human exploitation. However, studies to date have primarily focused on exploited wolf populations, in which density-dependent mechanisms are likely weak due to artificially low wolf densities. Using 13 years of data on 280 collared wolves in Yellowstone National Park, we assessed the effect of wolf density, prey abundance and population structure, as well as winter severity, on age-specific survival in two areas (prey-rich vs. prey-poor) of the national park. We further analysed cause-specific mortality and explored the factors driving intraspecific aggression in the prey-rich northern area of the park. Overall, survival rates decreased during the study. In northern Yellowstone, density dependence regulated adult survival through an increase in intraspecific aggression, independent of prey availability. In the interior of the park, adult survival was less variable and density-independent, despite reduced prey availability. There was no effect of prey population structure in northern Yellowstone, or of winter severity in either area. Survival was similar among yearlings and adults, but lower for adults older than 6 years. Our results indicate that density-dependent intraspecific aggression is a major driver of adult wolf survival in northern Yellowstone, suggesting intrinsic density-dependent mechanisms have the potential to regulate wolf populations at high ungulate densities. When low prey availability or high removal rates maintain wolves at lower densities, limited inter-pack interactions may prevent density-dependent survival, consistent with our findings in the interior of the park.

Testing hypotheses in evolutionary ecology with imperfect detection: capture-recapture structural equation modeling.

Studying evolutionary mechanisms in natural populations often requires testing multifactorial scenarios of causality involving direct and indirect relationships among individual and environmental variables. It is also essential to account for the imperfect detection of individuals to provide unbiased demographic parameter estimates. To cope with these issues, we developed a new approach combining structural equation models with capture-recapture models (CR-SEM) that allows the investigation of competing hypotheses about individual and environmental variability observed in demographic parameters. We employ Markov chain Monte Carlo sampling in a Bayesian framework to (1) estimate model parameters, (2) implement a model selection procedure to evaluate competing hypotheses about causal mechanisms, and (3) assess the fit of models to data using posterior predictive checks. We illustrate the value of our approach using two case studies on wild bird populations. We first show that CR-SEM can be useful to quantify the action of selection on a set of phenotypic traits with an analysis of selection gradients on morphological traits in Common Blackbirds (Turdus merula). In a second case study on Blue Tits (Cyanistes caeruleus), we illustrate the use of CR-SEM to study evolutionary trade-offs in the wild, while accounting for varying environmental conditions.

To breed or not to breed: a seabird's response to extreme climatic events.

Intermittent breeding is an important life-history strategy that has rarely been quantified in the wild and for which drivers remain unclear. It may be the result of a trade-off between survival and reproduction, with individuals skipping breeding when breeding conditions are below a certain threshold. Heterogeneity in individual quality can also lead to heterogeneity in intermittent breeding. We modelled survival, recruitment and breeding probability of the red-footed booby (Sula sula), using a 19 year mark-recapture dataset involving more than 11,000 birds. We showed that skipping breeding was more likely in El-Niño years, correlated with an increase in the local sea surface temperature, supporting the hypothesis that it may be partly an adaptive strategy of birds to face the trade-off between survival and reproduction owing to environmental constraints. We also showed that the age-specific probability of first breeding attempt was synchronized among different age-classes and higher in El-Niño years. This result suggested that pre-breeders may benefit from lowered competition with experienced breeders in years of high skipping probabilities.

Importance of accounting for detection heterogeneity when estimating abundance: the case of French wolves.

Assessing conservation strategies requires reliable estimates of abundance. Because detecting all individuals is most often impossible in free-ranging populations, estimation procedures have to account for a <1 detection probability. Capture-recapture methods allow biologists to cope with this issue of detectability. Nevertheless, capture-recapture models for open populations are built on the assumption that all individuals share the same detection probability, although detection heterogeneity among individuals has led to underestimating abundance of closed populations. We developed multievent capture-recapture models for an open population and proposed an associated estimator of population size that both account for individual detection heterogeneity (IDH). We considered a two-class mixture model with weakly and highly detectable individuals to account for IDH. In a noninvasive capture-recapture study of wolves we based on genotypes identified in feces and hairs, we found a large underestimation of population size (27% on average) occurred when IDH was ignored.