Heat over heritability: Increasing body size in response to global warming is not stabilized by genetic effects in Bechstein's bats.

How well populations can cope with global warming will often depend on the evolutionary potential and plasticity of their temperature-sensitive, fitness-relevant traits. In Bechstein's bats (Myotis bechsteinii), body size has increased over the last decades in response to warmer summers. If this trend continues it may threaten populations as larger females exhibit higher mortality. To assess the evolutionary potential of body size, we applied a Bayesian 'animal model' to estimate additive genetic variance, heritability and evolvability of body size, based on a 25-year pedigree of 332 wild females. Both heritability and additive genetic variance were reduced in hot summers compared to average and cold summers, while evolvability of body size was generally low. This suggests that the observed increase in body size was mostly driven by phenotypic plasticity. Thus, if warm summers continue to become more frequent, body size likely increases further and the resulting fitness loss could threaten populations.

Long-term field study reveals that warmer summers lead to larger and longer-lived females only in northern populations of Natterer's bats.

Animals often respond to climate change with changes in morphology, e.g., shrinking body size with increasing temperatures, as expected by Bergmann's rule. Because small body size can have fitness costs for individuals, this trend could threaten populations. Recent studies, however, show that morphological responses to climate change and the resulting fitness consequences cannot be generalized even among related species. In this long-term study, we investigate the interaction between ambient temperature, body size and survival probability in a large number of individually marked wild adult female Natterer's bats (Myotis nattereri). We compare populations from two geographical regions in Germany with a different climate. In a sliding window analysis, we found larger body sizes in adult females that were raised in warmer summers only in the northern population, but not in the southern population that experienced an overall warmer climate. With a capture-mark-recapture approach, we showed that larger individuals had higher survival rates, demonstrating that weather conditions in early life could have long-lasting fitness effects. The different responses in body size to warmer temperatures in the two regions highlight that fitness-relevant morphological responses to climate change have to be viewed on a regional scale and may affect local populations differently.

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.

Data gaps and opportunities for comparative and conservation biology.

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.

Long-term study shows that increasing body size in response to warmer summers is associated with a higher mortality risk in a long-lived bat species.

Change in body size is one of the universal responses to global warming, with most species becoming smaller. While small size in most species corresponds to low individual fitness, small species typically show high population growth rates in cross-species comparisons. It is unclear, therefore, how climate-induced changes in body size ultimately affect population persistence. Unravelling the relationship between body size, ambient temperature and individual survival is especially important for the conservation of endangered long-lived mammals such as bats. Using an individual-based 24-year dataset from four free-ranging Bechstein's bat colonies (Myotis bechsteinii), we show for the first time a link between warmer summer temperatures, larger body sizes and increased mortality risk. Our data reveal a crucial time window in June-July, when juveniles grow to larger body sizes in warmer conditions. Body size is also affected by colony size, with larger colonies raising larger offspring. At the same time, larger bats have higher mortality risks throughout their lives. Our results highlight the importance of understanding the link between warmer weather and body size as a fitness-relevant trait for predicting species-specific extinction risks as consequences of global warming.

Diversity of ageing across the tree of life.

Evolution drives, and is driven by, demography. A genotype moulds its phenotype's age patterns of mortality and fertility in an environment; these two patterns in turn determine the genotype's fitness in that environment. Hence, to understand the evolution of ageing, age patterns of mortality and reproduction need to be compared for species across the tree of life. However, few studies have done so and only for a limited range of taxa. Here we contrast standardized patterns over age for 11 mammals, 12 other vertebrates, 10 invertebrates, 12 vascular plants and a green alga. Although it has been predicted that evolution should inevitably lead to increasing mortality and declining fertility with age after maturity, there is great variation among these species, including increasing, constant, decreasing, humped and bowed trajectories for both long- and short-lived species. This diversity challenges theoreticians to develop broader perspectives on the evolution of ageing and empiricists to study the demography of more species.

The emergence of longevous populations.

The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Constant mortality and fertility over age in Hydra.

Senescence, the increase in mortality and decline in fertility with age after maturity, was thought to be inevitable for all multicellular species capable of repeated breeding. Recent theoretical advances and compilations of data suggest that mortality and fertility trajectories can go up or down, or remain constant with age, but the data are scanty and problematic. Here, we present compelling evidence for constant age-specific death and reproduction rates in Hydra, a basal metazoan, in a set of experiments comprising more than 3.9 million days of observations of individual Hydra. Our data show that 2,256 Hydra from two closely related species in two laboratories in 12 cohorts, with cohort age ranging from 0 to more than 41 y, have extremely low, constant rates of mortality. Fertility rates for Hydra did not systematically decline with advancing age. This falsifies the universality of the theories of the evolution of aging that posit that all species deteriorate with age after maturity. The nonsenescent life history of Hydra implies levels of maintenance and repair that are sufficient to prevent the accumulation of damage for at least decades after maturity, far longer than the short life expectancy of Hydra in the wild. A high proportion of stem cells, constant and rapid cell turnover, few cell types, a simple body plan, and the fact that the germ line is not segregated from the soma are characteristics of Hydra that may make nonsenescence feasible. Nonsenescence may be optimal because lifetime reproduction may be enhanced more by extending adult life spans than by increasing daily fertility.

COMADRE: a global data base of animal demography.

UNLABELLED: The open-data scientific philosophy is being widely adopted and proving to promote considerable progress in ecology and evolution. Open-data global data bases now exist on animal migration, species distribution, conservation status, etc. However, a gap exists for data on population dynamics spanning the rich diversity of the animal kingdom world-wide. This information is fundamental to our understanding of the conditions that have shaped variation in animal life histories and their relationships with the environment, as well as the determinants of invasion and extinction. Matrix population models (MPMs) are among the most widely used demographic tools by animal ecologists. MPMs project population dynamics based on the reproduction, survival and development of individuals in a population over their life cycle. The outputs from MPMs have direct biological interpretations, facilitating comparisons among animal species as different as Caenorhabditis elegans, Loxodonta africana and Homo sapiens. Thousands of animal demographic records exist in the form of MPMs, but they are dispersed throughout the literature, rendering comparative analyses difficult. Here, we introduce the COMADRE Animal Matrix Database, an open-data online repository, which in its version 1.0.0 contains data on 345 species world-wide, from 402 studies with a total of 1625 population projection matrices. COMADRE also contains ancillary information (e.g. ecoregion, taxonomy, biogeography, etc.) that facilitates interpretation of the numerous demographic metrics that can be derived from its MPMs. We provide R code to some of these examples. SYNTHESIS: We introduce the COMADRE Animal Matrix Database, a resource for animal demography. Its open-data nature, together with its ancillary information, will facilitate comparative analysis, as will the growing availability of databases focusing on other aspects of the rich animal diversity, and tools to query and combine them. Through future frequent updates of COMADRE, and its integration with other online resources, we encourage animal ecologists to tackle global ecological and evolutionary questions with unprecedented sample size.

Artificially raised roost temperatures lead to larger body sizes in wild bats.

Climate warming has major consequences for animal populations, as ambient temperature profoundly influences all organisms' physiology, behavior, or both.1 Body size in many organisms has been found to change with increased ambient temperatures due to influences on metabolism and/or access to resources.2,3,4,5,6 Changes in body size, in turn, can affect the dynamics and persistence of populations.7 Notably, in some species, body size has increased over the last decades in response to warmer temperatures.3,8 This has primarily been attributed to higher food availability,3 but might also result from metabolic savings in warmer environments.9,10 Bechstein's bats (Myotis bechsteinii) grow to larger body sizes in warmer summers,11 which affects their demography as larger females reproduce earlier at the expense of a shorter life expectancy.12,13 However, it remains unclear whether larger body sizes in warmer summers were due to thermoregulatory benefits or due to increased food availability. To disentangle these effects, we artificially heated communal day roosts of wild maternity colonies over four reproductive seasons. We used generalized mixed models to analyze these experimental results along with 25 years of long-term data comprising a total of 741 juveniles. We found that individuals raised in heated roosts grew significantly larger than those raised in unheated conditions. This suggests that metabolic savings in warmer conditions lead to increased body size, potentially resulting in the decoupling of body growth from prey availability. Our study highlights a direct mechanism by which climate change may alter fitness-relevant traits, with potentially dire consequences for population persistence.

Global warming leads to larger bats with a faster life history pace in the long-lived Bechstein's bat (Myotis bechsteinii).

Whether species can cope with environmental change depends considerably on their life history. Bats have long lifespans and low reproductive rates which make them vulnerable to environmental changes. Global warming causes Bechstein's bats (Myotis bechsteinii) to produce larger females that face a higher mortality risk. Here, we test whether these larger females are able to offset their elevated mortality risk by adopting a faster life history. We analysed an individual-based 25-year dataset from 331 RFID-tagged wild bats and combine genetic pedigrees with data on survival, reproduction and body size. We find that size-dependent fecundity and age at first reproduction drive the observed increase in mortality. Because larger females have an earlier onset of reproduction and shorter generation times, lifetime reproductive success remains remarkably stable across individuals with different body sizes. Our study demonstrates a rapid shift to a faster pace of life in a mammal with a slow life history.

Precipitation during two weeks in spring influences reproductive success of first-year females in the long-lived Natterer's bat.

Bats are characterized by low reproductive rates in contrast with most of other small mammals. This makes their populations vulnerable when inclement environmental conditions such as cold and rainy weather impair the reproductive success of females. The fine-scale effect of weather on bats, however, remains largely unknown. Using a sliding window analysis approach on an 18-year individualized dataset on six Natterer's bat (Myotis nattereri) colonies, we investigated the effect of fine-scale weather conditions on age-specific reproductive success. We found that increased precipitation during a short time window in spring strongly reduced the probability of successful reproduction of first-year (FY) females. Our data suggest that this time window is concomitant with implantation or early pregnancy, before substantial investment into embryo development. In addition, larger FY had higher reproductive success, suggesting that reproduction may be condition dependent in young females. Reproductive success of older females was not affected by either weather or individual parameters. Our results show that changes in precipitation pattern may compromise the reproductive success of FY females. Further studies are needed to better understand the impact of weather conditions on reproductive success in long-lived bats under climate change scenarios.

Deterioration, death and the evolution of reproductive restraint in late life.

Explaining why organisms schedule reproduction over their lifetimes in the various ways that they do is an enduring challenge in biology. An influential theoretical prediction states that organisms should increasingly invest in reproduction as they approach the end of their life. An apparent mismatch of empirical data with this prediction has been attributed to age-related constraints on the ability to reproduce. Here we present a general framework for the evolution of age-related reproductive trajectories. Instead of characterizing an organism by its age, we characterize it by its physiological condition. We develop a common currency that if maximized at each time guarantees the whole life history is optimal. This currency integrates reproduction, mortality and changes in condition. We predict that under broad conditions it will be optimal for organisms to invest less in reproduction as they age, thus challenging traditional interpretations of age-related traits and renewing debate about the extent to which observed life histories are shaped by constraint versus adaptation. Our analysis gives a striking illustration of the differences between an age-based and a condition-based approach to life-history theory. It also provides a unified account of not only standard life-history models but of related models involving the allocation of limited resources.

Differences in seasonal survival suggest species-specific reactions to climate change in two sympatric bat species.

Long-lived animals with a low annual reproductive output need a long time to recover from population crashes and are, thus, likely to face high extinction risk, if the current global environmental change will increase mortality rates. To aid conservation of those species, knowledge on the variability of mortality rates is essential. Unfortunately, however, individual-based multiyear data sets that are required for that have only rarely been collected for free-ranging long-lived mammals. Here, we used a five-year data set comprising activity data of 1,445 RFID-tagged individuals of two long-lived temperate zone bat species, Natterer's bats (Myotis nattereri) and Daubenton's bats (Myotis daubentonii), at their joint hibernaculum. Both species are listed as being of high conservation interest by the European Habitats Directive. Applying mixed-effects logistic regression, we explored seasonal survival differences in these two species which differ in foraging strategy and phenology. In both species, survival over the first winter of an individual's life was much lower than survival over subsequent winters. Focussing on adults only, seasonal survival patterns were largely consistent with higher winter and lower summer survival but varied in its level across years in both species. Our analyses, furthermore, highlight the importance of species-specific time periods for survival. Daubenton's bats showed a much stronger difference in survival between the two seasons than Natterer's bats. In one exceptional winter, the population of Natterer's bats crashed, while the survival of Daubenton's bats declined only moderately. While our results confirm the general seasonal survival pattern typical for hibernating mammals with higher winter than summer survival, they also show that this pattern can be reversed under particular conditions. Overall, our study points toward a high importance of specific time periods for population dynamics and suggests species-, population-, and age class-specific responses to global climate change.

Rare catastrophic events drive population dynamics in a bat species with negligible senescence.

Bats are remarkably long-lived with lifespans exceeding even those of same-sized birds. Despite a recent interest in the extraordinary longevity of bats very little is known about the shape of mortality over age, and how mortality rates are affected by the environment. Using a large set of individual-based data collected over 19 years in four free-ranging colonies of Bechstein's bats (Myotis bechsteinii), we found no increase in the rate of mortality and no decrease in fertility demonstrating no senescence until high ages. Our finding of negligible senescence is highly unusual for long-lived mammals, grouping Bechstein's bats with long-lived seabirds. The most important determinant of adult mortality was one particular winter season, which affected all ages and sizes equally. Apart from this winter, mortality risk did not differ between the winter and the summer season. Colony membership, a proxy for local environmental conditions, also had no effect. In addition to their implications for understanding the extra-ordinary longevity in bats, our results have strong implications for the conservation of bats, since rare catastrophic mortality events can only be detected in individual based long-term field studies. With many bat species globally threatened, such data are crucial for the successful implementation of conservation programs.

No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl.

Understanding immune function in the context of other life-history traits is crucial to understand the evolution of life histories, at both the individual and species levels. As the interest in assessing immune function for these comparative purposes grows, an important question remains unanswered: can immune function be broadly characterized using one or two simple measures? Often, interpretation of individual assays is ambiguous and relationships among different measures of immune function remain poorly understood. Thus, we employed five protocols to measure 13 variables of immune function in ten species of waterfowl (Anseriformes). All assays were based on a single blood sample subdivided into leukocyte (blood smear) and plasma (frozen until analysis) components. All assays were run using samples from every individual, and a nested analysis was used to partition variation/covariation at the levels of species and individuals within species. We detected positive correlations between functionally related measures of immunity within species, but these were absent from comparisons between species. A canonical correlation analysis revealed no significant relationships between the plasma and leukocyte assays at the levels of both individual and species, suggesting that these measures of immunity are neither competitive nor synergistic. We conclude that one measure of each assay type may be required to maximally characterize immune function in studies of a single species, while the same is not true in studies among species.

Worker lifespan is an adaptive trait during colony establishment in the long-lived ant Lasius niger.

Eusociality has been recognized as a strong driver of lifespan evolution. While queens show extraordinary lifespans of 20years and more, worker lifespan is short and variable. A recent comparative study found that in eusocial species with larger average colony sizes the disparities in the lifespans of the queen and the worker are also greater, which suggests that lifespan might be an evolved trait. Here, we tested whether the same pattern holds during colony establishment: as colonies grow larger, worker lifespan should decrease. We studied the mortality of lab-reared Lasius niger workers from colonies at two different developmental stages (small and intermediate-sized) in a common garden experiment. Workers were kept in artificial cohorts that differed only with respect to the stage of the colony they were born in. We found that the stage of the birth colony affected the body size and the survival probability of the workers. The workers that had emerged from early stage colonies were smaller and had lower mortality during the first 400days of their life than the workers born in colonies at a later stage. Our results suggest that early stage colonies produce small workers with an increased survival probability. These workers are gradually augmented by larger workers with a decreased survival probability that serve as a redundant workforce with easily replaceable individuals. We doubt that the observed differences in lifespan are driven by differences in body size. Rather, we suspect that physiological mechanisms are the basis for the observed differences in lifespan.

Is food availability a circannual zeitgeber in tropical birds? A field experiment on stonechats in tropical Africa.

Equatorial stonechats (Saxicola torquata axillaris) in Africa are seasonal breeders like their temperate-zone conspecifics (S.t. rubicola). Their annual cycle in gonadal size and function is controlled by an endogenous circannual rhythmicity that has been shown to run for up to 10 years in a constant equatorial photoperiod under laboratory conditions, with a period deviating from 12 months. In nature, however, this rhythm is synchronized with the actual year. Because photoperiod is essentially constant at the equator, it is likely that other environmental factors act as zeitgebers. The authors test whether food availability affects reproductive cycles of free-living East African stonechats. The authors offered supplemental food to the birds 2 months before the regular onset of the breeding season. Supplementally fed males started to sing and display earlier than males of control pairs that did not receive extra food. Although the supplemented food advanced the onset of the breeding season in the pairs that were fed, the onset of the postnuptial molt following the breeding season was not correspondingly shifted. Furthermore, in the year following the experiment, all pairs initiated breeding at the same time. The authors conclude that food availability does not act as a zeitgeber, but rather as a factor that modifies the timing of reproduction without affecting the underlying rhythmicity. The authors propose that this is adaptive under environmental conditions that are relatively constant within a given year but may vary considerably between years. The zeitgeber synchronizing the endogenous rhythmicity remains to be identified.

Ant Colonies Do Not Trade-Off Reproduction against Maintenance.

The question on how individuals allocate resources into maintenance and reproduction is one of the central questions in life history theory. Yet, resource allocation into maintenance on the organismic level can only be measured indirectly. This is different in a social insect colony, a "superorganism" where workers represent the soma and the queen the germ line of the colony. Here, we investigate whether trade-offs exist between maintenance and reproduction on two levels of biological organization, queens and colonies, by following single-queen colonies of the ant Cardiocondyla obscurior throughout the entire lifespan of the queen. Our results show that maintenance and reproduction are positively correlated on the colony level, and we confirm results of an earlier study that found no trade-off on the individual (queen) level. We attribute this unexpected outcome to the existence of a positive feedback loop where investment into maintenance (workers) increases the rate of resource acquisition under laboratory conditions. Even though food was provided ad libitum, variation in productivity among the colonies suggests that resources can only be utilized and invested into additional maintenance and reproduction by the colony if enough workers are available. The resulting relationship between per-capita and colony productivity in our study fits well with other studies conducted in the field, where decreasing per-capita productivity and the leveling off of colony productivity have been linked to density dependent effects due to competition among colonies. This suggests that the absence of trade-offs in our laboratory study might also be prevalent under natural conditions, leading to a positive association of maintenance, (= growth) and reproduction. In this respect, insect colonies resemble indeterminate growing organisms.

Testosterone in tropical birds: effects of environmental and social factors.

Previous investigations suggest that male tropical birds have lower plasma testosterone concentrations than northern latitude species. To test whether this generalization is valid, we analyzed all currently available plasma testosterone data of tropical birds. We focused on peak breeding testosterone levels using phylogenetic and conventional statistics. Explanatory variables considered were social mating system, type of territoriality, breeding season length, and altitude. On average, tropical birds had lower mean peak testosterone levels than northern temperate birds. However, in several tropical species, testosterone levels were well within the range of northern latitude birds. Without controlling for phylogeny, breeding season length, type of territoriality, and altitude explained a significant proportion of the variance in testosterone levels. The shorter the breeding season, the higher the testosterone levels. Tropical birds that defend a breeding season territory had higher testosterone levels than birds that were year-round territorial or colonial, and testosterone levels were positively correlated with altitude. When controlling for phylogeny, only breeding season length predicted testosterone levels. In conclusion, we propose to refine previous notions of low plasma testosterone levels in tropical birds: short breeding seasons and perhaps environmental conditions at high altitudes precipitate conditions under which high testosterone levels are beneficial in the tropics.