Warming temperatures drive at least half of the magnitude of long-term trait changes in European birds.

SignificanceClimate change is impacting wild populations, but its relative importance compared to other causes of change is still unclear. Many studies assume that changes in traits primarily reflect effects of climate change, but this assumption is rarely tested. We show that in European birds global warming was likely the single most important contributor to temporal trends in laying date, body condition, and offspring number. However, nontemperature factors were also important and acted in the same direction, implying that attributing temporal trends solely to rising temperatures overestimates the impact of climate warming. Differences among species in the amount of trait change were predominantly determined by these nontemperature effects, suggesting that species differences are not due to variation in sensitivity to temperature.

Adaptive potential in the face of a transmissible cancer in Tasmanian devils.

Emerging infectious diseases (EIDs) not only cause catastrophic declines in wildlife populations but also generate selective pressures that may result in rapid evolutionary responses. One such EID is devil facial tumour disease (DFTD) in the Tasmanian devil. DFTD is almost always fatal and has reduced the average lifespan of individuals by around 2 years, likely causing strong selection for traits that reduce susceptibility to the disease, but population decline has also left Tasmanian devils vulnerable to inbreeding depression. We analysed 22 years of data from an ongoing study of a population of Tasmanian devils on Freycinet Peninsula, Tasmania, to (1) identify whether DFTD may be causing selection on body size, by estimating phenotypic and genetic correlations between DFTD and size traits, (2) estimate the additive genetic variance of susceptibility to DFTD, and (3) investigate whether size traits or susceptibility to DFTD were under inbreeding depression. We found a positive phenotypic relationship between head width and susceptibility to DFTD, but this was not underpinned by a genetic correlation. Conversely, we found a negative phenotypic relationship between body weight and susceptibility to DFTD, and there was evidence for a negative genetic correlation between susceptibility to DFTD and body weight. There was additive genetic variance in susceptibility to DFTD, head width and body weight, but there was no evidence for inbreeding depression in any of these traits. These results suggest that Tasmanian devils have the potential to respond adaptively to DFTD, although the realised evolutionary response will critically further depend on the evolution of DFTD itself.

Testing the evolutionary potential of an alpine plant: phenotypic plasticity in response to growth temperature outweighs parental environmental effects and other genetic causes of variation.

Phenotypic plasticity and rapid evolution are fundamental processes by which organisms can maintain their function and fitness in the face of environmental changes. Here we quantified the plasticity and evolutionary potential of an alpine herb Wahlenbergia ceracea. Utilizing its mixed-mating system, we generated outcrossed and self-pollinated families that were grown in either cool or warm environments, and that had parents that had also been grown in either cool or warm environments. We then analysed the contribution of environmental and genetic factors to variation in a range of phenotypic traits including phenology, leaf mass per area, photosynthetic function, thermal tolerance, and reproductive fitness. The strongest effect was that of current growth temperature, indicating strong phenotypic plasticity. All traits except thermal tolerance were plastic, whereby warm-grown plants flowered earlier, grew larger, and produced more reproductive stems compared with cool-grown plants. Flowering onset and biomass were heritable and under selection, with early flowering and larger plants having higher relative fitness. There was little evidence for transgenerational plasticity, maternal effects, or genotype×environment interactions. Inbreeding delayed flowering and reduced reproductive fitness and biomass. Overall, we found that W. ceracea has the capacity to respond rapidly to climate warming via plasticity, and the potential for evolutionary change.

Antler size in red deer: declining selection and increasing genetic variance with age, but little senescence.

While senescence is a common occurrence in wild populations, not all traits decline with age simultaneously and some do not show any senescence. A lack of senescence in secondary sexual traits is thought to be due to their importance for reproductive success. However, if reproductive success senesces, why would secondary sexual traits apparently not senesce? Here, we explored this question in a wild population of red deer (Cervus elaphus) using antler form (number of points), a secondary sexual trait which shows little senescence, despite the occurrence of reproductive senescence. In line with expectations for traits that senesce, genetic variance in antler form increased with age and selection weakened with age. Therefore, there was no indication that a stronger selection on individuals that survived to older ages was countering the dilution of selection due to fewer individuals being alive. Furthermore, the effect of selective disappearance masking a slight decline in antler form in the oldest years was small. Interestingly, although genetic variance and positive selection of antler form were found, there was no evidence of a response to selection, supporting a genetic decoupling of antler senescence and reproductive senescence. Finally, a positive genetic covariance in antler form among age classes provides a possible explanation for the lack of senescence. These findings suggest that the antler form is under a genetic constraint that prevents it from senescing, providing an interesting evolutionary explanation for negligible senescence in a secondary sexual trait, and consequently, the existence of asynchrony in senescence among traits within populations.

Fluctuating optimum and temporally variable selection on breeding date in birds and mammals.

Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.

Genomic analysis reveals a polygenic architecture of antler morphology in wild red deer (Cervus elaphus).

Sexually selected traits show large variation and rapid evolution across the animal kingdom, yet genetic variation often persists within populations despite apparent directional selection. A key step in solving this long-standing paradox is to determine the genetic architecture of sexually selected traits to understand evolutionary drivers and constraints at the genomic level. Antlers are a form of sexual weaponry in male red deer (Cervus elaphus). On the island of Rum, Scotland, males with larger antlers have increased breeding success, yet there has been no evidence of any response to selection at the genetic level. To try and understand the mechanisms underlying this observation, we investigate the genetic architecture of ten antler traits and their principal components using genomic data from >38,000 SNPs. We estimate the heritabilities and genetic correlations of the antler traits using a genomic relatedness approach. We then use genome-wide association and haplotype-based regional heritability to identify regions of the genome underlying antler morphology, and an empirical Bayes approach to estimate the underlying distributions of allele effect sizes. We show that antler morphology is highly repeatable over an individual's lifetime, heritable and has a polygenic architecture and that almost all antler traits are positively genetically correlated with some loci identified as having pleiotropic effects. Our findings suggest that a large mutational target and genetic covariances among antler traits, in part maintained by pleiotropy, are likely to contribute to the maintenance of genetic variation in antler morphology in this population.

Susceptibility to a sexually transmitted disease in a wild koala population shows heritable genetic variance but no inbreeding depression.

The koala, one of the most iconic Australian wildlife species, is facing several concomitant threats that are driving population declines. Some threats are well known and have clear methods of prevention (e.g., habitat loss can be reduced with stronger land-clearing control), whereas others are less easily addressed. One of the major current threats to koalas is chlamydial disease, which can have major impacts on individual survival and reproduction rates and can translate into population declines. Effective management strategies for the disease in the wild are currently lacking, and, to date, we know little about the determinants of individual susceptibility to disease. Here, we investigated the genetic basis of variation in susceptibility to chlamydia using one of the most intensively studied wild koala populations. We combined data from veterinary examinations, chlamydia testing, genetic sampling and movement monitoring. Out of our sample of 342 wild koalas, 60 were found to have chlamydia. Using genotype information on 5007 SNPs to investigate the role of genetic variation in determining disease status, we found no evidence of inbreeding depression, but a heritability of 0.11 (95% CI: 0.06-0.23) for the probability that koalas had chlamydia. Heritability of susceptibility to chlamydia could be relevant for future disease management, as it suggests adaptive potential for the population.

The role of selection and evolution in changing parturition date in a red deer population.

Changing environmental conditions cause changes in the distributions of phenotypic traits in natural populations. However, determining the mechanisms responsible for these changes-and, in particular, the relative contributions of phenotypic plasticity versus evolutionary responses-is difficult. To our knowledge, no study has yet reported evidence that evolutionary change underlies the most widely reported phenotypic response to climate change: the advancement of breeding times. In a wild population of red deer, average parturition date has advanced by nearly 2 weeks in 4 decades. Here, we quantify the contribution of plastic, demographic, and genetic components to this change. In particular, we quantify the role of direct phenotypic plasticity in response to increasing temperatures and the role of changes in the population structure. Importantly, we show that adaptive evolution likely played a role in the shift towards earlier parturition dates. The observed rate of evolution was consistent with a response to selection and was less likely to be due to genetic drift. Our study provides a rare example of observed rates of genetic change being consistent with theoretical predictions, although the consistency would not have been detected with a solely phenotypic analysis. It also provides, to our knowledge, the first evidence of both evolution and phenotypic plasticity contributing to advances in phenology in a changing climate.

Phenological sensitivity to climate across taxa and trophic levels.

Differences in phenological responses to climate change among species can desynchronise ecological interactions and thereby threaten ecosystem function. To assess these threats, we must quantify the relative impact of climate change on species at different trophic levels. Here, we apply a Climate Sensitivity Profile approach to 10,003 terrestrial and aquatic phenological data sets, spatially matched to temperature and precipitation data, to quantify variation in climate sensitivity. The direction, magnitude and timing of climate sensitivity varied markedly among organisms within taxonomic and trophic groups. Despite this variability, we detected systematic variation in the direction and magnitude of phenological climate sensitivity. Secondary consumers showed consistently lower climate sensitivity than other groups. We used mid-century climate change projections to estimate that the timing of phenological events could change more for primary consumers than for species in other trophic levels (6.2 versus 2.5-2.9 days earlier on average), with substantial taxonomic variation (1.1-14.8 days earlier on average).

Aging and Senescence across Reproductive Traits and Survival in Superb Fairy-Wrens (Malurus cyaneus).

AbstractWhy do senescence rates of fitness-related traits often vary dramatically? By considering the full aging trajectories of multiple traits, we can better understand how a species' life history shapes the evolution of senescence within a population. Here, we examined age-related changes in sex-specific survival, reproduction, and several components of reproduction using a long-term study of a cooperatively breeding songbird, the superb fairy-wren (Malurus cyaneus). We compared aging patterns between traits by estimating standardized rates of maturation, age of onset of senescence, and rates of senescence while controlling for confounding factors reflecting individual variability in life history. We found striking differences in aging and senescence patterns between survival and reproduction as well as between reproductive traits. In both sexes, survival started to decline from maturity onward. In contrast, all reproductive traits showed improvements into early adulthood, and many showed little or no evidence of senescence. In females, despite senescence in clutch size, number of offspring surviving to independence did not decline in late life, possibly due to improvements in maternal care with age. Superb fairy-wrens have exceptionally high levels of extragroup paternity, and while male within-group reproductive success did not change with age, extragroup reproductive success showed a dramatic increase in early ages, followed by a senescent decline, suggesting that male reproductive aging is driven by sexual selection. We discuss how the superb fairy-wrens' complex life history may contribute to the disparate aging patterns across different traits.

Sex and morph differences in age-dependent trait changes in a polymorphic songbird.

There is growing evidence of important variation in how animals age, in particular in how the expression of traits changes with age among different species and populations. However, less is known about variation within populations, which may include variation in ageing patterns between different types of individuals (e.g. sexes or distinct polymorphisms) and between different types of traits (e.g. general traits versus those used in social signalling contexts). We used 6 years of longitudinal data to examine age-related changes in trait expression in a captive population of Gouldian finches (Erythrura gouldiae), a socially monogamous songbird with genetically determined colour morphs that differ in behaviour and physiology. We contrasted ageing patterns of different types of traits (social signalling vs. size-related) in both sexes and in two colour morphs, using a mixed model approach to account for both within- and between-individual effects. We found pronounced sex differences in how social signalling traits change with age, showing a quadratic pattern in males, but not changing with age in females. In contrast, we observed no sex-specific ageing patterns in size traits. We also found subtle morph differences in how size-related traits changed with age, with black morphs stable or increasing with age while red morphs showing a decline with age. Finally, we found an interesting sex by morph interaction in one important social signal (headband width). These results highlight the importance of using within-individual approaches to understand ageing patterns across types of individuals (sex, morph, etc.) and the need for further research on the ageing patterns of traits that may experience different selective pressures.

When to start and when to stop: Effects of climate on breeding in a multi-brooded songbird.

Climate warming has been shown to affect the timing of the onset of breeding of many bird species across the world. However, for multi-brooded species, climate may also affect the timing of the end of the breeding season, and hence also its duration, and these effects may have consequences for fitness. We used 28 years of field data to investigate the links between climate, timing of breeding, and breeding success in a cooperatively breeding passerine, the superb fairy-wren (Malurus cyaneus). This multi-brooded species from southeastern Australia has a long breeding season and high variation in phenology between individuals. By applying a "sliding window" approach, we found that higher minimum temperatures in early spring resulted in an earlier start and a longer duration of breeding, whereas less rainfall and more heatwaves (days > 29°C) in late summer resulted in an earlier end and a shorter duration of breeding. Using a hurdle model analysis, we found that earlier start dates did not predict whether or not females produced any young in a season. However, for successful females who produced at least one young, earlier start dates were associated with higher numbers of young produced in a season. Earlier end dates were associated with a higher probability of producing at least one young, presumably because unsuccessful females kept trying when others had ceased. Despite larger scale trends in climate, climate variables in the windows relevant to this species' phenology did not change across years, and there were no temporal trends in phenology during our study period. Our results illustrate a scenario in which higher temperatures advanced both start and end dates of individuals' breeding seasons, but did not generate an overall temporal shift in breeding times. They also suggest that the complexity of selection pressures on breeding phenology in multi-brooded species may have been underestimated.

Do the ages of parents or helpers affect offspring fitness in a cooperatively breeding bird?

Age-related changes in parental phenotypes or genotypes can impact offspring fitness, but separating germline from nongermline transgenerational effects of ageing is difficult for wild populations. Further, in cooperatively breeding species, in addition to parental ages, the age of 'helpers' attending offspring may also affect juvenile performance. Using a 30-year study of a cooperative breeder with very high rates of extra-pair paternity, the superb fairy-wren (Malurus cyaneus), we investigated the effects of maternal, paternal and helper ages on three measures of offspring performance: nestling weight, juvenile survival to independence and recruitment to the breeding population. Mothers with a longer lifespan had offspring with higher juvenile survival, indicating selective disappearance, but the effect of maternal age on juvenile survival was of similar magnitude but negative. For extra-pair offspring, there was no evidence of any effect of the ages of either the genetic sire or the cuckolded 'social' father. However, for within-pair offspring, there was a positive effect of paternal age on juvenile survival, which we suggest may be driven by sexual selection. There were positive associations between the average age of helpers attending a nest and two of the three aspects of offspring performance; these effects were stronger than any of the effects of parental age. In general, the multiple associations between offspring fitness and the ages of adults around them appeared to be driven more by age-related changes in environmental effects than by age-related changes in the germline.

A new explanation for unexpected evolution in body size.

Bigger is apparently frequently fitter, and body size is typically heritable, so why don't animals in wild populations evolve towards larger sizes? Different explanations have been proposed for this apparent "paradox of stasis." A new study of snow voles in the Swiss Alps finds higher survival in animals with larger body mass and heritability of body mass, but, surprisingly, a genetic decline in body mass is also indicated. The authors suggest a novel explanation for this observation: the appearance of positive phenotypic selection is driven by a confounding variable of the age at which a juvenile is measured, whereas the evolutionarily relevant selection actually acts negatively on mass via its association with development time. Thus, genes for larger mass are not actually "fitter" because they are associated with longer development times, and juvenile snow voles with longer development times run the risk of not completing development before the first winter snow. However, the genetic decline in body size is not apparent at the phenotypic level, presumably because of countervailing trends in environmental effects on the phenotype.

No evidence that warmer temperatures are associated with selection for smaller body sizes.

Reductions in animal body size over recent decades are often interpreted as an adaptive evolutionary response to climate warming. However, for reductions in size to reflect adaptive evolution, directional selection on body size within populations must have become negative, or where already negative, to have become more so, as temperatures increased. To test this hypothesis, we performed traditional and phylogenetic meta-analyses of the association between annual estimates of directional selection on body size from wild populations and annual mean temperatures from 39 longitudinal studies. We found no evidence that warmer environments were associated with selection for smaller size. Instead, selection consistently favoured larger individuals, and was invariant to temperature. These patterns were similar in ectotherms and endotherms. An analysis using year rather than temperature revealed similar patterns, suggesting no evidence that selection has changed over time, and also indicating that the lack of association with annual temperature was not an artefact of choosing an erroneous time window for aggregating the temperature data. Although phenotypic trends in size will be driven by a combination of genetic and environmental factors, our results suggest little evidence for a necessary ingredient-negative directional selection-for declines in body size to be considered an adaptive evolutionary response to changing selection pressures.

How to analyse plant phenotypic plasticity in response to a changing climate.

Contents Summary 1235 I. Introduction 1235 II. The many shapes of phenotypic plasticity 1236 III. Random regression mixed model framework 1237 IV. Conclusions 1240 Acknowledgements 1240 References 1240 SUMMARY: Plant biology is experiencing a renewed interest in the mechanistic underpinnings and evolution of phenotypic plasticity that calls for a re-evaluation of how we analyse phenotypic responses to a rapidly changing climate. We suggest that dissecting plant plasticity in response to increasing temperature needs an approach that can represent plasticity over multiple environments, and considers both population-level responses and the variation between genotypes in their response. Here, we outline how a random regression mixed model framework can be applied to plastic traits that show linear or nonlinear responses to temperature. Random regressions provide a powerful and efficient means of characterising plasticity and its variation. Although they have been used widely in other fields, they have only recently been implemented in plant evolutionary ecology. We outline their structure and provide an example tutorial of their implementation.

Consistent within-individual plasticity is sufficient to explain temperature responses in red deer reproductive traits.

Warming global temperatures are affecting a range of aspects of wild populations, but the exact mechanisms driving associations between temperature and phenotypic traits may be difficult to identify. Here, we use a 36-year data set on a wild population of red deer to investigate the causes of associations between temperature and two important components of female reproduction: timing of breeding and offspring size. By separating within- versus between-individual associations with temperature for each trait, we show that within-individual phenotypic plasticity (changes within a female's lifetime) was entirely sufficient to generate the observed population-level association with temperature at key times of year. However, despite apparently adequate statistical power, we found no evidence of any variation between females in their responses (i.e. no "IxE" interactions). Our results suggest that female deer show plasticity in reproductive traits in response to temperatures in the year leading up to calving and that this response is consistent across individuals, implying no potential for either selection or heritability of plasticity. We estimate that the plastic response to rising temperatures explained 24% of the observed advance in mean calving date over the study period. We highlight the need for comparable analyses of other systems to determine the contribution of within-individual plasticity to population-level responses to climate change.

Estimation of Genetic Variance in Fitness, and Inference of Adaptation, When Fitness Follows a Log-Normal Distribution.

Additive genetic variance in relative fitness (σA2(w)) is arguably the most important evolutionary parameter in a population because, by Fisher's fundamental theorem of natural selection (FTNS; Fisher RA. 1930. The genetical theory of natural selection. 1st ed. Oxford: Clarendon Press), it represents the rate of adaptive evolution. However, to date, there are few estimates of σA2(w) in natural populations. Moreover, most of the available estimates rely on Gaussian assumptions inappropriate for fitness data, with unclear consequences. "Generalized linear animal models" (GLAMs) tend to be more appropriate for fitness data, but they estimate parameters on a transformed ("latent") scale that is not directly interpretable for inferences on the data scale. Here we exploit the latest theoretical developments to clarify how best to estimate quantitative genetic parameters for fitness. Specifically, we use computer simulations to confirm a recently developed analog of the FTNS in the case when expected fitness follows a log-normal distribution. In this situation, the additive genetic variance in absolute fitness on the latent log-scale (σA2(l)) equals (σA2(w)) on the data scale, which is the rate of adaptation within a generation. However, due to inheritance distortion, the change in mean relative fitness between generations exceeds σA2(l) and equals (exp⁡(σA2(l))-1). We illustrate why the heritability of fitness is generally low and is not a good measure of the rate of adaptation. Finally, we explore how well the relevant parameters can be estimated by animal models, comparing Gaussian models with Poisson GLAMs. Our results illustrate 1) the correspondence between quantitative genetics and population dynamics encapsulated in the FTNS and its log-normal-analog and 2) the appropriate interpretation of GLAM parameter estimates.

Inbreeding depression across the lifespan in a wild mammal population.

Inbreeding depression is of major concern for the conservation of threatened species, and inbreeding avoidance is thought to be a key driver in the evolution of mating systems. However, the estimation of individual inbreeding coefficients in natural populations has been challenging, and, consequently, the full effect of inbreeding on fitness remains unclear. Genomic inbreeding coefficients may resolve the long-standing paucity of data on inbreeding depression in adult traits and total fitness. Here we investigate inbreeding depression in a range of life history traits and fitness in a wild population of red deer (Cervus elaphus) in Scotland using individual inbreeding coefficients derived from dense Single-Nucleotide Polymorphism (SNP) data (Fgrm). We find associations between[Formula: see text]and annual breeding success in both sexes, and between maternal inbreeding coefficient and offspring survival. We also confirm previous findings of inbreeding depression in birth weight and juvenile survival. In contrast, inbreeding coefficients calculated from a deep and comparatively complete pedigree detected inbreeding depression in juvenile survival, but not in any adult fitness component. The total effect of inbreeding on lifetime breeding success (LBS) was substantial in both sexes: for Fgrm = 0.125, a value resulting from a half-sib mating, LBS declined by 72% for females and 95% for males. Our results demonstrate that SNP-based estimates of inbreeding provide a powerful tool for evaluating inbreeding depression in natural populations, and suggest that, to date, the prevalence of inbreeding depression in adult traits may have been underestimated.

Microbes follow Humboldt: temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes.

More than 200 years ago, Alexander von Humboldt reported that tropical plant species richness decreased with increasing elevation and decreasing temperature. Surprisingly, coordinated patterns in plant, bacterial, and fungal diversity on tropical mountains have not yet been observed, despite the central role of soil microorganisms in terrestrial biogeochemistry and ecology. We studied an Andean transect traversing 3.5 km in elevation to test whether the species diversity and composition of tropical forest plants, soil bacteria, and fungi follow similar biogeographical patterns with shared environmental drivers. We found coordinated changes with elevation in all three groups: species richness declined as elevation increased, and the compositional dissimilarity among communities increased with increased separation in elevation, although changes in plant diversity were larger than in bacteria and fungi. Temperature was the dominant driver of these diversity gradients, with weak influences of edaphic properties, including soil pH. The gradients in microbial diversity were strongly correlated with the activities of enzymes involved in organic matter cycling, and were accompanied by a transition in microbial traits towards slower-growing, oligotrophic taxa at higher elevations. We provide the first evidence of coordinated temperature-driven patterns in the diversity and distribution of three major biotic groups in tropical ecosystems: soil bacteria, fungi, and plants. These findings suggest that interrelated and fundamental patterns of plant and microbial communities with shared environmental drivers occur across landscape scales. These patterns are revealed where soil pH is relatively constant, and have implications for tropical forest communities under future climate change.