Early-life behavior, survival, and maternal personality in a wild marsupial.

Individual behavior varies for many reasons, but how early in life are such differences apparent, and are they under selection? We investigated variation in early-life behavior in a wild eastern gray kangaroo (Macropus giganteus) population, and quantified associations of behavior with early survival. Behavior of young was measured while still in the pouch and as subadults, and survival to weaning was monitored. We found consistent variation between offspring of different mothers in levels of activity at the pouch stage, in flight initiation distance (FID) as subadults, and in subadult survival, indicating similarity between siblings. There was no evidence of covariance between the measures of behavior at the pouch young versus subadult stages, nor of covariance of the early-life behavioral traits with subadult survival. However, there was a strong covariance between FIDs of mothers and those of their offspring tested at different times. Further, of the total repeatability of subadult FID (51.5%), more than half could be attributed to differences between offspring of different mothers. Our results indicate that 1) behavioral variation is apparent at a very early stage of development (still in the pouch in the case of this marsupial); 2) between-mother differences can explain much of the repeatability (or "personality") of juvenile behavior; and 3) mothers and offspring exhibit similar behavioral responses to stimuli. However, 4) we found no evidence of selection via covariance between early-life or maternal behavioral traits and juvenile survival in this wild marsupial.

Winter mortality of a passerine bird increases following hotter summers and during winters with higher maximum temperatures.

Climate change may influence animal population dynamics through reproduction and mortality. However, attributing changes in mortality to specific climate variables is challenging because the exact time of death is usually unknown in the wild. Here, we investigated climate effects on adult mortality in Australian superb fairy-wrens (Malurus cyaneus). Over a 27-year period, mortality outside the breeding season nearly doubled. This nonbreeding season mortality increased with lower minimum (night-time) and higher maximum (day-time) winter temperatures and with higher summer heat wave intensity. Fine-scale analysis showed that higher mortality in a given week was associated with higher maxima 2 weeks prior and lower minima in the current fortnight, indicating costs of temperature drops. Increases in summer heat waves and in winter maximum temperatures collectively explained 62.6% of the increase in mortality over the study period. Our results suggest that warming climate in both summer and winter can adversely affect survival, with potentially substantial population consequences.

Maternal effects do not resolve the paradox of stasis in birth weight in a wild red deer populaton.

In natural populations, quantitative traits seldom show short-term evolution at the rate predicted by evolutionary models. Resolving this "paradox of stasis" is a key goal in evolutionary biology, as it directly challenges our capacity to predict evolutionary change. One particularly promising hypothesis to explain the lack of evolutionary responses in a key offspring trait, body weight, is that positive selection on juveniles is counterbalanced by selection against maternal investment in offspring growth, given that reproduction is costly for the mothers. Here, we used data from one of the longest individual-based studies of a wild mammal population to test this hypothesis. We first showed that despite positive directional selection on birth weight, and heritable variation for this trait, no genetic change has been observed for birth weight over the past 47 years in the study population. Contrarily to our expectation, we found no evidence of selection against maternal investment in birth weight-if anything, selection favors mothers that produce large calves. Accordingly, we show that genetic change in birth weight over the study period is actually lower than that predicted from models including selection on maternal performance; ultimately our analysis here only deepens rather than resolves the paradox of stasis.

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.

Effects of developmental and adult environments on ageing.

Developmental and adult environments can interact in complex ways to influence the fitness of individuals. Most studies investigating effects of the environment on fitness focus on environments experienced and traits expressed at a single point in an organism's life. However, environments vary with time, so the effects of the environments that organisms experience at different ages may interact to affect how traits change throughout life. Here, we test whether thermal stress experienced during development leads individuals to cope better with thermal stress as adults. We manipulated temperature during both development and adulthood and measured a range of life-history traits, including senescence, in male and female seed beetles (Callosobruchus maculatus). We found that thermal stress during development reduced adult reproductive performance of females. In contrast, life span and age-dependent mortality were affected more by adult than developmental environments, with high adult temperatures decreasing longevity and increasing age-dependent mortality. Aside from an interaction between developmental and adult environments to affect age-dependent changes in male weight, we did not find any evidence of a beneficial acclimation response to developmental thermal stress. Overall, our results show that effects of developmental and adult environments can be both sex and trait specific, and that a full understanding of how environments interact to affect fitness and ageing requires the integrated study of conditions experienced during different stages of ontogeny.

Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.

The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

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.

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.

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.

hiphop: Improved paternity assignment among close relatives using a simple exclusion method for biallelic markers.

Assignment of parentage with molecular markers is most difficult when the true parents have close relatives in the adult population. Here, we present an efficient solution to that problem by extending simple exclusion approaches to parentage analysis with single nucleotide polymorphic markers (SNPs). We augmented the previously published homozygote opposite test (hot), which counts mismatches due to the offspring and candidate parent having different homozygous genotypes, with an additional test. In this case, parents homozygous for the same SNP are incompatible with heterozygous offspring (i.e., "Homozygous Identical Parents, Heterozygous Offspring are Precluded": hiphop). We tested this approach in a cooperatively breeding bird, the superb fairy-wren, Malurus cyaneus, where rates of extra-pair paternity are exceptionally high, and where paternity assignment is challenging because breeding males typically have first-order adult relatives in their neighbourhood. Combining the tests and conditioning on the maternal genotype with a set of 1376 autosomal SNPs always allowed us to distinguish a single most likely sire from his relatives, and also to identify cases where the true sire must have been unsampled. In contrast, if just the hot test was used, we failed to identify a single most-likely sire in 2.5% of cases. Resampling enabled us to create guidelines for the number of SNPs required when first-order relatives coexist in the mating pool. Our method, implemented in the R package hiphop, therefore provides unambiguous parentage assignments even in systems with complex social organisation. We also identified a suite of Z- and W-linked SNPs that always identified sex correctly.

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.

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.

The effects of competition on fitness depend on the sex of both competitors.

In intraspecific competition, the sex of competing individuals is likely to be important in determining the outcome of competitive interactions and the way exposure to conspecifics during development influences adult fitness traits. Previous studies have explored differences between males and females in their response to intraspecific competition. However, few have tested how the sex of the competitors, or any interactions between focal and competitor sex, influences the nature and intensity of competition. We set up larval seed beetles Callosobruchus maculatus to develop either alone or in the presence of a male or female competitor and measured a suite of traits: development time, emergence weight; male ejaculate mass, copulation duration, and lifespan; and female lifetime fecundity, offspring egg-adult survival, and lifespan. We found effects of competition and competitor sex on the development time and emergence weight of both males and females, and also of an interaction between focal and competitor sex: Females emerged lighter when competing with another female, while males did not. There was little effect of larval competition on male and female adult fitness traits, with the exception of the effect of a female competitor on a focal female's offspring survival rate. Our results highlight the importance of directly measuring the effects of competition on fitness traits, rather than distant proxies for fitness, and suggest that competition with the sex with the greater resource requirements (here females) might play a role in driving trait evolution. We also found that male-male competition during development resulted in shorter copulation times than male-female competition, a result that remained when controlling for the weight of competitors. Although it is difficult to definitively tease apart the effects of social environment and access to resources, this result suggests that something about the sex of competitors other than their size is driving this pattern.

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.

The genetic architecture of maternal effects across ontogeny in the red deer.

Maternal effects, either environmental or genetic in origin, are an underappreciated source of phenotypic variance in natural populations. Maternal genetic effects have the potential to constrain or enhance the evolution of offspring traits depending on their magnitude and their genetic correlation with direct genetic effects. We estimated the maternal effect variance and its genetic component for 12 traits expressed over the life history in a pedigreed population of wild red deer (morphology, survival/longevity, breeding success). We only found support for maternal genetic effect variance in the two neonatal morphological traits: birth weight ( hMg2 = 0.31) and birth leg length ( hMg2 = 0.17). For these two traits, the genetic correlation between maternal and direct additive effects was not significantly different from zero, indicating no constraint to evolution from genetic architecture. In contrast, variance in maternal genetic effects enhanced the additive genetic variance available to respond to natural selection. Maternal effect variance was negligible for late-life traits. We found no evidence for sex differences in either the direct or maternal genetic architecture of offspring traits. Our results suggest that maternal genetic effect variance declines over the lifetime, but also that this additional heritable genetic variation may facilitate evolutionary responses of early-life traits.

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.

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.

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.