Spatial variation in avian bill size is associated with temperature extremes in a major radiation of Australian passerines.

Morphology is integral to body temperature regulation. Recent advances in understanding of thermal physiology suggest a role of the avian bill in thermoregulation. To explore the adaptive significance of bill size for thermoregulation we characterized relationships between bill size and climate extremes. Most previous studies focused on climate means, ignoring frequencies of extremes, and do not reflect thermoregulatory costs experienced over shorter time scales. Using 79 species (9847 museum specimens), we explore how bill size variation is associated with temperature extremes in a large and diverse radiation of Australasian birds, Meliphagides, testing a series of predictions. Overall, across the continent, bill size variation was associated with both climate extremes and means and was most strongly associated with winter temperatures; associations at the level of climate zones differed from continent-wide associations and were complex, yet consistent with physiology and a thermoregulatory role for avian bills. Responses to high summer temperatures were nonlinear suggesting they may be difficult to detect in large-scale continental analyses using previous methodologies. We provide strong evidence that climate extremes have contributed to the evolution of bill morphology in relation to thermoregulation and show the importance of including extremes to understand fine-scale trait variation across space.

How interacting anthropogenic pressures alter the plasticity of breeding time in two common songbirds.

Phenological adjustment is the first line of adaptive response of vertebrates when seasonality is disrupted by climate change. The prevailing response is to reproduce earlier in warmer springs, but habitat changes, such as forest degradation, are expected to affect phenological plasticity, for example, due to loss of reliability of environmental cues used by organisms to time reproduction. Relying on a two-decade, country-level capture-based monitoring of common songbirds' reproduction, we investigated how habitat anthropization, here characterized by the rural-urban and forest-farmland gradients, affected the average phenology and plasticity to local temperature in two common species, the great tit Parus major and the blue tit Cyanistes caeruleus. We built a hierarchical model that simultaneously estimated fledging phenology and its response to spring temperatures based on the changes in the proportion of juveniles captured over the breeding season. Both species fledge earlier in warmer sites (blue tit: 2.94 days/°C, great tit: 3.83 days/°C), in warmer springs (blue tit: 2.49 days/°C, great tit: 2.75 days/°C) and in most urbanized habitats (4 days for blue tit and 2 days for great tit). The slope of the reaction norm of fledging phenology to spring temperature varied across sites in both species, but this variation was explained by habitat anthropization only in the deciduous forest specialist, the blue tit. In this species, the responses to spring temperature were shallower in agricultural landscapes and slightly steeper in more urban areas. Habitat anthropization did not explain variation in the slope of the reaction norm in the habitat-generalist species (great tit), for which mean fledgling phenology and plasticity were correlated (i.e., steeper response in later sites). The effects of habitat change on phenological reaction norms provide another way through which combined environmental degradations may threaten populations' persistence, to an extent depending on species and on the changes in their prey phenology and abundance.

Mistletoes could moderate drought impacts on birds, but are themselves susceptible to drought-induced dieback.

Mistletoes are hemiparasitic plants and keystone species in many ecosystems globally. Given predicted increases in drought frequency and intensity, mistletoes may be crucial for moderating drought impacts on community structure. Dependent on host vascular flows, mistletoes can succumb to stress when water availability falls, making them susceptible to mortality during drought. We counted mistletoe across greater than 350 000 km2 of southeastern Australia and conducted standardized bird surveys between 2016 and 2021, spanning a major drought event in 2018-2019. We aimed to identify predictors of mistletoe abundance and mortality and determine whether mistletoes might moderate drought impacts on woodland birds. Live mistletoe abundance varied with tree species composition, land use and presence of mistletoebirds. Mistletoe mortality was widespread, consistent with high 2018/2019 summer temperatures, low 2019/2020 summer rainfall and the interaction between summer temperatures and rainfall in 2019/2020. The positive association between surviving mistletoes and woodland birds was greatest in the peak drought breeding seasons of 2018/2019 and 2019/2020, particularly for small residents and insectivores. Paradoxically, mistletoes could moderate drought impacts on birds, but are themselves vulnerable to drought-induced mortality. An improved understanding of the drivers and dynamics of mistletoe mortality is needed to address potential cascading trophic impacts associated with mistletoe die-off.

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.

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.

Limited mass-independent individual variation in resting metabolic rate in a wild population of snow voles (Chionomys nivalis).

Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass-independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long-term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni- and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass-dependent and mass-independent components, while accounting for measurement error. RMR varies among individuals, that is, is repeatable (R = .46) and strongly co-varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass-independent RMR is reduced by 41% to R = .27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error and decompose the relative importance of mass-dependent and mass-independent physiological variation.

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.

Bigger Is Fitter? Quantitative Genetic Decomposition of Selection Reveals an Adaptive Evolutionary Decline of Body Mass in a Wild Rodent Population.

In natural populations, quantitative trait dynamics often do not appear to follow evolutionary predictions. Despite abundant examples of natural selection acting on heritable traits, conclusive evidence for contemporary adaptive evolution remains rare for wild vertebrate populations, and phenotypic stasis seems to be the norm. This so-called "stasis paradox" highlights our inability to predict evolutionary change, which is especially concerning within the context of rapid anthropogenic environmental change. While the causes underlying the stasis paradox are hotly debated, comprehensive attempts aiming at a resolution are lacking. Here, we apply a quantitative genetic framework to individual-based long-term data for a wild rodent population and show that despite a positive association between body mass and fitness, there has been a genetic change towards lower body mass. The latter represents an adaptive response to viability selection favouring juveniles growing up to become relatively small adults, i.e., with a low potential adult mass, which presumably complete their development earlier. This selection is particularly strong towards the end of the snow-free season, and it has intensified in recent years, coinciding which a change in snowfall patterns. Importantly, neither the negative evolutionary change, nor the selective pressures that drive it, are apparent on the phenotypic level, where they are masked by phenotypic plasticity and a non causal (i.e., non genetic) positive association between body mass and fitness, respectively. Estimating selection at the genetic level enabled us to uncover adaptive evolution in action and to identify the corresponding phenotypic selective pressure. We thereby demonstrate that natural populations can show a rapid and adaptive evolutionary response to a novel selective pressure, and that explicitly (quantitative) genetic models are able to provide us with an understanding of the causes and consequences of selection that is superior to purely phenotypic estimates of selection and evolutionary change.

Analogues of the fundamental and secondary theorems of selection, assuming a log-normal distribution of expected fitness.

It is increasingly common for studies of evolution in natural populations to infer the quantitative genetic basis of fitness (e.g., the additive genetic variance for relative fitness), and of relationships between traits and fitness (e.g., the additive genetic covariance of traits with relative fitness). There is a certain amount of tension between the theory that justifies estimating these quantities, and methodological considerations relevant to their empirical estimation. In particular, the additive genetic variances and covariances involving relative fitness are justified by the fundamental and secondary theorems of selection, which pertain to relative fitness on the scale that it is expressed. However, naturally-occurring fitness distributions lend themselves to analysis with generalized linear mixed models (GLMMs), which conduct analysis on a different scale, typically on the scale of the logarithm of expected values, from which fitness is expressed. This note presents relations between evolutionary change in traits, and the rate of adaptation in fitness, and log quantitative genetic parameters of fitness, potentially reducing the discord between theoretical and methodological considerations to the operationalization of the secondary and fundamental theorems of selection.

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.