The correlation between coloration and exploration behaviour varies across hierarchical levels in a wild passerine bird

In vertebrates, darker individuals are often found to be more active and willing to take risks (representing characteristics of a ‘proactive’ coping style), whereas lighter individuals are instead more cautious and less active (representing characteristics of a ‘reactive’ coping style). It is thus generally expected that melanin‐based coloration and proactivity form a suite of positively integrated traits at the among‐individual level. Here, we use a multigenerational pedigree of free‐living great tits (Parus major) to partition variation in, and the correlation between, melanin‐based breast stripe (‘tie’) size and exploration behaviour (a proxy for coping style) into its among‐ and within‐individual components. We show that both traits harbour heritable variation. Against predictions, tie size and speed of exploration were negatively correlated at the among‐individual level due to the combined influences of permanent environmental and additive genetic effects. By contrast, the two traits were weakly positively correlated within individuals (i.e. individuals increasing in tie size after moult tended to become more explorative). The patterns of among‐individual covariance were not caused by correlational selection as we found additive and opposite selection pressures acting on the two traits. These findings imply that testing hypotheses regarding the existence of a ‘syndrome’ at the among‐individual level strictly requires variance partitioning to avoid inappropriate interpretations as the negative ‘unpartitioned’ phenotypic correlation between exploration and tie size resulted from counteracting effects of within‐ and among‐individual correlations. Identifying sources and levels of (co)variation in phenotypic traits is thus critical to our understanding of biological patterns and evolutionary processes.     

Exploring patterns of variation in clutch size–density reaction norms in a wild passerine bird

Negative density dependence of clutch size is a ubiquitous characteristic of avian populations and is partly due to within‐individual phenotypic plasticity. Yet, very little is known about the extent to which individuals differ in their degree of phenotypic plasticity, whether such variation has a genetic basis and whether level of plasticity can thus evolve in response to selection. Using 18 years of data of a Dutch great tit population (Parus major), we show that females reduced clutch size with increasing population density (slopes of the reaction norms), differed strongly in their average clutch size (elevations of the reaction norms) at the population‐mean density and that the latter variation was partly heritable. In contrast, we could not detect individual variation in phenotypic plasticity (‘I × E’). Level of plasticity is thus not likely to evolve in response to selection in this population. Observed clutch sizes deviated more from the estimated individual reaction norms in certain years and densities, implying that the within‐individual between‐year variance (so‐called residual variance) of clutch size was heterogeneous with respect to these factors. Given the observational nature of this study, experimental manipulation of density is now warranted to confirm the causality of the observed density effects. Our analyses demonstrate that failure to acknowledge this heterogeneity would have inflated the estimate of ‘I × E’ and led to misinterpretation of the data. This paper thereby emphasizes the fact that heterogeneity in residuals can provide biologically insightful information about the ecological processes underlying the data.     

Temperature has a causal effect on avian timing of reproduction

Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. We tested the direct effect of temperature on laying dates in great tits (Parus major) using climatized aviaries in a 6-year experiment. We mimicked the temperature patterns from two specific years in which our wild population laid either early (‘warm’ treatment) or late (‘cold’ treatment). Laying dates were affected by temperature directly. As the relevant temperature period started three weeks prior to the mean laying date, with a range of just 4°C between the warm and the cold treatments, and as the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. We furthermore show a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. Our results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.     

Density fluctuations represent a key process maintaining personality variation in a wild passerine bird

Heritable personality variation is subject to fluctuating selection in many animal taxa; a major unresolved question is why this is the case. A parsimonious explanation must involve a general ecological process: a likely candidate is the omnipresent spatiotemporal variation in conspecific density. We tested whether spatiotemporal variation in density within and among nest box plots of great tits (Parus major) predicted variation in selection acting on exploratory behaviour (n = 48 episodes of selection). We found viability selection favouring faster explorers under lower densities but slower explorers under higher densities. Temporal variation in local density represented the primary factor explaining personality‐related variation in viability selection. Importantly, birds did not anticipate changes in selection by means of adaptive density‐dependent plasticity. This study thereby provides an unprecedented example of the key importance of the interplay between fluctuating selection and lack of adaptive behavioural plasticity in maintaining animal personality variation in the wild.     

Female variation in allocation of steroid hormones,antioxidants and fatty acids: a multilevel analysis in a wild passerine bird

The environment where an embryo develops can be influenced by components of maternal origin, which can shape offspring phenotypes and therefore maternal fitness. In birds that produce more than one egg per clutch, females differ in the concentration of components they allocate into the yolk along the laying sequence. However, identification of processes that shape female yolk allocation and thus offspring phenotype still remains a major challenge within evolutionary ecology. A way to increase our understanding is by acknowledging that allocation patterns can differ depending on the level of analysis, such as the population versus the among‐female (within‐population) level. We employed mixed models to analyze at both levels the variation in allocation along the laying sequence of four steroid hormones, three antioxidants, and four groups of fatty acids present in the egg yolks of wild great tits Parus major. We also quantified repeatabilities for each component to study female consistency. At a population level, the concentrations/proportions of five yolk components varied along the laying sequence, implying that the developmental environment is different for offspring developing in first versus last eggs. Females varied substantially in the mean allocation of components and in their plasticity along the laying sequence. For most components, these two parameters were negatively correlated. Females were also remarkably repeatable in their allocation. Overall, our data emphasize the need to account for female variation in yolk allocation along the laying sequence at multiple levels, as variation at a population level is underpinned by different individual patterns. Our findings also highlight the importance of considering both levels of analysis in future studies investigating the causes and fitness consequences of yolk compounds. Finally, our results on female repeatability confirm that analyzing one egg per nest is a suitable way to address the consequences of yolk resource deposition for the offspring.     

Heritability estimates from genomewide relatedness matrices in wild populations: Application to a passerine,using a small sample size

Genomic developments have empowered the investigation of heritability in wild populations directly from genomewide relatedness matrices (GRM). Such GRM‐based approaches can in particular be used to improve or substitute approaches based on social pedigree (PED‐social). However, measuring heritability from GRM in the wild has not been widely applied yet, especially using small samples and in nonmodel species. Here, we estimated heritability for four quantitative traits (tarsus length, wing length, bill length and body mass), using PED‐social, a pedigree corrected by genetic data (PED‐corrected) and a GRM from a small sample (n = 494) of blue tits from natural populations in Corsica genotyped at nearly 50,000 filtered SNPs derived from RAD‐seq. We also measured genetic correlations among traits, and we performed chromosome partitioning. Heritability estimates were slightly higher when using GRM compared to PED‐social, and PED‐corrected yielded intermediate values, suggesting a minor underestimation of heritability in PED‐social due to incorrect pedigree links, including extra‐pair paternity, and to lower information content than the GRM. Genetic correlations among traits were similar between PED‐social and GRM but credible intervals were very large in both cases, suggesting a lack of power for this small data set. Although a positive linear relationship was found between the number of genes per chromosome and the chromosome heritability for tarsus length, chromosome partitioning similarly showed a lack of power for the three other traits. We discuss the usefulness and limitations of the quantitative genetic inferences based on genomic data in small samples from wild populations.     

Incubation behavior adjustments,driven by ambient temperature variation,improve synchrony between hatch dates and caterpillar peak in a wild bird population

For organisms living in seasonal environments, synchronizing the peak energetic demands of reproduction with peak food availability is a key challenge. Understanding the extent to which animals can adjust behavior to optimize reproductive timing, and the cues they use to do this, is essential for predicting how they will respond to future climate change. In birds, the timing of peak energetic demand is largely determined by the timing of clutch initiation; however, considerable alterations can still occur once egg laying has begun. Here, we use a wild population of great tits (Parus major) to quantify individual variation in different aspects of incubation behavior (onset, duration, and daily intensity) and conduct a comprehensive assessment of the causes and consequences of this variation. Using a 54‐year dataset, we demonstrate that timing of hatching relative to peak prey abundance (synchrony) is a better predictor of reproductive success than clutch initiation or clutch completion timing, suggesting adjustments to reproductive timing via incubation are adaptive in this species. Using detailed in‐nest temperature recordings, we found that postlaying, birds improved their synchrony with the food peak primarily by varying the onset of incubation, with duration changes playing a lesser role. We then used a sliding time window approach to explore which spring temperature cues best predict variance in each aspect of incubation behavior. Variation in the onset of incubation correlated with mean temperatures just prior to laying; however, incubation duration could not be explained by any of our temperature variables. Daily incubation intensity varied in response to daily maximum temperatures throughout incubation, suggesting female great tits respond to temperature cues even in late stages of incubation. Our results suggest that multiple aspects of the breeding cycle influence the final timing of peak energetic demand. Such adjustments could compensate, in part, for poor initial timing, which has significant fitness impacts.     

Chemical regulation of body feather microbiota in a wild bird

The microbiota has a broad range of impacts on host physiology and behaviour, pointing out the need to improve our comprehension of the drivers of host–microbiota composition. Of particular interest is whether the microbiota is acquired passively, or whether and to what extent hosts themselves shape the acquisition and maintenance of their microbiota. In birds, the uropygial gland produces oily secretions used to coat feathers that have been suggested to act as an antimicrobial defence mechanism regulating body feather microbiota. However, our comprehension of this process is still limited. In this study, we for the first time coupled high‐throughput sequencing of the microbiota of both body feathers and the direct environment (i.e., the nest) in great tits with chemical analyses of the composition of uropygial gland secretions to examine whether host chemicals have either specific effects on some bacteria or nonspecific broad‐spectrum effects on the body feather microbiota. Using a network approach investigating the patterns of co‐occurrence or co‐exclusions between chemicals and bacteria within the body feather microbiota, we found no evidence for specific promicrobial or antimicrobial effects of uropygial gland chemicals. However, we found that one group of chemicals was negatively correlated to bacterial richness on body feathers, and a higher production of these chemicals was associated with a poorer body feather bacterial richness compared to the nest microbiota. Our study provides evidence that chemicals produced by the host might function as a nonspecific broad‐spectrum antimicrobial defence mechanism limiting colonization and/or maintenance of bacteria on body feathers, providing new insight about the drivers of the host's microbiota composition in wild organisms.     

Social and spatial effects on genetic variation between foraging flocks in a wild bird population

Social interactions are rarely random. In some instances, animals exhibit homophily or heterophily, the tendency to interact with similar or dissimilar conspecifics, respectively. Genetic homophily and heterophily influence the evolutionary dynamics of populations, because they potentially affect sexual and social selection. Here, we investigate the link between social interactions and allele frequencies in foraging flocks of great tits (Parus major) over three consecutive years. We constructed co‐occurrence networks which explicitly described the splitting and merging of 85,602 flocks through time (fission–fusion dynamics), at 60 feeding sites. Of the 1,711 birds in those flocks, we genotyped 962 individuals at 4,701 autosomal single nucleotide polymorphisms (SNPs). By combining genomewide genotyping with repeated field observations of the same individuals, we were able to investigate links between social structure and allele frequencies at a much finer scale than was previously possible. We explicitly accounted for potential spatial effects underlying genetic structure at the population level. We modelled social structure and spatial configuration of great tit fission–fusion dynamics with eigenvector maps. Variance partitioning revealed that allele frequencies were strongly affected by group fidelity (explaining 27%–45% of variance) as individuals tended to maintain associations with the same conspecifics. These conspecifics were genetically more dissimilar than expected, shown by genomewide heterophily for pure social (i.e., space‐independent) grouping preferences. Genomewide homophily was linked to spatial configuration, indicating spatial segregation of genotypes. We did not find evidence for homophily or heterophily for putative socially relevant candidate genes or any other SNP markers. Together, these results demonstrate the importance of distinguishing social and spatial processes in determining population structure.     

Evidence for lower plasticity in CTMAX at warmer developmental temperatures

Understanding the capacity for different species to reduce their susceptibility to climate change via phenotypic plasticity is essential for accurately predicting species extinction risk. The climatic variability hypothesis suggests that spatial and temporal variation in climatic variables should select for more plastic phenotypes. However, empirical support for this hypothesis is limited. Here, we examine the capacity for ten Drosophila species to increase their critical thermal maxima (CT_MAX) through developmental acclimation and/or adult heat hardening. Using four fluctuating developmental temperature regimes, ranging from 13 to 33 °C, we find that most species can increase their CT_MAX via developmental acclimation and adult hardening, but found no relationship between climatic variables and absolute measures of plasticity. However, when plasticity was dissected across developmental temperatures, a positive association between plasticity and one measure of climatic variability (temperature seasonality) was found when development took place between 26 and 28 °C, whereas a negative relationship was found when development took place between 20 and 23 °C. In addition, a decline in CT_MAX and egg‐to‐adult viability, a proxy for fitness, was observed in tropical species at the warmer developmental temperatures (26–28 °C); this suggests that tropical species may be at even greater risk from climate change than currently predicted. The combined effects of developmental acclimation and adult hardening on CT_MAX were small, contributing to a <0.60 °C shift in CT_MAX. Although small shifts in CT_MAX may increase population persistence in the shorter term, the degree to which they can contribute to meaningful responses in the long term is unclear.     

Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird

Oxidative stress was recently demonstrated to affect several fitness‐related traits and is now well recognized to shape animal life‐history evolution. However, very little is known about how much resistance to oxidative stress is determined by genetic and environmental effects and hence about its potential for evolution, especially in wild populations. In addition, our knowledge of phenotypic sexual dimorphism and cross‐sex genetic correlations in resistance to oxidative stress remains extremely limited despite important evolutionary implications. In free‐living great tits (Parus major), we quantified heritability, common environmental effect, sexual dimorphism and cross‐sex genetic correlation in offspring resistance to oxidative stress by performing a split‐nest cross‐fostering experiment where 155 broods were split, and all siblings (n = 791) translocated and raised in two other nests. Resistance to oxidative stress was measured as both oxidative damage to lipids and erythrocyte resistance to a controlled free‐radical attack. Both measurements of oxidative stress showed low additive genetic variances, high common environmental effects and phenotypic sexual dimorphism with males showing a higher resistance to oxidative stress. Cross‐sex genetic correlations were not different from unity, and we found no substantial heritability in resistance to oxidative stress at adult age measured on 39 individuals that recruited the subsequent year. Our study shows that individual ability to resist to oxidative stress is primarily influenced by the common environment and has a low heritability with a consequent low potential for evolution, at least at an early stage of life.     

Climate drives among‐year variation in natural selection on flowering time

To predict long‐term responses to climate change, we need to understand how changes in temperature and precipitation elicit both immediate phenotypic responses and changes in natural selection. We used 22 years of data for the perennial herb Lathyrus vernus to examine how climate influences flowering phenology and phenotypic selection on phenology. Plants flowered earlier in springs with higher temperatures and higher precipitation. Early flowering was associated with a higher fitness in nearly all years, but selection for early flowering was significantly stronger in springs with higher temperatures and lower precipitation. Climate influenced selection through trait distributions, mean fitness and trait?fitness relationships, the latter accounting for most of the among‐year variation in selection. Our results show that climate both induces phenotypic responses and alters natural selection, and that the change in the optimal phenotype might be either weaker, as for spring temperature, or stronger, as for precipitation, than the optimal response.     

Selection on incremental variation of eye size in a wild population of Daphnia

Several studies of eye morphology have analysed macroevolutionary patterns in the diversity of eyes, and although these studies are often linked to environment or behaviour, they provide only indirect evidence of selection. Specific data to show the microevolutionary potential for adaptation by natural selection in eye morphology have been lacking. We document directional selection on eye size, an important determinant of visual capabilities, in a wild population of the freshwater microcrustacean Daphnia. We show that even slight changes in eye size may have major consequences for fitness. An increase in eye diameter of 19.9 μm – slightly more than one standard deviation – is associated with an increase in clutch size of one egg, or an increase of nearly 20% of the mean clutch size. Furthermore, relative eye size is genetically variable and thus could evolve in response to the observed selective pressure. We conclude that selection on incremental variation in eye size may have led to differences observed on broader taxonomic scales.     

Obtaining accurate measurements of the size and volume of insects fed to nestlings from video recordings

Video recordings are commonly used to study the types, amount, and size of food items provided to nestling birds. However, the accuracy and repeatability of estimates of the size of food items from video recordings has not been examined. We assessed three aspects of the reliability of measuring prey size from video recordings of Great Tits (Parus major) provisioning nestlings. To test the accuracy of measurements of prey size (length and width) used to determine prey volume, we molded artificial plasticine caterpillars and compared their size and volume as determined using measurements of length and width on screenshots of video recordings (using the vertical diameter of nest‐box entrance holes as a size reference) to their actual size and volume. We also examined within‐ and among‐observer repeatability of measurements of the size and volume of actual prey items delivered to nestlings by adult Great Tits. We found that observers were able to accurately measure prey size and determine volume, with high agreement between the actual size and volume of plasticine caterpillars and the size and volume as determined from measurements made on screenshots from video recordings (r_ICC = 0.99). In addition, within‐ and among‐observer repeatability were also high (r_ICC = 0.98 and 0.93, respectively). Overall, our results suggest that the size of prey items delivered to nestlings by adults in video recordings can be accurately measured and those measurements, in turn, can be used to accurately determine the volume of those insect prey.     

Accounting for interspecific competition and age structure in demographic analyses of density dependence improves predictions of fluctuations in population size

Understanding species coexistence has long been a major goal of ecology. Coexistence theory for two competing species posits that intraspecific density dependence should be stronger than interspecific density dependence. Great tits and blue tits are two bird species that compete for food resources and nesting cavities. On the basis of long‐term monitoring of these two competing species at sites across Europe, combining observational and manipulative approaches, we show that the strength of density regulation is similar for both species, and that individuals have contrasting abilities to compete depending on their age. For great tits, density regulation is driven mainly by intraspecific competition. In contrast, for blue tits, interspecific competition contributes as much as intraspecific competition, consistent with asymmetric competition between the two species. In addition, including age‐specific effects of intra‐ and interspecific competition in density‐dependence models improves predictions of fluctuations in population size by up to three times.     

Annual plants change in size over a century of observations

Studies have documented changes in animal body sizes over the last century, but very little is known about changes in plant sizes, even though reduced plant productivity is potentially responsible for declines in size of other organisms. Here, I ask whether warming trends in the Great Basin have affected plant size by measuring specimens preserved on herbarium sheets collected between 1893 and 2011. I asked how maximum and minimum temperatures, precipitation, and the Pacific Decadal Oscillation (PDO) in the year of collection affected plant height, leaf size, and flower number, and asked whether changes in climate resulted in decreasing sizes for seven annual forbs. Species had contrasting responses to climate factors, and would not necessarily be expected to respond in parallel to climatic shifts. There were generally positive relationships between plant size and increased minimum and maximum temperatures, which would have been predicted to lead to small increases in plant sizes over the observation period. While one species increased in size and flower number over the observation period, five of the seven species decreased in plant height, four of these decreased in leaf size, and one species also decreased in flower production. One species showed no change. The mechanisms behind these size changes are unknown, and the limited data available on these species (germination timing, area of occupancy, relative abundance) did not explain why some species shrank while others grew or did not change in size over time. These results show that multiple annual forbs are decreasing in size, but that even within the same functional group, species may have contrasting responses to similar environmental stimuli. Changes in plant size could have cascading effects on other members of these communities, and differential responses to directional change may change the composition of plant communities over time.