The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird.

A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude - almost the entire geographical range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugium, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear 'islands of differentiation', even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species' range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics.

Social network centrality predicts dietary decisions in a wild bird population.

How individuals balance costs and benefits of group living remains central to understanding sociality. In relation to diet, social foraging provides many advantages but also increases competition. Nevertheless, social individuals may offset increased competition by broadening their diet and consuming novel foods. Despite the expected relationships between social behavior and dietary decisions, how sociality shapes individuals' novel food consumption remains largely untested in natural populations. Here, we use wild great tits to experimentally test how sociality predicts dietary decisions. We show that individuals with more social connections have higher propensity to use novel foods compared to socially peripheral individuals, and this is unrelated to neophobia, observations, and demographic factors. These findings indicate sociable individuals may offset potential costs of competition by foraging more broadly. We discuss how social environments may drive behavioral change in natural populations, and the implications for the causes and consequences of social strategies and dietary decisions.

The genomics of adaptation to climate in European great tit (Parus major) populations.

The recognition that climate change is occurring at an unprecedented rate means that there is increased urgency in understanding how organisms can adapt to a changing environment. Wild great tit (Parus major) populations represent an attractive ecological model system to understand the genomics of climate adaptation. They are widely distributed across Eurasia and they have been documented to respond to climate change. We performed a Bayesian genome-environment analysis, by combining local climate data with single nucleotide polymorphisms genotype data from 20 European populations (broadly spanning the species' continental range). We found 36 genes putatively linked to adaptation to climate. Following an enrichment analysis of biological process Gene Ontology (GO) terms, we identified over-represented terms and pathways among the candidate genes. Because many different genes and GO terms are associated with climate variables, it seems likely that climate adaptation is polygenic and genetically complex. Our findings also suggest that geographical climate adaptation has been occurring since great tits left their Southern European refugia at the end of the last ice age. Finally, we show that substantial climate-associated genetic variation remains, which will be essential for adaptation to future changes.

Spatially heterogeneous shifts in vegetation phenology induced by climate change threaten the integrity of the avian migration network.

Phenological responses to climate change frequently vary among trophic levels, which can result in increasing asynchrony between the peak energy requirements of consumers and the availability of resources. Migratory birds use multiple habitats with seasonal food resources along migration flyways. Spatially heterogeneous climate change could cause the phenology of food availability along the migration flyway to become desynchronized. Such heterogeneous shifts in food phenology could pose a challenge to migratory birds by reducing their opportunity for food availability along the migration path and consequently influencing their survival and reproduction. We develop a novel graph-based approach to quantify this problem and deploy it to evaluate the condition of the heterogeneous shifts in vegetation phenology for 16 migratory herbivorous waterfowl species in Asia. We show that climate change-induced heterogeneous shifts in vegetation phenology could cause a 12% loss of migration network integrity on average across all study species. Species that winter at relatively lower latitudes are subjected to a higher loss of integrity in their migration network. These findings highlight the susceptibility of migratory species to climate change. Our proposed methodological framework could be applied to migratory species in general to yield an accurate assessment of the exposure under climate change and help to identify actions for biodiversity conservation in the face of climate-related risks.

Variation in local population size predicts social network structure in wild songbirds.

The structure of animal societies is a key determinant of many ecological and evolutionary processes. Yet, we know relatively little about the factors and mechanisms that underpin detailed social structure. Among other factors, social structure can be influenced by habitat configuration. By shaping animal movement decisions, heterogeneity in habitat features, such as vegetation and the availability of resources, can influence the spatiotemporal distribution of individuals and subsequently key socioecological properties such as the local population size and density. Differences in local population size and density can impact opportunities for social associations and may thus drive substantial variation in local social structure. Here, we investigated spatiotemporal variation in population size at 65 distinct locations in a small songbird, the great tit (Parus major) and its effect on social network structure. We first explored the within-location consistency of population size from weekly samples and whether the observed variation in local population size was predicted by the underlying habitat configuration. Next, we created social networks from the birds' foraging associations at each location for each week and examined if local population size affected social structure. We show that population size is highly repeatable within locations across weeks and years and that some of the observed variation in local population size was predicted by the underlying habitat, with locations closer to the forest edge having on average larger population sizes. Furthermore, we show that local population size affected social structure inferred by four global network metrics. Using simple simulations, we then reveal that much of the observed social structure is shaped by social processes. Across different population sizes, the birds' social structure was largely explained by their preference to forage in flocks. In addition, over and above effects of social foraging, social preferences between birds (i.e. social relationships) shaped certain network features such as the extent of realized social connections. Our findings thus suggest that individual social decisions substantially contribute to shaping certain social network features over and above effects of population size alone.

Temporal avoidance as a means of reducing competition between sympatric species.

Human activity has modified the availability of natural resources and the abundance of species that rely on them, potentially changing interspecific competition dynamics. Here, we use large-scale automated data collection to quantify spatio-temporal competition among species with contrasting population trends. We focus on the spatial and temporal foraging behaviour of subordinate marsh tits Poecile palustris among groups of socially and numerically dominant blue tits Cyanistes caeruleus and great tits Parus major. The three species exploit similar food resources in mixed groups during autumn-winter. Using 421 077 winter recordings of individually marked birds at 65 automated feeding stations in Wytham Woods (Oxfordshire, UK), we found that marsh tits were less likely to join larger groups of heterospecifics, and they accessed food less frequently in larger groups than in smaller ones. Marsh tit numbers within groups declined throughout the diurnal and winter periods, while the number of blue and great tits increased. However, sites that attracted larger groups of these heterospecifics also attracted more marsh tits. The results suggest that subordinate species exhibit temporal avoidance of socially and numerically dominant heterospecifics, but have limited ability for spatial avoidance, indicating that behavioural plasticity enables only a partial reduction of interspecific competition.

Social learning mechanisms shape transmission pathways through replicate local social networks of wild birds.

The emergence and spread of novel behaviours via social learning can lead to rapid population-level changes whereby the social connections between individuals shape information flow. However, behaviours can spread via different mechanisms and little is known about how information flow depends on the underlying learning rule individuals employ. Here, comparing four different learning mechanisms, we simulated behavioural spread on replicate empirical social networks of wild great tits and explored the relationship between individual sociality and the order of behavioural acquisition. Our results reveal that, for learning rules dependent on the sum and strength of social connections to informed individuals, social connectivity was related to the order of acquisition, with individuals with increased social connectivity and reduced social clustering adopting new behaviours faster. However, when behavioural adoption depends on the ratio of an individuals' social connections to informed versus uninformed individuals, social connectivity was not related to the order of acquisition. Finally, we show how specific learning mechanisms may limit behavioural spread within networks. These findings have important implications for understanding whether and how behaviours are likely to spread across social systems, the relationship between individuals' sociality and behavioural acquisition, and therefore for the costs and benefits of sociality.

Social Familiarity and Spatially Variable Environments Independently Determine Reproductive Fitness in a Wild Bird.

AbstractThe social interactions that an individual experiences are a key component of its environment and can have important consequences for reproductive success. The dear enemy effect posits that having familiar neighbors at a territory boundary can reduce the need for territory defense and competition and potentially increase cooperation. Although fitness benefits of reproducing among familiar individuals are documented in many species, it remains unclear to what extent these relationships are driven by direct benefits of familiarity itself versus other socioecological covariates of familiarity. We use 58 years of great tit (Parus major) breeding data to disentangle the relationship between neighbor familiarity, partner familiarity, and reproductive success while simultaneously considering individual and spatiotemporal effects. We find that neighbor familiarity was positively associated with reproductive success for females but not males, while an individual's familiarity with their breeding partner was associated with fitness benefits for both sexes. There was strong spatial heterogeneity in all investigated fitness components, but our findings were robust and significant over and above these effects. Our analyses are consistent with direct effects of familiarity on individuals' fitness outcomes. These results suggest that social familiarity can yield direct fitness benefits, potentially driving the maintenance of long-term bonds and evolution of stable social systems.

Phenotypic plasticity increases exposure to extreme climatic events that reduce individual fitness.

Climate models, and empirical observations, suggest that anthropogenic climate change is leading to changes in the occurrence and severity of extreme climatic events (ECEs). Effects of changes in mean climate on phenology, movement, and demography in animal and plant populations are well documented. In contrast, work exploring the impacts of ECEs on natural populations is less common, at least partially due to the challenges of obtaining sufficient data to study such rare events. Here, we assess the effect of changes in ECE patterns in a long-term study of great tits, near Oxford, over a 56-year period between 1965 and 2020. We document marked changes in the frequency of temperature ECEs, with cold ECEs being twice as frequent in the 1960s than at present, and hot ECEs being ~three times more frequent between 2010 and 2020 than in the 1960s. While the effect of single ECEs was generally quite small, we show that increased exposure to ECEs often reduces reproductive output, and that in some cases the effect of different types of ECE is synergistic. We further show that long-term temporal changes in phenology, resulting from phenotypic plasticity, lead to an elevated risk of exposure to low temperature ECEs early in reproduction, and hence suggest that changes in ECE exposure may act as a cost of plasticity. Overall, our analyses reveal a complex set of risks of exposure and effects as ECE patterns change and highlight the importance of considering responses to changes in both mean climate and extreme events. Patterns in exposure and effects of ECEs on natural populations remain underexplored and continued work will be vital to establish the impacts of ECEs on populations in a changing climate.

Disentangling the causes of age-assortative mating in bird populations with contrasting life-history strategies.

Age shapes fundamental processes related to behaviour, survival and reproduction, where age influences reproductive success, non-random mating with respect to age can magnify or mitigate such effects. Consequently, the correlation in partners' age across a population may influence its productivity. Despite widespread evidence for age-assortative mating, little is known about what drives this assortment and its variation. Specifically, the relative importance of active (same-age mate preference) and passive processes (assortment as a consequence of other spatial or temporal effects) in driving age assortment is not well understood. In this paper, we compare breeding data from a great tit and mute swan population (51- and 31-year datasets, respectively) to tease apart the contributions of pair retention, cohort age structure and active age-related mate selection to age assortment in species with contrasting life histories. Both species show age-assortative mating and variable assortment between years. However, we demonstrate that the drivers of age assortment differ between the species, as expected from their life histories and resultant demographic differences. In great tits, pair fidelity has a weak effect on age-assortative mating through pair retention; variation in age assortment is primarily driven by fluctuations in age structure from variable juvenile recruitment. Age-assortative mating is, therefore, largely passive, with no evidence consistent with active age-related mate selection. In mute swans, age assortment is partly explained by pair retention, but not population age structure, and evidence exists for active age-assortative pairing. This difference is likely to result from shorter life-spans in great tits compared with mute swans, leading to fundamental differences in their population age structure, whereby a larger proportion of great tit populations consist of a single age cohort. In mute swans, age-assortative pairing through mate selection may also be driven by greater age-dependent variation in fitness. The study highlights the importance of considering how different life histories and demographic differences arising from these affect population processes that appear congruent across species. We suggest that future research should focus on uncovering the proximate mechanisms that lead to variation in active age-assortative mate selection (as seen in mute swans); and the consequences of variation in age structure on the ecological and social functioning of wild populations.

Temperature synchronizes temporal variation in laying dates across European hole-nesting passerines.

Identifying the environmental drivers of variation in fitness-related traits is a central objective in ecology and evolutionary biology. Temporal fluctuations of these environmental drivers are often synchronized at large spatial scales. Yet, whether synchronous environmental conditions can generate spatial synchrony in fitness-related trait values (i.e., correlated temporal trait fluctuations across populations) is poorly understood. Using data from long-term monitored populations of blue tits (Cyanistes caeruleus, n = 31), great tits (Parus major, n = 35), and pied flycatchers (Ficedula hypoleuca, n = 20) across Europe, we assessed the influence of two local climatic variables (mean temperature and mean precipitation in February-May) on spatial synchrony in three fitness-related traits: laying date, clutch size, and fledgling number. We found a high degree of spatial synchrony in laying date but a lower degree in clutch size and fledgling number for each species. Temperature strongly influenced spatial synchrony in laying date for resident blue tits and great tits but not for migratory pied flycatchers. This is a relevant finding in the context of environmental impacts on populations because spatial synchrony in fitness-related trait values among populations may influence fluctuations in vital rates or population abundances. If environmentally induced spatial synchrony in fitness-related traits increases the spatial synchrony in vital rates or population abundances, this will ultimately increase the risk of extinction for populations and species. Assessing how environmental conditions influence spatiotemporal variation in trait values improves our mechanistic understanding of environmental impacts on populations.

Social phenotype-dependent selection of social environment in wild great and blue tits: an experimental study.

There is growing evidence that individuals actively assess the match between their phenotype and their environment when making habitat choice decisions (so-called matching habitat choice). However, to our knowledge, no studies have considered how the social environment may interact with social phenotype in determining habitat choice, despite habitat choice being an inherently social process and growing evidence for individual variation in sociability. We conducted an experiment using wild great and blue tits to understand how birds integrate their social phenotype and social environment when choosing where and how to feed. We used programmable feeders to (i) record social interactions and estimate social phenotype, and (ii) experimentally manipulate the local density experienced by birds of differing social phenotype. By tracking feeder usage, we estimated how social environment and social phenotype predicted feeder choice and feeding behaviour. Both social environment and social phenotype predicted feeder usage, but a bird's decision to remain in a particular social environment did not depend on their social phenotype. By contrast, for feeding behaviour, responses to the social environment depended on social phenotype. Our results provide rare evidence of matching habitat choice and shed light on the dependence of habitat choice on between-individual differences in social phenotype.

Limited domestic introgression in a final refuge of the wild pigeon.

Domesticated animals have been culturally and economically important throughout history. Many of their ancestral lineages are extinct or genetically endangered following hybridization with domesticated relatives. Consequently, they have been understudied compared to the ancestral lineages of domestic plants. The domestic pigeon Columba livia, which was pivotal in Darwin's studies, has maintained outsized cultural significance. Its role as a model organism spans the fields of behavior, genetics, and evolution. Domestic pigeons have hybridized with their progenitor, the Rock Dove, rendering the latter of dubious genetic status. Here, we use genomic and morphological data from the putative Rock Doves of the British Isles to identify relictual undomesticated populations. We reveal that Outer Hebridean Rock Doves have experienced minimal levels of introgression. Our results outline the contemporary status of these wild pigeons, highlighting the role of hybridization in the homogenization of genetic lineages.

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.

Bird populations most exposed to climate change are less sensitive to climatic variation.

The phenology of many species shows strong sensitivity to climate change; however, with few large scale intra-specific studies it is unclear how such sensitivity varies over a species' range. We document large intra-specific variation in phenological sensitivity to temperature using laying date information from 67 populations of two co-familial European songbirds, the great tit (Parus major) and blue tit (Cyanistes caeruleus), covering a large part of their breeding range. Populations inhabiting deciduous habitats showed stronger phenological sensitivity than those in evergreen and mixed habitats. However, populations with higher sensitivity tended to have experienced less rapid change in climate over the past decades, such that populations with high phenological sensitivity will not necessarily exhibit the strongest phenological advancement. Our results show that to effectively assess the impact of climate change on phenology across a species' range it will be necessary to account for intra-specific variation in phenological sensitivity, climate change exposure, and the ecological characteristics of a population.

Recognising the key role of individual recognition in social networks.

Many aspects of sociality rely on individuals recognising one another. Understanding how, when, and if individuals recognise others can yield insights into the foundations of social relationships and behaviours. Through synthesising individual recognition research in different sensory and social domains, and doing so across various related social contexts, we propose that a social network perspective can help to uncover how individual recognition may vary across different settings, species, and populations. Specifically, combining individual recognition with social networks has unrecognised potential for determining the level and relative importance of individual recognition complexity. This will provide insights not only on the ecology and evolution of individual recognition itself, but also on social structure, social transmission, and social interactions such as cooperation.

Habitat change and biased sampling influence estimation of diversity trends.

Recent studies have drawn contrasting conclusions about the extent to which local-scale measures of biodiversity are declining and whether such patterns conflict with the global-scale declines that have attracted much attention.1 A key source of high-quality data for such analyses comes from longitudinal biodiversity studies, which sample a given taxon repeatedly over time at a specific location.2 There has been relatively little consideration of how habitat change might lead to biases in the sampling and continuity of biodiversity time series data, and the consequent potential for bias in the biodiversity trends that result. Here, based on analysis of standardized routes from the North American Breeding Bird Survey (3,014 routes sampled over 18 years),3 we demonstrate that major local habitat change is associated with an increase in the rate of survey cessations. We further show that routes that were continued despite major habitat changes show reduced diversity. By simulating potential rates of loss, we show that the underlying real trends in taxonomic, functional, and phylogenetic diversity can even reverse in sign if more than a quarter of diversity is lost from routes that ceased and are thus no longer included in surveys. Our analyses imply that biodiversity loss can be underestimated by biases introduced if continued sampling in longitudinal studies is influenced by local change. We argue that researchers and conservation practitioners should be aware of the potential for bias in such data and seek to use more robust methods to evaluate biodiversity trends and make conservation decisions.