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.

Divergence in evolutionary potential of life history traits among wild populations is predicted by differences in climatic conditions.

Short-term adaptive evolution represents one of the primary mechanisms allowing species to persist in the face of global change. Predicting the adaptive response at the species level requires reliable estimates of the evolutionary potential of traits involved in adaptive responses, as well as understanding how evolutionary potential varies across a species' range. Theory suggests that spatial variation in the fitness landscape due to environmental variation will directly impact the evolutionary potential of traits. However, empirical evidence on the link between environmental variation and evolutionary potential across a species range in the wild is lacking. In this study, we estimate multivariate evolutionary potential (via the genetic variance-covariance matrix, or G-matrix) for six morphological and life history traits in 10 wild populations of great tits (Parus major) distributed across Europe. The G-matrix significantly varies in size, shape, and orientation across populations for both types of traits. For life history traits, the differences in G-matrix are larger when populations are more distant in their climatic niche. This suggests that local climates contribute to shaping the evolutionary potential of phenotypic traits that are strongly related to fitness. However, we found no difference in the overall evolutionary potential (i.e., G-matrix size) between populations closer to the core or the edge of the distribution area. This large-scale comparison of G-matrices across wild populations emphasizes that integrating variation in multivariate evolutionary potential is important to understand and predict species' adaptive responses to new selective pressures.

Metabolic adjustments to winter severity in two geographically separated great tit (Parus major) populations.

Understanding the potential limits placed on organisms by their ecophysiology is crucial for predicting their responses to varying environmental conditions. A main hypothesis for explaining avian thermoregulatory mechanisms is the aerobic capacity model, which posits a positive correlation between basal (basal metabolic rate [BMR]) and summit (Msum) metabolism. Most evidence for this hypothesis, however, comes from interspecific comparisons, and the ecophysiological underpinnings of avian thermoregulatory capacities hence remain controversial. Indeed, studies have traditionally relied on between-species comparisons, although, recently, there has been a growing recognition of the importance of intraspecific variation in ecophysiological responses. Therefore, here, we focused on great tits (Parus major), measuring BMR and Msum during winter in two populations from two different climates: maritime-temperate (Gontrode, Belgium) and continental (Zvenigorod, Russia). We tested for the presence of intraspecific geographical variation in metabolic rates and assessed the predictions following the aerobic capacity model. We found that birds from the maritime-temperate climate (Gontrode) showed higher BMR, whereas conversely, great tits from Zvenigorod showed higher levels of Msum. Within each population, our data did not fully support the aerobic capacity model's predictions. We argued that the decoupling of BMR and Msum observed may be caused by different selective forces acting on these metabolic rates, with birds from the continental-climate Zvenigorod population facing the need to conserve energy for surviving long winter nights (by keeping their BMR at low levels) while simultaneously being able to generate more heat (i.e., a high Msum) to withstand cold spells.

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.

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.

Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders.

Many organisms adjust their reproductive phenology in response to climate change, but phenological sensitivity to temperature may vary between species. For example, resident and migratory birds have vastly different annual cycles, which can cause differential temperature sensitivity at the breeding grounds, and may affect competitive dynamics. Currently, however, adjustment to climate change in resident and migratory birds have been studied separately or at relatively small geographical scales with varying time series durations and methodologies. Here, we studied differential effects of temperature on resident and migratory birds using the mean egg laying initiation dates from 10 European nest box schemes between 1991 and 2015 that had data on at least one resident tit species and at least one migratory flycatcher species. We found that both tits and flycatchers advanced laying in response to spring warming, but resident tit populations advanced more strongly in relation to temperature increases than migratory flycatchers. These different temperature responses have already led to a divergence in laying dates between tits and flycatchers of on average 0.94 days per decade over the current study period. Interestingly, this divergence was stronger at lower latitudes where the interval between tit and flycatcher phenology is smaller and winter conditions can be considered more favorable for resident birds. This could indicate that phenological adjustment to climate change by flycatchers is increasingly hampered by competition with resident species. Indeed, we found that tit laying date had an additional effect on flycatcher laying date after controlling for temperature, and this effect was strongest in areas with the shortest interval between both species groups. Combined, our results suggest that the differential effect of climate change on species groups with overlapping breeding ecology affects the phenological interval between them, potentially affecting interspecific interactions.

Large-scale geographical variation confirms that climate change causes birds to lay earlier.

Advances in the phenology of organisms are often attributed to climate change, but alternatively, may reflect a publication bias towards advances and may be caused by environmental factors unrelated to climate change. Both factors are investigated using the breeding dates of 25 long-term studied populations of Ficedula flycatchers across Europe. Trends in spring temperature varied markedly between study sites, and across populations the advancement of laying date was stronger in areas where the spring temperatures increased more, giving support to the theory that climate change causally affects breeding date advancement.

Variable responses to large-scale climate change in European Parus populations.

Spring temperatures in temperate regions have increased over the past 20 years and many organisms have responded to this increase by advancing the timing of their growth and reproduction. However, not all populations show an advancement of phenology. Understanding why some populations advance and others do not will give us insight into the possible constraints and selection pressures on the advancement of phenology. By combining two decades of data on 24 populations of tits (Parus sp.) from six European countries, we show that the phenological response to large-scale changes in spring temperature varies across a species' range, even between populations situated close to each other. We show that this variation cannot be fully explained by variation in the temperature change during the pre- and post-laying periods, as recently suggested. Instead, we find evidence for a link between rising temperatures and the frequency of second broods, which results in complex shifts in the laying dates of first clutches. Our results emphasize the need to consider links between different life-history parameters in order to predict the ecological consequences of large-scale climate changes.