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.

Temperature has an overriding role compared to photoperiod in regulating the seasonal timing of winter moth egg hatching.

To accurately predict species' phenology under climate change, we need to gain a detailed mechanistic understanding of how different environmental cues interact to produce the seasonal timing response. In the winter moth (Operophtera brumata), seasonal timing of egg hatching is strongly affected by ambient temperature and has been under strong climate change-induced selection over the past 25 years. However, it is unclear whether photoperiod received at the egg stage also influences timing of egg hatching. Here, we investigated the relative contribution of photoperiod and temperature in regulating winter moth egg development using two split-brood experiments. We experimentally shifted the photoperiod eggs received by 2-4 weeks compared to the actual calendar date and measured the timing of egg hatching, both at a constant temperature and in combination with two naturally changing temperature treatments - mimicking a cold and a warm year. We found an eight-fold larger effect of temperature compared to photoperiod on egg development time. Moreover, the very small photoperiod effects we found were outweighed by both between- and within-clutch variation in egg development time. Thus, we conclude that photoperiod received at the egg stage does likely not play a substantial role in regulating the seasonal timing of egg hatching in the winter moth. These insights into the regulatory mechanism of seasonal timing could have important implications for predicting insect climate change adaptation, as we might expect different targets of selection depending on the relative contribution of different environmental cues.

Odours of caterpillar-infested trees increase testosterone concentrations in male great tits.

Trees release Herbivore-Induced Plant Volatiles (HIPVs) into the air in response to damage inflicted by insects. It is known that songbirds use those compounds to locate their prey, but more recently the idea emerged that songbirds could also use those odours as cues in their reproductive decisions, as early spring HIPVs may contain information about the seasonal timing and abundance of insects. We exposed pre-breeding great tits (Parus major) to the odours of caterpillar-infested trees under controlled conditions, and monitored reproduction (timing of egg laying, number of eggs, egg size) and two of its main hormonal drivers (testosterone and 17ß-estradiol in males and females, respectively). We found that females exposed to HIPVs did not advance their laying dates, nor laid larger clutches, or larger eggs compared to control females. 17ß-estradiol concentrations in females were also similar between experimental and control birds. However, males exposed to HIPVs had higher testosterone concentrations during the egg-laying period. Our study supports the hypothesis that insectivorous songbirds are able to detect minute amounts of plant odours. The sole manipulation of plant scents was not sufficient to lure females into a higher reproductive investment, but males increased their reproductive effort in response to a novel source of information for seasonal breeding birds.

Short-time exposure to light at night affects incubation patterns and correlates with subsequent body weight in great tits (Parus major).

Artificial light at night (ALAN) widely affects wildlife by blurring light-dark differences, including transitions such as sunrise and sunset, thereby affecting regulation of diel rhythms. As a result, activity onsets in many wild diurnal songbirds advance under ALAN. From chronobiological studies, it is known that the direction and strength of the response to light depends on when during the night exposure takes place. However, these experiments are mostly done under continuous light conditions, when animals have free-running rhythms. It remains unclear whether phase-dependence also holds in entrained, wild songbirds; i.e., does the effect of ALAN on activity patterns differ between exposure in the morning compared to the evening? This information is essential to assess the effects of mitigation measures by limiting ALAN to selected times of the night. We exposed incubating great tits (Parus major) inside the nest-box to 4 h of dim light, of which 1 h overlapped with dawn before sunrise or dusk after sunset. We found a small advancing effect of morning-light on activity onset and of evening-light on offset compared to dark controls but not vice versa. Breeding success and chick condition were unaffected by the light treatments. However, light-treated females had lower weights 9-18 days after the end of the treatment compared to the controls, independent of whether ALAN occurred in the morning or the evening, indicating possible costs of ALAN. Despite the weak behavioral response, ALAN might have affected the females' circadian clock or physiology resulting in lower body condition.

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.

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.

Climate change does not equally affect temporal patterns of natural selection on reproductive timing across populations in two songbird species.

Climate change has led to changes in the strength of directional selection on seasonal timing. Understanding the causes and consequences of these changes is crucial to predict the impact of climate change. But are observed patterns in one population generalizable to others, and can spatial variation in selection be explained by environmental variation among populations? We used long-term data (1955-2022) on blue and great tits co-occurring in four locations across the Netherlands to assess inter-population variation in temporal patterns of selection on laying date. To analyse selection, we combine reproduction and adult survival into a joined fitness measure. We found distinct spatial variation in temporal patterns of selection which overall acted towards earlier laying, and which was due to selection through reproduction rather than through survival. The underlying relationships between temperature, bird and caterpillar phenology were however the same across populations, and the spatial variation in selection patterns is thus caused by spatial variation in the temperatures and other habitat characteristics to which birds and caterpillars respond. This underlines that climate change is not necessarily equally affecting populations, but that we can understand this spatial variation, which enables us to predict climate change effects on selection for other populations.

Long-term exposure to experimental light affects the ground-dwelling invertebrate community, independent of light spectra.

Our planet endures a progressive increase in artificial light at night (ALAN), which affects virtually all species, and thereby biodiversity. Mitigation strategies include reducing its intensity and duration, and the adjustment of light spectrum using modern light emitting diode (LED) light sources. Here, we studied ground-dwelling invertebrate (predominantly insects, arachnids, molluscs, millipedes, woodlice and worms) diversity and community composition after 3 or 4 years of continued nightly exposure (every night from sunset to sunrise) to experimental ALAN with three different spectra (white-, and green- and red-dominated light), as well as for a dark control, in natural forest-edge habitat. Diversity of pitfall-trapped ground-dwelling invertebrates, and the local contribution to beta diversity, did not differ between the dark control and illuminated sites, or between the different spectra. The invertebrate community composition, however, was significantly affected by the presence of light. Keeping lights off during single nights did show an immediate effect on the composition of trapped invertebrates compared to illuminated nights. These effects of light on species composition may impact ecosystems by cascading effects across the food web. This article is part of the theme issue 'Light pollution in complex ecological systems'.

Phenological mismatch affects individual fitness and population growth in the winter moth.

Climate change can severely impact species that depend on temporary resources by inducing phenological mismatches between consumer and resource seasonal timing. In the winter moth, warmer winters caused eggs to hatch before their food source, young oak leaves, became available. This phenological mismatch changed the selection on the temperature sensitivity of egg development rate. However, we know little about the fine-scale fitness consequences of phenological mismatch at the individual level and how this mismatch affects population dynamics in the winter moth. To determine the fitness consequences of mistimed egg hatching relative to timing of oak budburst, we quantified survival and pupation weight in a feeding experiment. We found that mismatch greatly increased mortality rates of freshly hatched caterpillars, as well as affecting caterpillar growth and development time. We then investigated whether these individual fitness consequences have population-level impacts by estimating the effect of phenological mismatch on population dynamics, using our long-term data (1994-2021) on relative winter moth population densities at four locations in The Netherlands. We found a significant effect of mismatch on population density with higher population growth rates in years with a smaller phenological mismatch. Our results indicate that climate change-induced phenological mismatch can incur severe individual fitness consequences that can impact population density in the wild.

Individual life histories: neither slow nor fast, just diverse.

The slow-fast continuum is a commonly used framework to describe variation in life-history strategies across species. Individual life histories have also been assumed to follow a similar pattern, especially in the pace-of-life syndrome literature. However, whether a slow-fast continuum commonly explains life-history variation among individuals within a population remains unclear. Here, we formally tested for the presence of a slow-fast continuum of life histories both within populations and across species using detailed long-term individual-based demographic data for 17 bird and mammal species with markedly different life histories. We estimated adult lifespan, age at first reproduction, annual breeding frequency, and annual fecundity, and identified the main axes of life-history variation using principal component analyses. Across species, we retrieved the slow-fast continuum as the main axis of life-history variation. However, within populations, the patterns of individual life-history variation did not align with a slow-fast continuum in any species. Thus, a continuum ranking individuals from slow to fast living is unlikely to shape individual differences in life histories within populations. Rather, individual life-history variation is likely idiosyncratic across species, potentially because of processes such as stochasticity, density dependence, and individual differences in resource acquisition that affect species differently and generate non-generalizable patterns across species.

Genotypes selected for early and late avian lay date differ in their phenotype, but not fitness, in the wild.

Global warming has shifted phenological traits in many species, but whether species are able to track further increasing temperatures depends on the fitness consequences of additional shifts in phenological traits. To test this, we measured phenology and fitness of great tits (Parus major) with genotypes for extremely early and late egg lay dates, obtained from a genomic selection experiment. Females with early genotypes advanced lay dates relative to females with late genotypes, but not relative to nonselected females. Females with early and late genotypes did not differ in the number of fledglings produced, in line with the weak effect of lay date on the number of fledglings produced by nonselected females in the years of the experiment. Our study is the first application of genomic selection in the wild and led to an asymmetric phenotypic response that indicates the presence of constraints toward early, but not late, lay dates.

Combining acoustic tracking and LiDAR to study bat flight behaviour in three-dimensional space.

BACKGROUND: Habitat structure strongly influences niche differentiation, facilitates predator avoidance, and drives species-specific foraging strategies of bats. Vegetation structure is also a strong driver of echolocation call characteristics. The fine-scale assessment of how bats utilise such structures in their natural habitat is instrumental in understanding how habitat composition shapes flight- and acoustic behaviour. However, it is notoriously difficult to study their species-habitat relationship in situ. METHODS: Here, we describe a methodology combining Light Detection and Ranging (LiDAR) to characterise three-dimensional vegetation structure and acoustic tracking to map bat behaviour. This makes it possible to study fine-scale use of habitat by bats, which is essential to understand spatial niche segregation in bats. Bats were acoustically tracked with microphone arrays and bat calls were classified to bat guild using automated identification. We did this in multiple LiDAR scanned vegetation plots in forest edge habitat. The datasets were spatially aligned to calculate the distance between bats' positions and vegetation structures. RESULTS: Our results are a proof of concept of combining LiDAR with acoustic tracking. Although it entails challenges with combining mass-volumes of fine-scale bat movements and vegetation information, we show the feasibility and potential of combining those two methods through two case studies. The first one shows stereotyped flight patterns of pipistrelles around tree trunks, while the second one presents the distance that bats keep to the vegetation in the presence of artificial light. CONCLUSION: By combining bat guild specific spatial behaviour with precise information on vegetation structure, the bat guild specific response to habitat characteristics can be studied in great detail. This opens up the possibility to address yet unanswered questions on bat behaviour, such as niche segregation or response to abiotic factors in interaction with natural vegetation. This combination of techniques can also pave the way for other applications linking movement patterns of other vocalizing animals and 3D space reconstruction.

Towards evolutionary predictions: Current promises and challenges.

Evolution has traditionally been a historical and descriptive science, and predicting future evolutionary processes has long been considered impossible. However, evolutionary predictions are increasingly being developed and used in medicine, agriculture, biotechnology and conservation biology. Evolutionary predictions may be used for different purposes, such as to prepare for the future, to try and change the course of evolution or to determine how well we understand evolutionary processes. Similarly, the exact aspect of the evolved population that we want to predict may also differ. For example, we could try to predict which genotype will dominate, the fitness of the population or the extinction probability of a population. In addition, there are many uses of evolutionary predictions that may not always be recognized as such. The main goal of this review is to increase awareness of methods and data in different research fields by showing the breadth of situations in which evolutionary predictions are made. We describe how diverse evolutionary predictions share a common structure described by the predictive scope, time scale and precision. Then, by using examples ranging from SARS-CoV2 and influenza to CRISPR-based gene drives and sustainable product formation in biotechnology, we discuss the methods for predicting evolution, the factors that affect predictability and how predictions can be used to prevent evolution in undesirable directions or to promote beneficial evolution (i.e. evolutionary control). We hope that this review will stimulate collaboration between fields by establishing a common language for evolutionary predictions.

The opportunity for selection: A slippery concept in ecology and evolution.

Natural selection can only occur if individuals differ in fitness. For this reason, the variance in relative fitness has been equated with the 'opportunity for selection' ( I ), which has a long, albeit somewhat controversial, history. In this paper we discuss the use/misuse of I and related metrics in evolutionary ecology. The opportunity is only realised if some fraction of I is caused by trait variation. Thus, I > 0 does not imply that selection is occurring, as sometimes erroneously assumed, because all fitness variation could be independent of phenotype. The selection intensity on any given trait cannot exceed I , but this upper limit will never be reached because (a) stochastic factors always affect fitness, and (b) there might be multiple traits under selection. The expected magnitude of the stochastic component of I is negatively correlated with mean fitness. Uncertainty in realised I is also larger when mean fitness or population/sample size are low. Variation in I across time or space thus can be dominated (or solely driven) by variation in the strength of demographic stochasticity. We illustrate these points using simulations and empirical data from a population study on great tits Parus major. Our analysis shows that the scope for fecundity selection in the great tits is substantially higher when using annual number of recruits as the fitness measure, rather than fledglings or eggs, even after adjusting for the dependence of I on mean fitness. This suggests nonrandom survival of juveniles across families between life stages. Indeed, previous work on this population has shown that offspring recruitment is often nonrandom with respect to clutch size and laying date of parents, for example. We conclude that one cannot make direct inferences about selection based on fitness data alone. However, examining variation in ∆ I F (the opportunity for fecundity selection adjusted for mean fitness) across life stages, years or environments can offer clues as to when/where fecundity selection might be strongest, which can be useful for research planning and experimental design.

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.

Species-specific song responses emerge as a by-product of tuning to the local dialect.

Oscine birds preferentially respond to certain sounds over others from an early age, which focuses subsequent learning onto sexually relevant songs.1,2,3 Songs vary both across species and, due to cultural evolution, among populations of the same species. As a result, early song responses are expected to be shaped by selection both to avoid the fitness costs of cross-species learning4 and to promote learning of population-typical songs.5 These sources of selection are not mutually exclusive but can result in distinct geographic patterns of song responses in juvenile birds: if the risks of interspecific mating are the main driver of early song discrimination, then discrimination should be strongest where closely related species co-occur.4 In contrast, if early discrimination primarily facilitates learning local songs, then it should be tuned to songs typical of the local dialect.5,6,7 Here, we experimentally assess the drivers of song discrimination in nestling pied flycatchers (Ficedula hypoleuca). We first demonstrate that early discrimination against the songs of the closely related collared flycatcher (F. albicollis) is not strongly affected by co-occurrence. Second, across six European populations, we show that nestlings' early song responses are tuned to their local song dialect and that responses to the songs of collared flycatchers are similarly weak as to those of other conspecific dialects. Taken together, these findings provide clear experimental support for the hypothesis that cultural evolution, in conjunction with associated learning predispositions, drives the emergence of pre-mating reproductive barriers.

Transcriptional regulation underlying the temperature response of embryonic development rate in the winter moth.

Climate change will strongly affect the developmental timing of insects, as their development rate depends largely on ambient temperature. However, we know little about the genetic mechanisms underlying the temperature sensitivity of embryonic development in insects. We investigated embryonic development rate in the winter moth (Operophtera brumata), a species with egg dormancy which has been under selection due to climate change. We used RNA sequencing to investigate which genes are involved in the regulation of winter moth embryonic development rate in response to temperature. Over the course of development, we sampled eggs before and after an experimental change in ambient temperature, including two early development weeks when the temperature sensitivity of eggs is low and two late development weeks when temperature sensitivity is high. We found temperature-responsive genes that responded in a similar way across development, as well as genes with a temperature response specific to a particular development week. Moreover, we identified genes whose temperature effect size changed around the switch in temperature sensitivity of development rate. Interesting candidate genes for regulating the temperature sensitivity of egg development rate included genes involved in histone modification, hormonal signalling, nervous system development and circadian clock genes. The diverse sets of temperature-responsive genes we found here indicate that there are many potential targets of selection to change the temperature sensitivity of embryonic development rate. Identifying for which of these genes there is genetic variation in wild insect populations will give insight into their adaptive potential in the face of climate change.

Population bottleneck has only marginal effect on fitness evolution and its repeatability in dioecious Caenorhabditis elegans.

The predictability of evolution is expected to depend on the relative contribution of deterministic and stochastic processes. This ratio is modulated by effective population size. Smaller effective populations harbor less genetic diversity and stochastic processes are generally expected to play a larger role, leading to less repeatable evolutionary trajectories. Empirical insight into the relationship between effective population size and repeatability is limited and focused mostly on asexual organisms. Here, we tested whether fitness evolution was less repeatable after a population bottleneck in obligately outcrossing populations of Caenorhabditis elegans. Replicated populations founded by 500, 50, or five individuals (no/moderate/strong bottleneck) were exposed to a novel environment with a different bacterial prey. As a proxy for fitness, population size was measured after one week of growth before and after 15 weeks of evolution. Surprisingly, we found no significant differences among treatments in their fitness evolution. Even though the strong bottleneck reduced the relative contribution of selection to fitness variation, this did not translate to a significant reduction in the repeatability of fitness evolution. Thus, although a bottleneck reduced the contribution of deterministic processes, we conclude that the predictability of evolution may not universally depend on effective population size, especially in sexual organisms.

Temporal correlations among demographic parameters are ubiquitous but highly variable across species.

Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species' life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.

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.