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.

Fluctuating optimum and temporally variable selection on breeding date in birds and mammals.

Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.

Differences in the temporal scale of reproductive investment across the slow-fast continuum in a passerine.

Life-history strategies differ with respect to investment in current versus 'future' reproduction, but when is this future? Under the novel 'temporality in reproductive investment hypothesis', we postulate variation should exist in the time frame over which reproductive costs are paid. Slow-paced individuals should pay reproductive costs over short (e.g. inter-annual) time scales to prevent reproductive costs accumulating, whereas fast-paced individuals should allow costs to accumulate (i.e. senescence). Using Fourier transforms, we quantify adjustments in clutch size with age, across four populations of blue tits (Cyanistes caeruleus). Fast populations had more prevalent and stronger long-term changes in reproductive investment, whereas slower populations had more prevalent short-term adjustments. Inter-annual environmental variation partly accounted for short-, but not long-term changes in reproductive investment. Our study reveals individuals differ in when they pay the cost of reproduction and that failure to partition this variation across different temporal scales and environments could underestimate reproductive trade-offs.

A global meta-analysis reveals higher variation in breeding phenology in urban birds than in their non-urban neighbours.

Cities pose a major ecological challenge for wildlife worldwide. Phenotypic variation, which can result from underlying genetic variation or plasticity, is an important metric to understand eco-evolutionary responses to environmental change. Recent work suggests that urban populations might have higher levels of phenotypic variation than non-urban counterparts. This prediction, however, has never been tested across species nor over a broad geographical range. Here, we conducted a meta-analysis of the avian literature to compare urban versus non-urban means and variation in phenology (i.e. lay date) and reproductive effort (i.e. clutch size, number of fledglings). First, we show that urban populations reproduce earlier and have smaller broods than non-urban conspecifics. Second, we show that urban populations have higher phenotypic variation in laying date than non-urban populations. This result arises from differences between populations within breeding seasons, conceivably due to higher landscape heterogeneity in urban habitats. These findings reveal a novel effect of urbanisation on animal life histories with potential implications for species adaptation to urban environments (which will require further investigation). The higher variation in phenology in birds subjected to urban disturbance could result from plastic responses to a heterogeneous environment, or from higher genetic variation in phenology, possibly linked to higher evolutionary potential.

Long-Term Decrease in Coloration: A Consequence of Climate Change?

AbstractClimate change has been shown to affect fitness-related traits in a wide range of taxa; for instance, warming leads to phenological advancements in many plant and animal species. The influence of climate change on social and secondary sexual traits, which are associated with fitness because of their role as quality signals, is, however, unknown. Here, we use more than 5,800 observations collected on two Mediterranean blue tit subspecies (Cyanistes caeruleus caeruleus and Cyanistes caeruleus ogliastrae) to explore whether blue crown and yellow breast patch colorations have changed over the past 15 years. Our data suggest that coloration has become duller and less chromatic in both sexes. In addition, in the Corsican C.c. ogliastrae, but not in the mainland C.c. caeruleus, the decrease is associated with an increase in temperature at molt. Quantitative genetic analyses do not reveal any microevolutionary change in the color traits over the study period, strongly suggesting that the observed change over time was caused by a plastic response to the environmental conditions. Overall, this study suggests that ornamental colorations could become less conspicuous because of warming, revealing climate change effects on sexual and social ornaments and calling for further research on the proximate mechanisms behind these effects.

Are behaviour and stress-related phenotypes in urban birds adaptive?

Urbanisation is a world-wide phenomenon converting natural habitats into new artificial ones. Environmental conditions associated with urbanisation represent great challenges for wildlife. Behaviour and stress tolerance are considered of major importance in the adaptation to novel urban habitats and numerous studies already reported behavioural and stress response phenotypes associated with urbanisation, often suggesting they represented adaptations, while rarely demonstrating it. The main goal of this study was to test the adaptive nature of urban shifts in behavioural and stress-related traits, and by adaptive we mean phenotypic change favouring traits in the same direction as selection. Using 7 years of monitoring of urban and forest great tits, we first tested for differences in exploratory behaviour, aggressiveness and breath rate, between both habitats. Second, we performed habitat-specific analyses of selection on the three former traits using (a) reproductive success and (b) survival estimated via capture-mark-recapture models, as fitness estimates, to determine whether shifts in these behavioural and stress-related traits were aligned with patterns of ongoing selection. We found that urban birds displayed higher exploratory behaviour and aggressiveness, and higher breath rate, compared to forest birds. Selection analyses overall revealed that these shifts were not adaptive and could even be maladaptive. In particular, higher handling aggression and higher breath rate in urban birds was associated with lower fitness. Higher exploration scores were correlated with lower survival in both habitats, but higher reproductive success only in forest males. Overall, differences in patterns of selection between habitats were not consistent with the phenotypic divergence observed. Taken together, these results highlight that phenotypic shifts observed in cities do not necessarily result from new selection pressures and could be maladaptive. We hypothesise that divergences in behavioural traits for urban birds could result from the filtering of individuals settling in cities. We thus encourage urban evolutionary scientists to further explore the adaptive potential of behavioural traits measured in urban habitats (a) by replicating this type of study in multiple cities and species, (b) by implementing studies focusing on immigrant phenotypes and (c) by measuring selection at multiple life stages.

Environmental conditions variably affect growth across the breeding season in a subarctic seabird.

Predicting the impacts of changing environments on phenotypes in wild populations remains a challenge. Growth, a trait that frequently influences fitness, is difficult to study as it is influenced by many environmental variables. To address this, we used a sliding window approach to determine the time windows when sea-surface and air temperatures have the potential to affect growth of black-legged kittiwakes (Rissa tridactyla) on a colony in the Northeast Pacific. We examined environmental drivers influencing nestling growth using data from a long-term (21-year) study, that food supplements a portion of the colony. The associations between kittiwake growth and climatic conditions in our study indicated that warmer environmental conditions can both positively and negatively impact nestling growth parameters depending on hatching order. We found that first-hatched nestlings had a heavier maximum mass under warm air temperatures and cold sea conditions. Warmer air temperatures negatively affected the second-hatched nestling in a brood. However, when air temperatures were warm, warmer sea-surface temperatures predicted heavy, fast-growing second-hatched nestlings in contrast to what we observed for first-hatched nestlings. Food supplementation alleviated the temperature effects, and competition among nestlings influenced how strongly a variable affected growth. We identified windows that might indicate specific biological pathways through which environmental variation affected growth directly or indirectly. Overall, our windows suggest that nestlings in shared nests will be most affected by warming conditions.

Evolutionary Genomics at the Human-Environment Interface in Africa.

We report on the first meeting of SMBE in Africa. SMBE Malawi was initiated to bring together African and international researchers who use genetics or genomics to study natural systems impacted by human activities. The goals of this conference were 1) to reach a world-class standard of science with a large number of contributions from Africa, 2) to initiate exchange between African and international researchers, and 3) to identify challenges and opportunities for evolutionary genomics research in Africa. As repored, we think that we have achieved these goals and make suggestions on the way forward for African evolutionary genomics research.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.

Understanding the Social Dynamics of Breeding Phenology: Indirect Genetic Effects and Assortative Mating in a Long-Distance Migrant.

AbstractPhenological traits, such as the timing of reproduction, are often influenced by social interactions between paired individuals. Such partner effects may occur when pair members affect each other's prebreeding environment. Partner effects can be environmentally and/or genetically determined, and quantifying direct and indirect genetic effects is important for understanding the evolutionary dynamics of phenological traits. Here, using 26 years of data from a pedigreed population of a migratory seabird, the common tern (Sterna hirundo), we investigate male and female effects on female laying date. We find that female laying date harbors both genetic and environmental variation and is additionally influenced by the environmental and, to a lesser extent, genetic component of its mate. We demonstrate this partner effect to be largely explained by male arrival date. Interestingly, analyses of mating patterns with respect to arrival date show mating to be strongly assortative, and using simulations we show that assortative mating leads to overestimation of partner effects. Our study provides evidence for partner effects on breeding phenology in a long-distance migrant while uncovering the potential causal pathways underlying the observed effects and raising awareness for confounding effects resulting from assortative mating or other common environmental effects.

Age-dependent phenological plasticity in a wild bird.

Life-history traits are often plastic in response to environmental factors such as temperature or precipitation, and they also vary with age in many species. Trait variation during the lifetime could thus be partly driven by age-dependent plasticity in these traits. We study whether plasticity of a phenological trait-the egg-laying date-with respect to spring temperature, varies with age, and explore whether this variation relates to changes in breeding success throughout the life cycle. We use data from a four-decade long-term monitoring of a wild population of blue tits in Corsica, to estimate age-dependent plasticity of reproductive phenology and annual reproductive success. We show that both laying date plasticity and annual reproductive success vary with age: young and old females are less plastic, and fledge fewer offspring, than middle-age females. Furthermore, in contrast to young and prime-age females, in old females fledging success does not depend on laying date. Phenological plasticity is a major mechanism for coping with rapid environmental variation. Our results suggest that understanding its role in adaptation to climate change and population persistence requires integrating the age structure of the population.

Surface temperatures of non-incubated eggs in great tits (Parus major) are strongly associated with ambient temperature.

Temperature is one of the best investigated environmental factors in ecological life-history studies and is increasingly considered in the contexts of climate change and urbanization. In avian ecology, few studies have examined the associations between thermal dynamics in the nest environment and its neighbouring air. Here, we placed avian nests and non-incubated eggs inside nest boxes at various air temperatures that ranged from 0.3 to 33.1 °C, both in the field and in laboratory conditions. We measured how the design of the boxes, their compass orientation and their location in more or less urbanized environments affected the surface temperature of nests and eggs. We also assessed whether covering the eggs with lining material influenced their surface temperature. Overall, across all performed tests, we found that the surface temperature of nests and eggs strongly reflected the air temperature measured outside of the nest boxes. While the design of the nest boxes had little influence on the temperature of nests and eggs, orienting the nest boxes to the north or to the west significantly decreased their surface temperature. The presence of lining material also kept eggs slightly warmer when air temperatures were low. Altogether these results suggest that non-incubated eggs are not well protected against extreme air temperatures prior to the onset of incubation. From an evolutionary point of view, producers of ectotherm eggs need therefore to time egg-laying appropriately in order to avoid unfavourable thermal nest environments.

Science policies: How should science funding be allocated? An evolutionary biologists' perspective.

In an ideal world, funding agencies could identify the best scientists and projects and provide them with the resources to undertake these projects. Most scientists would agree that in practice, how funding for scientific research is allocated is far from ideal and likely compromises research quality. We, nine evolutionary biologists from different countries and career stages, provide a comparative summary of our impressions on funding strategies for evolutionary biology across eleven different funding agencies. We also assess whether and how funding effectiveness might be improved. We focused this assessment on 14 elements within four broad categories: (a) topical shaping of science, (b) distribution of funds, (c) application and review procedures, and (d) incentives for mobility and diversity. These comparisons revealed striking among-country variation in those elements, including wide variation in funding rates, the effort and burden required for grant applications, and the extent of emphasis on societal relevance and individual mobility. We use these observations to provide constructive suggestions for the future and urge the need to further gather informed considerations from scientists on the effects of funding policies on science across countries and research fields.

Urban versus forest ecotypes are not explained by divergent reproductive selection.

Increasing urbanization offers a unique opportunity to study adaptive responses to rapid environmental change. Numerous studies have demonstrated phenotypic divergence between urban and rural organisms. However, comparing the direction and magnitude of natural selection between these environments has rarely been attempted. Using seven years of monitoring of great tits (Parus major) breeding in nest-boxes across the city of Montpellier and in a nearby oak forest, we find phenotypic divergence in four morphological and two life-history traits between urban and forest birds. We then measure reproductive selection on these traits, and compare selection between the habitats. Urban birds had significantly smaller morphological features than their rural counterparts, with a shorter tarsus, lower body mass, and smaller wing and tail lengths relative to their overall body size. While urban female tarsus length was under stabilizing selection, and forest males show positive selection for tarsus length and negative selection for body mass, selection gradients were significantly divergent between habitats only for body mass. Urban great tits also had earlier laying dates and smaller clutches. Surprisingly, we found selection for earlier laying date in the forest but not in the city. Conversely, we detected no linear selection on clutch size in the forest, but positive selection on clutch size in the urban habitat. Overall, these results do not support the hypothesis that contemporary reproductive selection explains differences in morphology and life history between urban- and forest-breeding great tits. We discuss how further experimental approaches will help confirm whether the observed divergence is maladaptive while identifying the environmental drivers behind it.

Gene flow does not prevent personality and morphological differentiation between two blue tit populations.

Understanding the causes and consequences of population phenotypic divergence is a central goal in ecology and evolution. Phenotypic divergence among populations can result from genetic divergence, phenotypic plasticity or a combination of the two. However, few studies have deciphered these mechanisms for populations geographically close and connected by gene flow, especially in the case of personality traits. In this study, we used a common garden experiment to explore the genetic basis of the phenotypic divergence observed between two blue tit (Cyanistes caeruleus) populations inhabiting contrasting habitats separated by 25 km, for two personality traits (exploration speed and handling aggression), one physiological trait (heart rate during restraint) and two morphological traits (tarsus length and body mass). Blue tit nestlings were removed from their population and raised in a common garden for up to 5 years. We then compared adult phenotypes between the two populations, as well as trait-specific Qst and Fst . Our results revealed differences between populations similar to those found in the wild, suggesting a genetic divergence for all traits. Qst -Fst comparisons revealed that the trait divergences likely result from dissimilar selection patterns rather than from genetic drift. Our study is one of the first to report a Qst -Fst comparison for personality traits and adds to the growing body of evidence that population genetic divergence is possible at a small scale for a variety of traits including behavioural traits.

Current spring warming as a driver of selection on reproductive timing in a wild passerine.

Evolutionary adaptation as a response to climate change is expected for fitness-related traits affected by climate and exhibiting genetic variance. Although the relationship between warmer spring temperature and earlier timing of reproduction is well documented, quantifications and predictions of the impact of global warming on natural selection acting on phenology in wild populations remain rare. If global warming affects fitness in a similar way across individuals within a population, or if fitness consequences are independent of phenotypic variation in key-adaptive traits, then no evolutionary response is expected for these traits. Here, we quantified the selection pressures acting on laying date during a 24-year monitoring of blue tits in southern Mediterranean France, a hot spot of climate warming. We explored the temporal fluctuation in annual selection gradients and we determined its temperature-related drivers. We first investigated the month-specific warming since 1970 in our study site and tested its influence on selection pressures, using a model averaging approach. Then, we quantified the selection strength associated with temperature anomalies experienced by the blue tit population. We found that natural selection acting on laying date significantly fluctuated both in magnitude and in sign across years. After identifying a significant warming in spring and summer, we showed that warmer daily maximum temperatures in April were significantly associated with stronger selection pressures for reproductive timing. Our results indicated an increase in the strength of selection by 46% for every +1°C anomaly. Our results confirm the general assumption that recent climate change translates into strong selection favouring earlier breeders in passerine birds. Our findings also suggest that differences in fitness among individuals varying in their breeding phenology increase with climate warming. Such climate-driven influence on the strength of directional selection acting on laying date could favour an adaptive response in this trait, since it is heritable.

Delayed phenology and reduced fitness associated with climate change in a wild hibernator.

The most commonly reported ecological effects of climate change are shifts in phenologies, in particular of warmer spring temperatures leading to earlier timing of key events. Among animals, however, these reports have been heavily biased towards avian phenologies, whereas we still know comparatively little about other seasonal adaptations, such as mammalian hibernation. Here we show a significant delay (0.47 days per year, over a 20-year period) in the hibernation emergence date of adult females in a wild population of Columbian ground squirrels in Alberta, Canada. This finding was related to the climatic conditions at our study location: owing to within-individual phenotypic plasticity, females emerged later during years of lower spring temperature and delayed snowmelt. Although there has not been a significant annual trend in spring temperature, the date of snowmelt has become progressively later owing to an increasing prevalence of late-season snowstorms. Importantly, years of later emergence were also associated with decreased individual fitness. There has consequently been a decline in mean fitness (that is, population growth rate) across the past two decades. Our results show that plastic responses to climate change may be driven by climatic trends other than increasing temperature, and may be associated with declines in individual fitness and, hence, population viability.

Disentangling drivers of reproductive performance in urban great tits: a food supplementation experiment.

Worldwide urban expansion induces degradation of the natural environment, resulting in new constraints in terms of breeding sites, anthropogenic disturbances as well as food resources. The alteration of resource abundance and type may induce non-adaptive investments in reproduction from urban dwellers. Food availability and quality have been identified as potential drivers of the decline in passerine body mass and fledging success in urbanized landscapes, particularly if birds misinterpret cues of food abundance used to adjust their reproductive investment. In a previous study, we demonstrated in urban great tits, Parus major, that highly preferred larger cavities have larger clutches with lower breeding success, leading to a maladaptive breeding investment. Previous studies also showed that urban great tits are smaller or thinner than rural ones, both at nestling and adult stages. Here, we present the results of a food-supplementation experiment to examine whether food resources mediate this maladaptive breeding investment and constrain the reproductive performance of this urban bird population. We predicted higher performance in food-supplemented broods, especially in larger cavities, and stronger effects of the supplementation in more artificialized territories. Surprisingly, we found that food-supplemented nestlings and their parents had lower body mass and condition, especially in areas with more pedestrians. Supplementation was also associated with lower nestling survival until fledging in places that presented lower levels of naturalness, independently of cavity size. This work highlights a lack of knowledge on avian feeding behaviour in cities, a key element for understanding how breeding performance is affected by human presence and habitat naturalness.

Beyond DNA: integrating inclusive inheritance into an extended theory of evolution.

Many biologists are calling for an 'extended evolutionary synthesis' that would 'modernize the modern synthesis' of evolution. Biological information is typically considered as being transmitted across generations by the DNA sequence alone, but accumulating evidence indicates that both genetic and non-genetic inheritance, and the interactions between them, have important effects on evolutionary outcomes. We review the evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, and outline methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations. These issues have implications for diverse areas, from the question of missing heritability in human complex-trait genetics to the basis of major evolutionary transitions.