Climate change and the optimal arrival of migratory birds

Recent climate change has sparked an interest in the timing of biological events, which is a general problem in life-history evolution. Reproduction in many organisms breeding in seasonal environments, e.g. migratory birds, is dependent on the exploitation of a short but rich food supply. If the seasonal timing of the food peak advances owing to climate change, then one would expect the bird to track those changes, hence, initiate migration and breeding earlier. However, when there is competition for territories and a risk of pre-breeding mortality, the optimal response to a shifting food distribution is no longer obvious. We develop a theoretical model to study how the optimal arrival time depends on the mean and variance of the food distribution, the degree of competition for territories and the risk of mortality. In general, the optimal shift in arrival date should never be as extreme as the shift in food peak date. Our results also show that we should expect the high variation of trends in arrival date observed among migratory birds, even if migration and information about climate change were unconstrained.     

Fine‐scale temporal adaptation within a salmonid population: mechanism and consequences

We demonstrate a clear example of local adaptation of seasonal timing of spawning and embryo development. The consequence is a population of pink salmon that is segmented into spawning groups that use the same limited habitat. We synthesize published observations with results of new analyses to demonstrate that genetic variation of these traits results in survival differentials related to that variation, and that density‐dependent embryo mortality and seasonally variable juvenile mortality are a mechanism of selection. Most examples of local adaptation in natural systems depend on observed correlations between environments and fitness traits, but do not fully demonstrate local adaptation: that the trait is genetically determined, exhibits different fitness in common environments or across different environments, and its variation is mechanistically connected to fitness differences. The geographic or temporal scales of local adaptation often remain obscure. Here, we show that heritable, fine‐scale differences of timing of reproductive migration in a pink salmon (Oncorhynchus gorbuscha) resulted in temporal structure that persisted several generations; the differences enable a density‐dependent population to pack more spawners into limited spawning habitat, that is, enhance its fitness. A balanced trade‐off of survivals results because embryos from early‐migrating fish have a lower freshwater survival (harsh early physical conditions and disturbance by late spawners), but emigrant fry from late‐migrating fish have lower marine survivals (timing of their vernal emergence into the estuarine environment). Such fine‐scale local adaptations increase the genetic portfolio of the populations and may provide a buffer against the impacts of climate change.     

Annual routines of non-migratory birds: optimal moult strategies

In a periodically changing environment it is important for animals to properly time the major events of their life in order to maximise their lifetime fitness. For a non-migratory bird the timing of breeding and moult are thought to be the most crucial. We develop a state-dependent optimal annual routine model that incorporates explicit density dependence in the food supply. In the model the birds' decisions depend on the time of year, their energy reserves, breeding status, experience, and the quality of two types of feathers (outer and inner primaries). Our model predicts that, under a seasonal environment, feathers with large effects on flight ability, higher abrasion rate and lower energetic cost of moult should be moulted closer to the winter (i.e. later) than those with the opposite attributes. Therefore, we argue that the sequence of moult may be an adaptive response to the problem of optimal timing of moult of differing feathers within the same feather tract. The model also predicts that environmental seasonality greatly affects optimal annual routines. Under high seasonality birds breed first then immediately moult, whereas under low seasonality an alternation occurs between breeding and moulting some of the feathers in one year and having a complete moult but no breeding in the other year. Increasing food abundance has a similar effect.     

Hatching date vs laying date: what should we look at to study avian optimal timing of reproduction?

Most research conducted on optimal timing of reproduction in birds has traditionally considered laying date of the first egg as the event that needs to be related to the time of maximum food availability. However, what (most) birds need to time with the seasonal peak of food availability is the moment of maximum food demand of their nestlings, which is more tightly related with hatching date than with laying date. After initiating egg laying, birds still have some opportunities to adjust the time of highest food demand, as during the several days elapsed between laying of the first egg until hatching, more precise cues will become available to birds in order to make a more accurate match with food availability. I provide an overview of the suite of mechanisms available to birds for shortening or enlarging the interval between laying and hatching date, which include laying gaps, adjustment of clutch size, variation in onset and intensity of incubation, and differential investment on eggs. Then I illustrate with an example the extent to which birds can adjust hatching dates after egg laying. I argue that birds should more accurately time hatching date rather than laying date to maximum food availability on the basis of available cues. Therefore, I suggest that researchers should target on hatching date rather than laying date to better study optimal timing of reproduction in birds. Exploration of responses other than adjusting laying date to changing environmental conditions will surely uncover key aspects of avian reproductive biology and behaviour that have been ignored until now. This is a necessary step towards a better understanding of capacities of organisms to adapt to a changing world in particular, and of fitness consequences of timing of reproduction in general.     

Finding the one: optimal choosiness under sequential mate choice

When mates are encountered sequentially, each encounter involves a decision whether to reject the current suitor and risk not finding a better mate, or to accept them despite their flaws. I provide a flexible framework for modelling optimal choosiness when mate encounters occur unpredictably in time. The model allows for temporal variation in the fitness benefits of mating, including seasonal breeding conditions, accrual of mate search costs, survival of the choosing individual or senescence of gametes. The basic optimality framework can be applied iteratively to obtain mate choice equilibria in dynamically evolving populations. My model predicts that individuals should be choosier when the average rate of mate encounters is high, but that choosiness should decline over time as the likelihood of future mate encounters decreases. When mate encounters are uncertain, there is a trade‐off between reproductive timing and mate choice (the ‘when’ and the ‘who’). Mate choice may be selected against when reproductive timing is highly important (e.g. when breeding conditions show a narrow peak in time). This can even lead to step‐shaped mate choice functions, where individuals abruptly switch from rejecting to accepting all suitors as peak breeding conditions approach. The model contributes to our understanding of why individuals may not express mate preferences, even when there is substantial variation in mate quality.     

Habitat selection by a large herbivore at multiple spatial and temporal scales is primarily governed by food resources

Habitat selection can be considered as a hierarchical process in which animals satisfy their habitat requirements at different ecological scales. Theory predicts that spatial and temporal scales should co‐vary in most ecological processes and that the most limiting factors should drive habitat selection at coarse ecological scales, but be less influential at finer scales. Using detailed location data on roe deer Capreolus capreolus inhabiting the Bavarian Forest National Park, Germany, we investigated habitat selection at several spatial and temporal scales. We tested 1) whether time‐varying patterns were governed by factors reported as having the largest effects on fitness, 2) whether the trade‐off between forage and predation risks differed among spatial and temporal scales and 3) if spatial and temporal scales are positively associated. We analysed the variation in habitat selection within the landscape and within home ranges at monthly intervals, with respect to land‐cover type and proxys of food and cover over seasonal and diurnal temporal scales. The fine‐scale temporal variation follows a nycthemeral cycle linked to diurnal variation in human disturbance. The large‐scale variation matches seasonal plant phenology, suggesting food resources being a greater limiting factor than lynx predation risk. The trade‐off between selection for food and cover was similar on seasonal and diurnal scale. Habitat selection at the different scales may be the consequence of the temporal variation and predictability of the limiting factors as much as its association with fitness. The landscape of fear might have less importance at the studied scale of habitat selection than generally accepted because of the predator hunting strategy. Finally, seasonal variation in habitat selection was similar at the large and small spatial scales, which may arise because of the marked philopatry of roe deer. The difference is supposed to be greater for wider ranging herbivores.     

The effect of climate change on the correlation between avian life-history traits

The ultimate reason why birds should advance their phenology in response to climate change is to match the shifting phenology of underlying levels of the food chain. In a seasonal environment, the timing of food abundance is one of the crucial factors to which birds should adapt their timing of reproduction. They can do this by shifting egg‐laying date (LD), and also by changing other life‐history characters that affect the period between laying of the eggs and hatching of the chicks. In a long‐term study of the migratory Pied Flycatcher, we show that the peak of abundance of nestling food (caterpillars) has advanced during the last two decades, and that the birds advanced their LD. LD strongly correlates with the timing of the caterpillar peak, but in years with an early food peak the birds laid their eggs late relative to this food peak. In such years, the birds advance their hatching date by incubating earlier in the clutch and reducing the interval between laying the last egg to hatching of the first egg, thereby partly compensating for their relative late LD. Paradoxically, they also laid larger clutches in the years with an early food peak, and thereby took more time to lay (i.e. one egg per day). Clutch size therefore declined more strongly with LD in years with an early food peak. This stronger response is adaptive because the fitness of an egg declined more strongly with date in early than in late years. Clearly, avian life‐history traits are correlated and Pied Flycatchers apparently optimize over the whole complex of the traits including LD, clutch size and the onset of incubation. Climate change will lead to changing selection pressures on this complex of traits and presumably the way they are correlated.     

Environmental and genetic influences on the germination of Arabidopsis thaliana in the field

Seasonal germination timing strongly influences lifetime fitness and can affect the ability of plant populations to colonize and persist in new environments. To quantify the influence of seasonal environmental factors on germination and to test whether pleiotropy or close linkage are significant constraints on the evolution of germination in different seasonal conditions, we dispersed novel recombinant genotypes of Arabidopsis thaliana into two geographic locations. To decouple the photoperiod during seed maturation from the postdispersal season that maternal photoperiod predicts, replicates of recombinant inbred lines were grown under short days and long days under controlled conditions, and their seeds were dispersed during June in Kentucky (KY) and during June and November in Rhode Island (RI). We found that postdispersal seasonal conditions influenced germination more strongly than did the photoperiod during seed maturation. Genetic variation was detected for germination responses to all environmental factors. Transgressive segregation created novel germination phenotypes, revealing a potential contribution of hybridization of ecotypes to the evolution of germination. A genetic trade-off in germination percentage across sites indicated that determinants of fitness at or before the germination stage may constrain the geographic range that a given genotype can inhabit. However, germination timing exhibited only weak pleiotropy across treatments, suggesting that different sets of genes contribute to variation in germination behavior in different seasonal conditions and geographic locations. Thus, the genetic potential exists for rapid evolution of appropriate germination responses in novel environments, facilitating colonization across a broad geographic range.     

Hard and soft selection on phenology through seasonal shifts in the general and social environments: A study on plant emergence time

The timing of transition out of one life‐history phase determines where in the seasonal succession of environments the next phase is spent. Shifts in the general environment (e.g., seasonal climate) affect the expected fitness for particular transition dates. Variation in transition date also leads to temporal variation in the social environment. For instance, early transition may confer a competitive advantage over later individuals. If so, the social environment will impose frequency‐ and density‐dependent selection components. In effect, the general environment imposes hard selection, whereas the social environment imposes soft selection on phenology. We examined hard and soft selection on seedling emergence time in an experiment on Brassica rapa. In monoculture (uniform social environment), early emergence results in up to a 1.5‐fold increase in seed production. In bicultures (heterogeneous social environment), early‐emerging plants capitalized on their head start, suppressing their late neighbors and increasing their fitness advantage to as much as 38‐fold, depending on density. We devised a novel adaptation of contextual analysis to partition total selection (i.e., cov(ω, z)) into the hard and soft components. Hard and soft components had similar strengths at low density, whereas soft selection was five times stronger than hard at high density.     

Seasonality of births in Homo sapiens in pre-industrial Finland: maximisation of offspring survivorship?

We examined the seasonal variation in human birth and infant survival rates in pre-modern Finland. If survival probabilities of children born during different seasons of the year differ and if timing of reproduction has been affected by natural selection, periodic variation in environment could have led to reproduction during the season of best infant survival expectations. Significant seasonal variation in both birth rate and survival probability was found, but the monthly birth and survival rates of newborn were uncorrelated. Hence, if there was any tendency to maximise the reproductive success, increase in some other component of fitness than the infant survival was probably targeted. The effect of major holidays on the birth rate was proved to be notable, suggesting that although the basis for seasonal variation in birth rate was biological, sociocultural factors had an impact on the timing of reproduction in humans. The overall mortality of infant boys exceeded that of infant girls in all seasons. This difference was smallest during the time of best food supplies, indicating that the development of males was less buffered against environmental disturbances than that of females.     

The selective advantage of reaction norms for environmental tolerance

A tolerance curve defines the dependence of a genotype's fitness on the state of an environmental gradient. It can be characterized by a mode (the genotype's optimal environment) and a width (the breadth of adaptation). It seems possible that one or both of these characters can be modified in an adaptive manner, at least partially, during development. Thus, we extend the theory of environmental tolerance to include reaction norms for the mode and the width of the tolerance curve. We demonstrate that the selective value of such reaction norms increases with increasing spatial heterogeneity and between-generation temporal variation in the environment and with decreasing within-generation temporal variation. Assuming that the maintenance of a high breadth of adaptation is costly, reaction, norms are shown to induce correlated selection for a reduction in this character. Nevertheless, regardless of the magnitude of the reaction norm, there is a nearly one to one relationship between the optimal breadth of adaptation and the within-generation temporal variation perceived by the organism. This suggests that empirical estimates of the breadth of adaptation may provide a useful index of this type of environmental variation from the organism's point of view.     

Is life‐history buffering or lability adaptive in stochastic environments?

It is commonly thought that temporal fluctuations in demographic parameters should be selected against because of the deleterious impacts variation can have on fitness. A critical underpinning of this prediction is the assumption that changes in environmental conditions map linearly into changes in demographic parameters over time. We detail why this assumption may often break down and why selection should not always favor buffering of demographic parameters against environmental stochasticity. To the contrary, nonlinear relationships between the environment and demographic performance can produce asymmetric temporal variation in demographic parameters that actually enhances fitness. We extend this result to structured populations using simulation and show that 'demographic lability' rather than 'buffering' may be adaptive, particularly in organisms with low juvenile or adult survival. Finally, we review previous ecological work, and indicate cases where 'demographic lability' may be adaptive, then conclude by identifying research that is needed to develop a theory of life-history evolution that encompasses both demographic buffering and lability.     

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

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

Foraging behavior in stochastic environments

How do temporally stochastic environments affect risk sensitivity in foraging behavior? We build a simple model of foraging under predation risks in stochastic environments, where the environments change over generations. We analyze the effects of stochastic environments on risk sensitivity of foraging animals by means of the difference between the geometric mean fitness and the arithmetic mean fitness. We assume that foraging is associated with predation risks whereas resting in the nest is safe because it is free of predators. In each generation, two different environments with given food amounts and predation risks occur with a certain probability. The geometric mean optimum is independent of food amounts. In most cases of stochastic environments, risk-averse tendency is increased, but in some limited conditions, more risk-prone behavior is favored. Specifically, risk-prone tendency is increased when the variation in food amount increases. Our results imply that the optimal behavior depends on the probability distribution of environmental effects under all selection regimes.     

Pre-laying climatic cues can time reproduction to optimally match offspring hatching and ice conditions in an Arctic marine bird

Individuals breeding in seasonal environments are under strong selection to time reproduction to match offspring demand and the quality of the post-natal environment. Timing requires both the ability to accurately interpret the appropriate environmental cues, and the flexibility to respond to inter-annual variation in these cues. Determining which cues are linked to reproductive timing, what these cues are predicting and understanding the fitness consequences of variation in timing, is therefore of paramount interest to evolutionary and applied ecologists, especially in the face of global climate change. We investigated inter-annual relationships between climatic variation and the timing of reproduction in Canada’s largest breeding population of Arctic common eiders (Somateria mollissima) in East Bay, Nunavut. Warmer spring temperatures predicted both earlier mean annual laying dates and the earlier ice-free conditions required by ducklings for post-natal growth. Warmer springs had higher variation in this temperature cue, and the population laying distribution became increasingly positively-skewed in warmer summers, potentially indicating that more low-quality females had the opportunity to commence laying in warmer years. Females that timed laying to match duckling hatching just prior to fully ice-free conditions obtained the highest duckling survival probability. Inter-annual data on repeated breeding attempts revealed that the individuals examined show a similar degree of laying flexibility in response to climatic variation; however, there was significant individual variation in the absolute timing of laying within an average year. This work sheds light on how reproductive timing is related to and influenced by variation in local climate and provides vital information on how climate-related variation in reproductive timing influence a fitness measure in an Arctic species. Results are especially relevant to future work in polar environments given that global climatic changes are predicted to be most intense at high latitudes.     

Environmental uncertainty, autocorrelation and the evolution of survival

Survival is a key fitness component and the evolution of age- and stage-specific patterns in survival is a central question in evolutionary biology. In variable environments, favouring chances of survival at the expense of other fitness components could increase fitness by spreading risk across uncertain conditions, especially if environmental conditions improve in the future. Both the magnitude of environmental variation and temporal autocorrelation in the environment might therefore affect the evolution of survival patterns. Despite this, the influence of temporal autocorrelation on the evolution of survival patterns has not been addressed. Here, we use a trade-off structure which reflects the empirically inspired paradigm of acquisition and allocation of resources to investigate how the evolutionarily stable survival probability is shaped in variable, density-dependent environments. We show that temporal autocorrelation is likely to be an important aspect of environmental variability that contributes to shaping age- and stage-specific patterns of survival probabilities in nature.     

Dealing with stochastic environmental variation in space and time: bet hedging by generalist,specialist, and diversified strategies

Building on previous work, we derive an optimization model for a two-state stochastic environment and evaluate the fitnesses of five reproductive strategies across generations. To do this, we characterize spatiotemporal variation and define grain (=patch) size as the scale of fitness autocorrelation. Fitness functions of environmental condition are Gaussian. The strategies include two specialists on each of the environmental conditions; two generalists that each fare equally well under both conditions, but one (a conservative bet hedger) optimizes the shape of the fitness function; and a diversified bet hedger producing an optimal mix of the two specialists within individual broods. When the environment is primarily in one of the two states, the specialist on that state achieves the highest fitness. In the more interesting situation where the two environments are equally prevalent in the long term, with low-moderate environmental variation, a generalist strategy (that copes with both states well) does best. Higher variation favors diversified bet hedgers, or surprisingly, specialists, depending mainly on whether spatial or temporal variation predominates. These strategies reduce variance in fitness and optimize the distribution of offspring among patches differently: specialists by spreading offspring among many independently varying patches, while diversified bet hedgers put all offspring into a few patches or a single patch. We distinguish features consistent with strategies like diversified bet hedgers that spread risk in time from features linked to strategies like specialists that spread risk in space. Finally, we present testable hypotheses arising from this study and suggest directions for future work.     

Seasonal mortality trends in tree‐feeding insects: a field experiment

Abstract 1. The majority of general life‐history models treat the environment as being invariable through time, even though temporal variation in selective agents could dramatically change the outcomes, e.g. in terms of optimal size and time at maturity. For herbivorous insects, seasonal differences in food quality are reasonably well described, but seasonal dynamics of top‐down selective forces are poorly documented. 2. The present study attempted to quantify seasonal changes in predation risk of folivorous insect larvae in temperate forest habitats. In a series of field experiments, artificial larvae were exposed to predators, and the resulting bird‐inflicted damage was recorded. The trials were repeated regularly throughout the course of two summers. 3. A distinct peak of larval mortality was recorded in mid‐June (the nestling period for most insectivorous passerine birds), after which predation risk declined to a plateau of 20–30% below the peak value. 4. The recorded pattern is interpreted as a consequence of seasonal changes in the number and behaviour of insectivorous birds, and the abundance of alternative food resources for these predators. 5. A quantitative analysis based on field data indicated that considering temporal variation in mortality in life‐history models is crucial for obtaining realistic predictions concerning central life‐history traits, such as final body size in different generations.     

Sex differences in the response to environmental cues regulating seasonal reproduction in birds

Although it is axiomatic that males and females differ in relation to many aspects of reproduction related to physiology, morphology and behaviour, relatively little is known about possible sex differences in the response to cues from the environment that control the timing of seasonal breeding. This review concerns the environmental regulation of seasonal reproduction in birds and how this process might differ between males and females. From an evolutionary perspective, the sexes can be expected to differ in the cues they use to time reproduction. Female reproductive fitness typically varies more as a function of fecundity selection, while male reproductive fitness varies more as a function sexual selection. Consequently, variation in the precision of the timing of egg laying is likely to have more serious fitness consequences for females than for males, while variation in the timing of recrudescence of the male testes and accompanying territory establishment and courtship are likely to have more serious fitness consequences for males. From the proximate perspective, sex differences in the control of reproduction could be regulated via the response to photoperiod or in the relative importance and action of supplementary factors (such as temperature, food supply, nesting sites and behavioural interactions) that adjust the timing of reproduction so that it is in step with local conditions. For example, there is clear evidence in several temperate zone avian species that females require both supplementary factors and long photoperiods in order for follicles to develop, while males can attain full gonadal size based on photoperiodic stimulation alone. The neuroendocrine basis of these sex differences is not well understood, though there are many candidate mechanisms in the brain as well as throughout the entire hypothalamo-pituitary-gonadal axis that might be important.     

Scale-dependent climate signals drive breeding phenology of three seabird species

Breeding at the right time is essential for animals in seasonal climates in order to ensure that the energy demands of reproduction, particularly the nutritional requirements of growing young, coincide with peak food availability. Global climate change is likely to cause shifts in the timing of peak food availability, and in order to adapt successfully to current and future climate change, animals need to be able to adjust the time at which they initiate breeding. Many animals use environmental cues available before the breeding season to predict the seasonal peak in food availability and adjust their phenology accordingly. We tested the hypothesis that regulation of breeding onset should reflect the scale at which organisms perceive their environment by comparing phenology of three seabird species at a North Sea colony. As predicted, the phenology of two dispersive species, black-legged kittiwake ( Rissa tridactyla ) and common guillemot ( Uria aalge ), correlated with a large-scale environmental cue (the North Atlantic Oscillation), whereas a resident species, European shag ( Phalacrocorax aristotelis ), was more affected by local conditions (sea surface temperature) around the colony. Annual mean breeding success was lower in late years for European shags, but not for the other two species. Since correlations among climate patterns at different scales are likely to change in the future, these findings have important implications for how migratory animals can respond to future climate change.