Season-specific genetic variation underlies early-life migration in a partially migratory bird.

Eco-evolutionary responses to environmentally induced selection fundamentally depend on magnitudes of genetic variation underlying traits that facilitate population persistence. Additive genetic variances and associated heritabilities can vary across environmental conditions, especially for labile phenotypic traits expressed through early life. However, short-term seasonal dynamics of genetic variances are rarely quantified in wild populations, precluding inference on eco-evolutionary outcomes in seasonally dynamic systems. This limitation applies to seasonal migration versus residence, constituting one key trait where rapid microevolution could rescue partially migratory populations from changing seasonal environments. We fitted novel quantitative genetic 'capture-recapture animal models' to multi-generational pedigree and year-round resighting data from 11 cohorts of European shags (Gulosus aristotelis), to estimate season-specific additive genetic variances in liabilities to migrate, and in resulting expression of migration, in juveniles' first autumn and winter. We demonstrate non-negligible genetic variation underlying early-life migration, with twice as large additive genetic variances and heritabilities in autumn than winter. Since early-life survival selection on migration typically occurs in winter, highest genetic variation and strongest selection are seasonally desynchronized. Our results reveal complex within- and among-year dynamics of early-life genetic and phenotypic variation, demonstrating that adequate inference of eco-evolutionary outcomes requires quantifying microevolutionary potential on appropriate scales and seasonal timeframes.

Early-life variation in migration is subject to strong fluctuating survival selection in a partially migratory bird.

Population dynamic and eco-evolutionary responses to environmental variation and change fundamentally depend on combinations of within- and among-cohort variation in the phenotypic expression of key life-history traits, and on corresponding variation in selection on those traits. Specifically, in partially migratory populations, spatio-seasonal dynamics depend on the degree of adaptive phenotypic expression of seasonal migration versus residence, where more individuals migrate when selection favours migration. Opportunity for adaptive (or, conversely, maladaptive) expression could be particularly substantial in early life, through the initial development of migration versus residence. However, within- and among-cohort dynamics of early-life migration, and of associated survival selection, have not been quantified in any system, preventing any inference on adaptive early-life expression. Such analyses have been precluded because data on seasonal movements and survival of sufficient young individuals, across multiple cohorts, have not been collected. We undertook extensive year-round field resightings of 9359 colour-ringed juvenile European shags Gulosus aristotelis from 11 successive cohorts in a partially migratory population. We fitted Bayesian multi-state capture-mark-recapture models to quantify early-life variation in migration versus residence and associated survival across short temporal occasions through each cohort's first year from fledging, thereby quantifying the degree of adaptive phenotypic expression of migration within and across years. All cohorts were substantially partially migratory, but the degree and timing of migration varied considerably within and among cohorts. Episodes of strong survival selection on migration versus residence occurred both on short timeframes within years, and cumulatively across entire first years, generating instances of instantaneous and cumulative net selection that would be obscured at coarser temporal resolutions. Further, the magnitude and direction of selection varied among years, generating strong fluctuating survival selection on early-life migration across cohorts, as rarely evidenced in nature. Yet, the degree of migration did not strongly covary with the direction of selection, indicating limited early-life adaptive phenotypic expression. These results reveal how dynamic early-life expression of and selection on a key life-history trait, seasonal migration, can emerge across seasonal, annual, and multi-year timeframes, yet be substantially decoupled. This restricts the potential for adaptive phenotypic, microevolutionary, and population dynamic responses to changing seasonal environments.

Hierarchical Variation in Phenotypic Flexibility across Timescales and Associated Survival Selection Shape the Dynamics of Partial Seasonal Migration.

AbstractPopulation responses to environmental variation ultimately depend on within-individual and among-individual variation in labile phenotypic traits that affect fitness and resulting episodes of selection. Yet complex patterns of individual phenotypic variation arising within and between time periods, as well as associated variation in selection, have not been fully conceptualized or quantified. We highlight how structured patterns of phenotypic variation in dichotomous threshold traits can theoretically arise and experience varying forms of selection, shaping overall phenotypic dynamics. We then fit novel multistate models to 10 years of band-resighting data from European shags to quantify phenotypic variation and selection in a key threshold trait underlying spatioseasonal population dynamics: seasonal migration versus residence. First, we demonstrate substantial among-individual variation alongside substantial between-year individual repeatability in within-year phenotypic variation ("flexibility"), with weak sexual dimorphism. Second, we demonstrate that between-year individual variation in within-year phenotypes ("supraflexibility") is structured and directional, consistent with the threshold trait model. Third, we demonstrate strong survival selection on within-year phenotypes-and hence on flexibility-that varies across years and sexes, including episodes of disruptive selection representing costs of flexibility. By quantitatively combining these results, we show how supraflexibility and survival selection on migratory flexibility jointly shape population-wide phenotypic dynamics of seasonal movement.

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.

Can attraction to and competition for high-quality habitats shape breeding propensity?

In many animal species, sexually mature individuals may skip breeding opportunities despite a likely negative impact on fitness. In spatio-temporally heterogeneous environments, habitat selection theory predicts that individuals select habitats where fitness prospects are maximized. Individuals are attracted to high-quality habitat patches where they compete for high-quality breeding sites. Since failures in contests to secure a site may prevent individuals from breeding, we hypothesized that attraction to and competition for high-quality habitats could shape breeding propensity. Under this hypothesis, we predicted the two following associations between breeding propensity and two key population features. (1) When mean habitat quality in the population increases in multiple patches such that availability of high-quality sites increases across the population, the resulting decrease in competition should positively affect breeding propensity. (2) When the number of individuals increases in the population, the resulting increase in competitors should negatively affect breeding propensity (negative density dependence). Using long-term data from kittiwakes Rissa tridactyla, we checked the prerequisite of prediction (1), that availability of high-quality sites is positively associated with current mean habitat quality in the population (represented by breeding success). We then applied integrated population modelling to quantify annual fluctuations in population mean breeding success, breeding propensity and number of individuals by breeding status (pre-breeders, breeders, skippers and immigrants), and tested our predictions. Our results showed that breeding propensity acts as an important driver of population growth. As expected, breeding propensity was positively associated with preceding mean habitat quality in the population, and negatively with the number of competitors. These relationships varied depending on breeding status, which likely reflects status dependence in competitive ability. These findings highlight the importance of competition for high-quality breeding sites in shaping breeding propensity. Thereby, we draw attention towards alternative and complementary explanations to more standard considerations regarding the energetic cost of reproduction, and point to possible side effects of habitat selection behaviours on individual life histories and population dynamics.

Modelling the responses of partially migratory metapopulations to changing seasonal migration rates: From theory to data.

Among-individual and within-individual variation in expression of seasonal migration versus residence is widespread in nature and could substantially affect the dynamics of partially migratory metapopulations inhabiting seasonally and spatially structured environments. However, such variation has rarely been explicitly incorporated into metapopulation dynamic models for partially migratory systems. We, therefore, lack general frameworks that can identify how variable seasonal movements, and associated season- and location-specific vital rates, can control system persistence. We constructed a novel conceptual framework that captures full-annual-cycle dynamics and key dimensions of metapopulation structure for partially migratory species inhabiting seasonal environments. We conceptualize among-individual variation in seasonal migration as two variable vital rates: seasonal movement probability and associated movement survival probability. We conceptualize three levels of within-individual variation (i.e. plasticity), representing seasonal or annual variation in seasonal migration or lifelong fixed strategies. We formulate these concepts as a general matrix model, which is customizable for diverse life-histories and seasonal landscapes. To illustrate how variable seasonal migration can affect metapopulation growth rate, demographic structure and vital rate elasticities, we parameterize our general models for hypothetical short- and longer-lived species. Analyses illustrate that elasticities of seasonal movement probability and associated survival probability can sometimes equal or exceed those of vital rates typically understood to substantially influence metapopulation dynamics (i.e. seasonal survival probability or fecundity), that elasticities can vary non-linearly, and that metapopulation outcomes depend on the level of within-individual plasticity. We illustrate how our general framework can be applied to evaluate the consequences of variable and changing seasonal movement probability by parameterizing our models for a real partially migratory metapopulation of European shags Gulosus aristotelis assuming lifelong fixed strategies. Given observed conditions, metapopulation growth rate was most elastic to breeding season adult survival of the resident fraction in the dominant population. However, given doubled seasonal movement probability, variation in survival during movement would become the primary driver of metapopulation dynamics. Our general conceptual and matrix model frameworks, and illustrative analyses, thereby highlight complex ways in which structured variation in seasonal migration can influence dynamics of partially migratory metapopulations, and pave the way for diverse future theoretical and empirical advances.

Episodes of opposing survival and reproductive selection cause strong fluctuating selection on seasonal migration versus residence.

Quantifying temporal variation in sex-specific selection on key ecologically relevant traits, and quantifying how such variation arises through synergistic or opposing components of survival and reproductive selection, is central to understanding eco-evolutionary dynamics, but rarely achieved. Seasonal migration versus residence is one key trait that directly shapes spatio-seasonal population dynamics in spatially and temporally varying environments, but temporal dynamics of sex-specific selection have not been fully quantified. We fitted multi-event capture-recapture models to year-round ring resightings and breeding success data from partially migratory European shags (Phalacrocorax aristotelis) to quantify temporal variation in annual sex-specific selection on seasonal migration versus residence arising through adult survival, reproduction and the combination of both (i.e. annual fitness). We demonstrate episodes of strong and strongly fluctuating selection through annual fitness that were broadly synchronized across females and males. These overall fluctuations arose because strong reproductive selection against migration in several years contrasted with strong survival selection against residence in years with extreme climatic events. These results indicate how substantial phenotypic and genetic variation in migration versus residence could be maintained, and highlight that biologically important fluctuations in selection may not be detected unless both survival selection and reproductive selection are appropriately quantified and combined.

Strong survival selection on seasonal migration versus residence induced by extreme climatic events.

Elucidating the full eco-evolutionary consequences of climate change requires quantifying the impact of extreme climatic events (ECEs) on selective landscapes of key phenotypic traits that mediate responses to changing environments. Episodes of strong ECE-induced selection could directly alter population composition, and potentially drive micro-evolution. However, to date, few studies have quantified ECE-induced selection on key traits, meaning that immediate and longer-term eco-evolutionary implications cannot yet be considered. One widely expressed trait that allows individuals to respond to changing seasonal environments, and directly shapes spatio-seasonal population dynamics, is seasonal migration versus residence. Many populations show considerable among-individual phenotypic variation, resulting in 'partial migration'. However, variation in the magnitude of direct survival selection on migration versus residence has not been rigorously quantified, and empirical evidence of whether seasonal ECEs induce, intensify, weaken or reverse such selection is lacking. We designed full annual cycle multi-state capture-recapture models that allow estimation of seasonal survival probabilities of migrants and residents from spatio-temporally heterogeneous individual resightings. We fitted these models to 9 years of geographically extensive year-round resighting data from partially migratory European shags Phalacrocorax aristotelis. We thereby quantified seasonal and annual survival selection on migration versus residence across benign and historically extreme non-breeding season (winter) conditions, and tested whether selection differed between females and males. We show that two of four observed ECEs, defined as severe winter storms causing overall low survival, were associated with very strong seasonal survival selection against residence. These episodes dwarfed the weak selection or neutrality evident otherwise, and hence caused selection through overall annual survival. The ECE that caused highest overall mortality and strongest selection also caused sex-biased mortality, but there was little overall evidence of sex-biased selection on migration versus residence. Our results imply that seasonal ECEs and associated mortality can substantially shape the landscape of survival selection on migration versus residence. Such ECE-induced phenotypic selection will directly alter migrant and resident frequencies, and thereby alter immediate spatio-seasonal population dynamics. Given underlying additive genetic variation, such ECEs could potentially cause micro-evolutionary changes in seasonal migration, and thereby cause complex eco-evolutionary population responses to changing seasonal environments.

Among-individual and within-individual variation in seasonal migration covaries with subsequent reproductive success in a partially migratory bird.

Within-individual and among-individual variation in expression of key environmentally sensitive traits, and associated variation in fitness components occurring within and between years, determine the extents of phenotypic plasticity and selection and shape population responses to changing environments. Reversible seasonal migration is one key trait that directly mediates spatial escape from seasonally deteriorating environments, causing spatio-seasonal population dynamics. Yet, within-individual and among-individual variation in seasonal migration versus residence, and dynamic associations with subsequent reproductive success, have not been fully quantified. We used novel capture-mark-recapture mixture models to assign individual European shags (Phalacrocorax aristotelis) to 'resident', 'early migrant', or 'late migrant' strategies in two consecutive years, using year-round local resightings. We demonstrate substantial among-individual variation in strategy within years, and directional within-individual change between years. Furthermore, subsequent reproductive success varied substantially among strategies, and relationships differed between years; residents and late migrants had highest success in the 2 years, respectively, matching the years in which these strategies were most frequently expressed. These results imply that migratory strategies can experience fluctuating reproductive selection, and that flexible expression of migration can be partially aligned with reproductive outcomes. Plastic seasonal migration could then potentially contribute to adaptive population responses to currently changing forms of environmental seasonality.

Correction to: Insights on dispersal and recruitment paradigms: sex- and age-dependent variations in a nomadic breeder.

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Insights on dispersal and recruitment paradigms: sex- and age-dependent variations in a nomadic breeder.

Sex- and age-dependence in recruitment and dispersal are often explained by costs arising from competition for holding a breeding territory over the years-a typical feature of species living in stable habitats. For instance, long-lived birds with male territoriality often exhibit large variation in recruitment age and higher dispersal in females and young individuals. As a corollary, we expected that species with ephemeral habitat suitability, and hence nomadic breeding, would show weak age- and sex-dependence in dispersal and low variation in recruitment age, because territory ownership is not maintained over the years. In addition, the higher cost of reproduction in females might not be (over)compensated for by costs of territoriality in males. Accordingly, females would recruit later than males. We explored these variations using multievent capture-recapture models over 13 years, 3479 (2392 sexed) slender-billed gulls (Chroicocephalus genei) and 45 colony sites along the French Mediterranean coast. As expected, variability in recruitment age was low with males recruiting earlier than females. Nonetheless, dispersal in and out of the study area decreased with age and was slightly higher in males than in females. Decreased dispersal with age might result from foraging benefits associated with increased spatial familiarity. Higher dispersal in males might be explained by a male-biased sex ratio or higher philopatry benefits in females (arising from their higher cost of reproduction). Sex- and age-dependent dispersal and recruitment may thus occur in the absence of year-to-year breeding territory ownership, which stresses the importance of considering other processes in shaping recruitment and dispersal patterns.

Breeding habitat selection across spatial scales: is grass always greener on the other side?

Habitat selection theory predicts that natural selection should favor mechanisms allowing individuals to choose habitats associated with the highest fitness prospects. However, identifying sources of information on habitat quality that individuals use to choose their breeding habitat has proved to be difficult. It has also proven difficult to identify dispersal costs that prevent individuals from joining the highest-quality sites. A synthesis that integrates dispersal costs and habitat selection mechanisms across space has remained elusive. Because costs of dispersal are generally distance-dependent, we suggest that a habitat selection strategy of sequential proximity search (SPS) can be favored by natural selection. This strategy requires that animals make decisions at multiple scales: whether to stay or leave the previous breeding site, depending on reproductive success; then, if dispersal is chosen, use information on neighborhood habitat quality to decide whether to stay in the neighborhood or leave, expanding the search area until the nearest suitable site is chosen. SPS minimizes distance-dependent dispersal costs while maximizing benefits of gaining a better habitat. We found evidence of breeding dispersal behavior consistent with this strategy in a kittiwake population stratified into a spatial hierarchy from colonies to nest sites. We used a mixed sequential regression model to study dispersal decisions, indexed by breeding dispersal movement, of 2,558 individuals over 32 yr. Scale-dependent dispersal propensities of kittiwakes varied according to breeding status, breeding experience, sex and individual identity. We suggest that distance-dependent dispersal costs result from strong competition among kittiwakes for nest sites. Individual decisions regarding dispersal (whether to leave or not, and where to go) depend on nesting habitat quality as well as the competitive ability required to keep territory ownership in a previous site, or to acquire a new site; this ability varies according to distance between sites and individual characteristics. Additional studies are needed to establish the generality of SPS in habitat selection.

Additive genetic and environmental variation interact to shape the dynamics of seasonal migration in a wild bird population.

Dissecting joint micro-evolutionary and plastic responses to environmental perturbations requires quantifying interacting components of genetic and environmental variation underlying expression of key traits. This ambition is particularly challenging for phenotypically discrete traits where multiscale decompositions are required to reveal nonlinear transformations of underlying genetic and environmental variation into phenotypic variation, and when effects must be estimated from incomplete field observations. We devised a joint multistate capture-recapture and quantitative genetic animal model, and fitted this model to full-annual-cycle resighting data from partially-migratory European shags (${Gulosus~{}aristotelis}$) to estimate key components of genetic, environmental and phenotypic variance in the ecologically critical discrete trait of seasonal migration versus residence. We demonstrate non-negligible additive genetic variance in latent liability for migration, resulting in detectable micro-evolutionary responses following two episodes of strong survival selection. Further, liability-scale additive genetic effects interacted with substantial permanent individual and temporary environmental effects to generate complex nonadditive effects on expressed phenotypes, causing substantial intrinsic gene-by-environment interaction variance on the phenotypic scale. Our analyses therefore reveal how temporal dynamics of partial seasonal migration arise from combinations of instantaneous micro-evolution and within-individual phenotypic consistency, and highlight how intrinsic phenotypic plasticity could expose genetic variation underlying discrete traits to complex forms of selection.

Properties of phenotypic plasticity in discrete threshold traits.

Forms of phenotypic plasticity in key traits, and forms of selection on and genetic variation in such plasticity, fundamentally underpin phenotypic, population dynamic, and evolutionary responses to environmental variation and directional change. Accordingly, numerous theoretical and empirical studies have examined properties and consequences of plasticity, primarily considering traits that are continuously distributed on observed phenotypic scales with linear reaction norms. However, many environmentally sensitive traits are expressed as discrete alternative phenotypes and are appropriately characterized as quantitative genetic threshold traits. Here, we highlight that forms of phenotypic plasticity, genetic variation, and inheritance in plasticity, and outcomes of selection on plasticity, could differ substantially between threshold traits and continuously distributed traits (as are typically considered). We thereby highlight theoretical developments that are required to rationalize and predict phenotypic and microevolutionary dynamics involving plastic threshold traits, and outline how intrinsic properties of such traits could provide relatively straightforward explanations for apparently idiosyncratic observed patterns of phenotypic variation. We summarize how key quantitative genetic parameters underlying threshold traits can be estimated, and thereby set the scene for embedding dynamic discrete traits into theoretical and empirical understanding of the role of plasticity in driving phenotypic, population, and evolutionary responses to environmental variation and change.

Conceptualizing the evolutionary quantitative genetics of phenological life-history events: Breeding time as a plastic threshold trait.

Successfully predicting adaptive phenotypic responses to environmental changes, and predicting resulting population outcomes, requires that additive genetic (co)variances underlying microevolutionary and plastic responses of key traits are adequately estimated on appropriate quantitative scales. Such estimation in turn requires that focal traits, and their underlying quantitative genetic architectures, are appropriately conceptualized. Here, we highlight that directly analyzing observed phenotypes as continuously distributed quantitative traits can potentially generate biased and misleading estimates of additive genetic variances and individual-by-environment and gene-by-environment interactions, and hence of forms of plasticity and genetic constraints, if in fact the underlying biology is best conceptualized as an environmentally sensitive threshold trait. We illustrate this scenario with particular reference to the key phenological trait of seasonal breeding date, which has become a focus for quantifying joint microevolutionary, plastic, and population responses to environmental change, but has also become a focus for highlighting that predicted adaptive outcomes are not always observed. Specifically, we use simple simulations to illustrate how potentially misleading inferences on magnitudes of additive genetic variance, and forms of environmental interactions, can arise by directly analyzing observed breeding dates if the transition to breeding in fact represents a threshold trait with latent-scale plasticity. We summarize how existing and new datasets could be (re)analyzed, potentially providing new insights into how critical microevolutionary and plastic phenological responses to environmental variation and change can arise and be constrained.