RESUMEN

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.

RESUMEN

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.

Asunto(s)

RESUMEN

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.

Asunto(s)

RESUMEN

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.

Asunto(s)