Long-distance dispersal in the short-distance dispersing house sparrow (Passer domesticus).

The house sparrow (Passer domesticus) is a small passerine known to be highly sedentary. Throughout a 30-year capture-mark-recapture study, we have obtained occasional reports of recoveries far outside our main metapopulation study system, documenting unusually long dispersal distances. Our records constitute the highest occurrence of long-distance dispersal events recorded for this species in Scandinavia. Such long-distance dispersals radically change the predicted distribution of dispersal distances and connectedness for our study metapopulation. Moreover, it reveals a much greater potential for colonization than formerly recorded for the house sparrow, which is an invasive species across four continents. These rare and occasional long-distance dispersal events are challenging to document but may have important implications for the genetic composition of small and isolated populations and for our understanding of dispersal ecology and evolution.

Evolutionary rescue from climate change: male indirect genetic effects on lay-dates and their consequences for population persistence.

Changes in avian breeding phenology are among the most apparent responses to climate change in free-ranging populations. A key question is whether populations will be able to keep up with the expected rates of environmental change. There is a large body of research on the mechanisms by which avian lay-dates track temperature change and the consequences of (mal)adaptation on population persistence. Often overlooked is the role of males, which can influence the lay-date of their mate through their effect on the prelaying environment. We explore how social plasticity causing male indirect genetic effects can help or hinder population persistence when female genes underpinning lay-date and male genes influencing female's timing of reproduction both respond to climate-mediated selection. We extend quantitative genetic moving optimum models to predict the consequences of social plasticity on the maximum sustainable rate of temperature change, and evaluate our model using a combination of simulated data and empirical estimates from the literature. Our results suggest that predictions for population persistence may be biased if indirect genetic effects and cross-sex genetic correlations are not considered and that the extent of this bias depends on sex differences in how environmental change affects the optimal timing of reproduction. Our model highlights that more empirical work is needed to understand sex-specific effects of environmental change on phenology and the fitness consequences for population dynamics. While we discuss our results exclusively in the context of avian breeding phenology, the approach we take here can be generalized to many different contexts and types of social interaction.

Personality traits differentially affect components of reproductive success in a Neotropical poison frog.

Individual reproductive success has several components, including the acquisition of mating partners, offspring production, and offspring survival until adulthood. While the effects of certain personality traits-such as boldness or aggressiveness-on single components of reproductive success are well studied, we know little about the composite and multifaceted effects behavioural traits can have on all the aspects of reproductive success. Behavioural traits positively linked to one component of reproductive success might not be beneficial for other components, and these effects may differ between sexes. We investigated the influence of boldness, aggressiveness, and exploration on the number of mating partners, mating events, and offspring surviving until adulthood in males and females of the Neotropical poison frog Allobates femoralis. Behavioural traits had different-even opposite-effects on distinct components of reproductive success in both males and females. For example, males who displayed high levels of aggressiveness and exploration (or low levels of aggressiveness and exploration) managed to attract high number of mating partners, while males with low levels of boldness, low levels of aggressiveness, and high levels of exploration had the most offspring surviving until adulthood. Our results therefore suggest correlational selection favouring particular combinations of behavioural traits.

The evolutionary ecology of variation in labile traits: selection on its among- and within-individual components.

Closer integration between behavioral ecology and quantitative genetics has resulted in a recent increase in studies partitioning sources of variation in labile traits. Repeatable between-individual differences are commonly documented, and their existence is generally explained using adaptive arguments, implying that selection has shaped variation at the among- and within-individual level. However, predicting the expected pattern of non-adaptive phenotypic variation around an optimal phenotypic value is difficult, hampering our ability to provide quantitative assessments of the adaptive nature of observed patterns of phenotypic variation within a population. We argue that estimating the strength of selection on trait variation among and within individuals provides a way to test adaptive theory concerned with phenotypic variation. To achieve this aim, we describe a nonlinear selection analysis that enables the study of the selective pressures on trait means and their among- and within-individual variation. By describing an integrative approach for studying the strength of selection on phenotypic variation at different levels, we hope to stimulate empirical studies investigating the ecological factors that can shape the repeatability, heritability, and coefficients of variation of labile and other repeatedly expressed traits.

Longitudinal telomere dynamics within natural lifespans of a wild bird.

Telomeres, the nucleotide sequences that protect the ends of eukaryotic chromosomes, shorten with each cell division and telomere loss may be influenced by environmental factors. Telomere length (TL) decreases with age in several species, but little is known about the sources of genetic and environmental variation in the change in TL (∆TL) in wild animals. In this study, we tracked changes in TL throughout the natural lifespan (from a few months to almost 9 years) of free-living house sparrows (Passer domesticus) in two different island populations. TL was measured in nestlings and subsequently up to four times during their lifetime. TL generally decreased with age (senescence), but we also observed instances of telomere lengthening within individuals. We found some evidence for selective disappearance of individuals with shorter telomeres through life. Early-life TL positively predicted later-life TL, but the within-individual repeatability in TL was low (9.2%). Using genetic pedigrees, we found a moderate heritability of ∆TL (h2 = 0.21), which was higher than the heritabilities of early-life TL (h2 = 0.14) and later-life TL measurements (h2 = 0.15). Cohort effects explained considerable proportions of variation in early-life TL (60%), later-life TL (53%), and ∆TL (37%), which suggests persistent impacts of the early-life environment on lifelong telomere dynamics. Individual changes in TL were independent of early-life TL. Finally, there was weak evidence for population differences in ∆TL that may be linked to ecological differences in habitat types. Combined, our results show that individual telomere biology is highly dynamic and influenced by both genetic and environmental variation in natural conditions.

The importance of distinguishing individual differences in 'social impact' versus 'social responsiveness' when quantifying indirect genetic effects on the evolution of social plasticity.

Social evolution and the dynamics of social interactions have previously been studied under the frameworks of quantitative genetics and behavioural ecology. In quantitative genetics, indirect genetic effects of social partners on the socially plastic phenotypes of focal individuals typically lack crucial detail already included in treatments of social plasticity in behavioural ecology. Specifically, whilst focal individuals (e.g. receivers) may show variation in their 'responsiveness' to the social environment, individual social partners (e.g. signallers) may have a differential 'impact' on focal phenotypes. Here we propose an integrative framework, that highlights the distinction between responsiveness versus impact in indirect genetic effects for a range of behavioural traits. We describe impact and responsiveness using a reaction norm approach and provide statistical models for the assessment of these effects of focal and social partner identity in different types of social interactions. By providing such a framework, we hope to stimulate future quantitative research investigating the causes and consequences of social interactions on phenotypic evolution.

Causes and consequences of variation in early-life telomere length in a bird metapopulation.

Environmental conditions during early-life development can have lasting effects shaping individual heterogeneity in fitness and fitness-related traits. The length of telomeres, the DNA sequences protecting chromosome ends, may be affected by early-life conditions, and telomere length (TL) has been associated with individual performance within some wild animal populations. Thus, knowledge of the mechanisms that generate variation in TL, and the relationship between TL and fitness, is important in understanding the role of telomeres in ecology and life-history evolution. Here, we investigate how environmental conditions and morphological traits are associated with early-life blood TL and if TL predicts natal dispersal probability or components of fitness in 2746 wild house sparrow (Passer domesticus) nestlings from two populations sampled across 20 years (1994-2013). We retrieved weather data and we monitored population fluctuations, individual survival, and reproductive output using field observations and genetic pedigrees. We found a negative effect of population density on TL, but only in one of the populations. There was a curvilinear association between TL and the maximum daily North Atlantic Oscillation index during incubation, suggesting that there are optimal weather conditions that result in the longest TL. Dispersers tended to have shorter telomeres than non-dispersers. TL did not predict survival, but we found a tendency for individuals with short telomeres to have higher annual reproductive success. Our study showed how early-life TL is shaped by effects of growth, weather conditions, and population density, supporting that environmental stressors negatively affect TL in wild populations. In addition, shorter telomeres may be associated with a faster pace-of-life, as individuals with higher dispersal rates and annual reproduction tended to have shorter early-life TL.

Spatial structure and dispersal dynamics in a house sparrow metapopulation.

The effects of spatial structure on metapopulation dynamics depend upon the interaction between local population dynamics and dispersal, and how this relationship is affected by the geographical isolation and spatial heterogeneity in habitat characteristics. Our aim is to examine how emigration and immigration of house sparrows Passer domesticus in a Norwegian archipelagic metapopulation are affected by key factors predicted by classic metapopulation models to affect dispersal-spatial and temporal variation in population size, inter-island distance, local demography and habitat characteristics. This metapopulation can be divided into two major habitat types: (a) islands closer to the mainland where sparrows breed in colonies on farms, and (b) islands without farms, situated farther away from the mainland where sparrows are exposed to harsher environmental conditions. Dispersal was spatially structured within the metapopulation; there was proportionally and numerically less emigration and immigration involving farm islands, as compared to non-farm islands. Furthermore, emigration and immigration occurred mostly between nearby islands. Moreover, emigration in response to spatial differences in mean population size differed between the habitat types, but populations with large mean received more immigrants in both habitat types. The number of emigrants and immigrants was negatively related to long-term recruit production, which was not the case in non-farm islands. The proportion and number of emigrants was positively related to temporal increases in recruit production on farm islands, however not on non-farm islands. Our results demonstrate that spatial heterogeneity in environmental conditions influences how spatial variation in long-term mean population size, and temporal and spatial variation in recruit production, affects dispersal dynamics. The spatial structure of this metapopulation is therefore best described by a spatially explicit model in which the exchange of individuals within each habitat type is strongly affected by the degree of geographical isolation, population size and recruit production. However, these relationships differed between the two habitat types; non-farm islands showing similarities to a mainland-island model type of structure, whereas farm islands showed features more associated with source-sink or balanced dispersal models. Such differential dispersal dynamics between habitat types are expected to have important consequences for the ecological and evolutionary dynamics within this metapopulation.

Dispersal in a house sparrow metapopulation: An integrative case study of genetic assignment calibrated with ecological data and pedigree information.

Dispersal has a crucial role determining ecoevolutionary dynamics through both gene flow and population size regulation. However, to study dispersal and its consequences, one must distinguish immigrants from residents. Dispersers can be identified using telemetry, capture-mark-recapture (CMR) methods, or genetic assignment methods. All of these methods have disadvantages, such as high costs and substantial field efforts needed for telemetry and CMR surveys, and adequate genetic distance required in genetic assignment. In this study, we used genome-wide 200K Single Nucleotide Polymorphism data and two different genetic assignment approaches (GSI_SIM, Bayesian framework; BONE, network-based estimation) to identify the dispersers in a house sparrow (Passer domesticus) metapopulation sampled over 16 years. Our results showed higher assignment accuracy with BONE. Hence, we proceeded to diagnose potential sources of errors in the assignment results from the BONE method due to variation in levels of interpopulation genetic differentiation, intrapopulation genetic variation and sample size. We show that assignment accuracy is high even at low levels of genetic differentiation and that it increases with the proportion of a population that has been sampled. Finally, we highlight that dispersal studies integrating both ecological and genetic data provide robust assessments of the dispersal patterns in natural populations.

Variation in generation time reveals density regulation as an important driver of pace of life in a bird metapopulation.

Generation time determines the pace of key demographic and evolutionary processes. Quantified as the weighted mean age at reproduction, it can be studied as a life-history trait that varies within and among populations and may evolve in response to ecological conditions. We combined quantitative genetic analyses with age- and density-dependent models to study generation time variation in a bird metapopulation. Generation time was heritable, and males had longer generation times than females. Individuals with longer generation times had greater lifetime reproductive success but not a higher expected population growth rate. Density regulation acted on recruit production, suggesting that longer generation times should be favoured when populations are closer to carrying capacity. Furthermore, generation times were shorter when populations were growing and longer when populations were closer to equilibrium or declining. These results support classic theory predicting that density regulation is an important driver of the pace of life-history strategies.

Most published selection gradients are underestimated: Why this is and how to fix it.

Ecologists and evolutionary biologists routinely estimate selection gradients. Most researchers seek to quantify selection on individual phenotypes, regardless of whether fixed or repeatedly expressed traits are studied. Selection gradients estimated to address such questions are attenuated unless analyses account for measurement error and biological sources of within-individual variation. Estimates of standardized selection gradients published in Evolution between 2010 and 2019 were primarily based on traits measured once (59% of 325 estimates). We show that those are attenuated: bias increases with decreasing repeatability but differently for linear versus nonlinear gradients. Others derived individual-mean trait values prior to analyses (41%), typically using few repeats per individual, which does not remove bias. We evaluated three solutions, all requiring repeated measures: (i) correcting gradients derived from classic models using estimates of trait correlations and repeatabilities, (ii) multivariate mixed-effects models, previously used for estimating linear gradients (seven estimates, 2%), which we expand to nonlinear analyses, and (iii) errors-in-variables models that account for within-individual variance, and are rarely used in selection studies. All approaches produced accurate estimates regardless of repeatability and type of gradient, however, errors-in-variables models produced more precise estimates and may thus be preferable.

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.

Collision between biological process and statistical analysis revealed by mean centring.

Animal ecologists often collect hierarchically structured data and analyse these with linear mixed-effects models. Specific complications arise when the effect sizes of covariates vary on multiple levels (e.g. within vs. among subjects). Mean centring of covariates within subjects offers a useful approach in such situations, but is not without problems. A statistical model represents a hypothesis about the underlying biological process. Mean centring within clusters assumes that the lower level responses (e.g. within subjects) depend on the deviation from the subject mean (relative) rather than on the absolute scale of the covariate. This may or may not be biologically realistic. We show that mismatch between the nature of the generating (i.e. biological) process and the form of the statistical analysis produce major conceptual and operational challenges for empiricists. We explored the consequences of mismatches by simulating data with three response-generating processes differing in the source of correlation between a covariate and the response. These data were then analysed by three different analysis equations. We asked how robustly different analysis equations estimate key parameters of interest and under which circumstances biases arise. Mismatches between generating and analytical equations created several intractable problems for estimating key parameters. The most widely misestimated parameter was the among-subject variance in response. We found that no single analysis equation was robust in estimating all parameters generated by all equations. Importantly, even when response-generating and analysis equations matched mathematically, bias in some parameters arose when sampling across the range of the covariate was limited. Our results have general implications for how we collect and analyse data. They also remind us more generally that conclusions from statistical analysis of data are conditional on a hypothesis, sometimes implicit, for the process(es) that generated the attributes we measure. We discuss strategies for real data analysis in face of uncertainty about the underlying biological process.

Phenotypic evolution in stochastic environments: The contribution of frequency- and density-dependent selection.

Understanding how environmental variation affects phenotypic evolution requires models based on ecologically realistic assumptions that include variation in population size and specific mechanisms by which environmental fluctuations affect selection. Here we generalize quantitative genetic theory for environmentally induced stochastic selection to include general forms of frequency- and density-dependent selection. We show how the relevant fitness measure under stochastic selection relates to Fisher's fundamental theorem of natural selection, and present a general class of models in which density regulation acts through total use of resources rather than just population size. In this model, there is a constant adaptive topography for expected evolution, and the function maximized in the long run is the expected factor restricting population growth. This allows us to generalize several previous results and to explain why apparently " K -selected" species with slow life histories often have low carrying capacities. Our joint analysis of density- and frequency-dependent selection reveals more clearly the relationship between population dynamics and phenotypic evolution, enabling a broader range of eco-evolutionary analyses of some of the most interesting problems in evolution in the face of environmental variation.

Pathways to social evolution and their evolutionary feedbacks.

In the context of social evolution, the ecological drivers of selection are the phenotypes of other individuals. The social environment can thus evolve, potentially changing the adaptive value for different social strategies. Different branches of evolutionary biology have traditionally focused on different aspects of these feedbacks. Here, we synthesize behavioral ecology theory concerning evolutionarily stable strategies when fitness is frequency dependent with quantitative genetic models providing statistical descriptions of evolutionary responses to social selection. Using path analyses, we review how social interactions influence the strength of selection and how social responsiveness, social impact, and non-random social assortment affect responses to social selection. We then detail how the frequency-dependent nature of social interactions fits into this framework and how it imposes selection on traits mediating social responsiveness, social impact, and social assortment, further affecting evolutionary dynamics. Throughout, we discuss the parameters in quantitative genetics models of social evolution from a behavioral ecology perspective and identify their statistical counterparts in empirical studies. This integration of behavioral ecology and quantitative genetic perspectives should lead to greater clarity in the generation of hypotheses and more focused empirical research regarding evolutionary pathways and feedbacks inherent in specific social interactions.

Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation.

Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations.

Drivers of long-term invertebrate community stability in changing Swedish lakes.

Research on ecosystem stability has had a strong focus on local systems. However, environmental change often occurs slowly at broad spatial scales, which requires regional-level assessments of long-term stability. In this study, we assess the stability of macroinvertebrate communities across 105 lakes in the Swedish "lakescape." Using a hierarchical mixed-model approach, we first evaluate the environmental pressures affecting invertebrate communities in two ecoregions (north, south) using a 23 year time series (1995-2017) and then examine how a set of environmental and physical variables affect the stability of these communities. Results show that lake latitude, size, total phosphorus and alkalinity affect community composition in northern and southern lakes. We find that lake stability is affected by species richness and lake size in both ecoregions and alkalinity and total phosphorus in northern lakes. There is large heterogeneity in the patterns of community stability of individual lakes, but relationships between that stability and environmental drivers begin to emerge when the lakescape, composed of many discrete lakes, is the focal unit of study. The results of this study highlight that broad-scale comparisons in combination with long time series are essential to understand the effects of environmental change on the stability of lake communities in space and time.

Individual variation in age-dependent reproduction: Fast explorers live fast but senesce young?

Adaptive integration of life history and behaviour is expected to result in variation in the pace-of-life. Previous work focused on whether 'risky' phenotypes live fast but die young, but reported conflicting support. We posit that individuals exhibiting risky phenotypes may alternatively invest heavily in early-life reproduction but consequently suffer greater reproductive senescence. We used a 7-year longitudinal dataset with >1,200 breeding records of >800 female great tits assayed annually for exploratory behaviour to test whether within-individual age dependency of reproduction varied with exploratory behaviour. We controlled for biasing effects of selective (dis)appearance and within-individual behavioural plasticity. Slower and faster explorers produced moderate-sized clutches when young; faster explorers subsequently showed an increase in clutch size that diminished with age (with moderate support for declines when old), whereas slower explorers produced moderate-sized clutches throughout their lives. There was some evidence that the same pattern characterized annual fledgling success, if so, unpredictable environmental effects diluted personality-related differences in this downstream reproductive trait. Support for age-related selective appearance was apparent, but only when failing to appreciate within-individual plasticity in reproduction and behaviour. Our study identifies within-individual age-dependent reproduction, and reproductive senescence, as key components of life-history strategies that vary between individuals differing in risky behaviour. Future research should thus incorporate age-dependent reproduction in pace-of-life studies.

Effects of manipulated levels of predation threat on parental provisioning and nestling begging.

Parental provisioning behavior is a major determinant of offspring growth and survival, but high provisioning rates might come at the cost of increased predation threat. Parents should thus adjust provisioning activity according to current predation threat levels. Moreover, life-history theory predicts that response to predation threat should be correlated with investment in current reproduction. We experimentally manipulated perceived predation threat in free-living great tits (Parus major) by presenting parents with a nest predator model while monitoring different aspects of provisioning behavior and nestling begging. Experiments were conducted in 2 years differing greatly in ecological conditions, including food availability. We further quantified male territorial aggressiveness and male and female exploratory tendency. Parents adjusted provisioning according to current levels of threat in an apparently adaptive way. They delayed nest visits during periods of elevated perceived predation threat and subsequently compensated for lost feeding opportunities by increasing provisioning once the immediate threat had diminished. Nestling begging increased after elevated levels of predation threat, but returned to baseline levels by the end of the experiment, suggesting that parents had fully compensated for lost feeding opportunities. There was no evidence for a link between male exploration behavior or aggressiveness and provisioning behavior. In contrast, fast-exploring females provisioned at higher rates, but only in the year with poor environmental conditions, which might indicate a greater willingness to invest in current reproduction in general. Future work should assess whether these personality-related differences in delivery rates under harsher conditions came at a cost of reduced residual reproductive value.

Life-history evolution under fluctuating density-dependent selection and the adaptive alignment of pace-of-life syndromes.

We present a novel perspective on life-history evolution that combines recent theoretical advances in fluctuating density-dependent selection with the notion of pace-of-life syndromes (POLSs) in behavioural ecology. These ideas posit phenotypic co-variation in life-history, physiological, morphological and behavioural traits as a continuum from the highly fecund, short-lived, bold, aggressive and highly dispersive 'fast' types at one end of the POLS to the less fecund, long-lived, cautious, shy, plastic and socially responsive 'slow' types at the other. We propose that such variation in life histories and the associated individual differences in behaviour can be explained through their eco-evolutionary dynamics with population density - a single and ubiquitous selective factor that is present in all biological systems. Contrasting regimes of environmental stochasticity are expected to affect population density in time and space and create differing patterns of fluctuating density-dependent selection, which generates variation in fast versus slow life histories within and among populations. We therefore predict that a major axis of phenotypic co-variation in life-history, physiological, morphological and behavioural traits (i.e. the POLS) should align with these stochastic fluctuations in the multivariate fitness landscape created by variation in density-dependent selection. Phenotypic plasticity and/or genetic (co-)variation oriented along this major POLS axis are thus expected to facilitate rapid and adaptively integrated changes in various aspects of life histories within and among populations and/or species. The fluctuating density-dependent selection POLS framework presented here therefore provides a series of clear testable predictions, the investigation of which should further our fundamental understanding of life-history evolution and thus our ability to predict natural population dynamics.