Assessing variation in life‐history tactics within a population using mixture regression models: a practical guide for evolutionary ecologists

Mixed models are now well‐established methods in ecology and evolution because they allow accounting for and quantifying within‐ and between‐individual variation. However, the required normal distribution of the random effects can often be violated by the presence of clusters among subjects, which leads to multi‐modal distributions. In such cases, using what is known as mixture regression models might offer a more appropriate approach. These models are widely used in psychology, sociology, and medicine to describe the diversity of trajectories occurring within a population over time (e.g. psychological development, growth). In ecology and evolution, however, these models are seldom used even though understanding changes in individual trajectories is an active area of research in life‐history studies. Our aim is to demonstrate the value of using mixture models to describe variation in individual life‐history tactics within a population, and hence to promote the use of these models by ecologists and evolutionary ecologists. We first ran a set of simulations to determine whether and when a mixture model allows teasing apart latent clustering, and to contrast the precision and accuracy of estimates obtained from mixture models versus mixed models under a wide range of ecological contexts. We then used empirical data from long‐term studies of large mammals to illustrate the potential of using mixture models for assessing within‐population variation in life‐history tactics. Mixture models performed well in most cases, except for variables following a Bernoulli distribution and when sample size was small. The four selection criteria we evaluated [Akaike information criterion (AIC), Bayesian information criterion (BIC), and two bootstrap methods] performed similarly well, selecting the right number of clusters in most ecological situations. We then showed that the normality of random effects implicitly assumed by evolutionary ecologists when using mixed models was often violated in life‐history data. Mixed models were quite robust to this violation in the sense that fixed effects were unbiased at the population level. However, fixed effects at the cluster level and random effects were better estimated using mixture models. Our empirical analyses demonstrated that using mixture models facilitates the identification of the diversity of growth and reproductive tactics occurring within a population. Therefore, using this modelling framework allows testing for the presence of clusters and, when clusters occur, provides reliable estimates of fixed and random effects for each cluster of the population. In the presence or expectation of clusters, using mixture models offers a suitable extension of mixed models, particularly when evolutionary ecologists aim at identifying how ecological and evolutionary processes change within a population. Mixture regression models therefore provide a valuable addition to the statistical toolbox of evolutionary ecologists. As these models are complex and have their own limitations, we provide recommendations to guide future users.     

Looking for a needle in a haystack: inference about individual fitness components in a heterogeneous population

Studies of wild vertebrates have provided evidence of substantial differences in lifetime reproduction among individuals and the sequences of life history ‘states’ during life (breeding, nonbreeding, etc.). Such differences may reflect ‘fixed’ differences in fitness components among individuals determined before, or at the onset of reproductive life. Many retrospective life history studies have translated this idea by assuming a ‘latent’ unobserved heterogeneity resulting in a fixed hierarchy among individuals in fitness components. Alternatively, fixed differences among individuals are not necessarily needed to account for observed levels of individual heterogeneity in life histories. Individuals with identical fitness traits may stochastically experience different outcomes for breeding and survival through life that lead to a diversity of ‘state’ sequences with some individuals living longer and being more productive than others, by chance alone. The question is whether individuals differ in their underlying fitness components in ways that cannot be explained by observable ‘states’ such as age, previous breeding success, etc. Here, we compare statistical models that represent these opposing hypotheses, and mixtures of them, using data from kittiwakes. We constructed models that accounted for observed covariates, individual random effects (unobserved heterogeneity), first‐order Markovian transitions between observed states, or combinations of these features. We show that individual sequences of states are better accounted for by models incorporating unobserved heterogeneity than by models including first‐order Markov processes alone, or a combination of both. If we had not considered individual heterogeneity, models including Markovian transitions would have been the best performing ones. We also show that inference about age‐related changes in fitness components is sensitive to incorporation of underlying individual heterogeneity in models. Our approach provides insight into the sources of individual heterogeneity in life histories, and can be applied to other data sets to examine the ubiquity of our results across the tree of life.     

Individual variation in growth trajectories: phenotypic and genetic correlations in ontogeny of the house finch (Carpodacus mexicanus)

We studied patterns of growth in a recently established natural population of the house finch (Carpodacus mexicanus) to examine whether phenotypic and genetic covariation among age‐specific trait values is likely to constrain morphological change favoured by selection acting on adults. We found variable patterns of allometric relationships during ontogeny, and documented relatively weak covariations among ages or among traits in individual growth trajectories. Frequent compensatory growth largely cancelled out the initial differences among nestlings, potentially enabling house finches to raise offspring under diverse and unpredictable environmental conditions. Moderate levels of additive genetic variance in morphological traits throughout ontogeny, and relatively low and fluctuating phenotypic and genetic covariation among ages imply strong potential for evolutionary change in morphological traits under selection. This conclusion is consistent with the profound population‐level divergence in morphological patterns that accompanied very successful colonization of most of North America by the house finch over the last 50 years.     

Individual heterogeneity in life histories and eco‐evolutionary dynamics

Individual heterogeneity in life history shapes eco‐evolutionary processes, and unobserved heterogeneity can affect demographic outputs characterising life history and population dynamical properties. Demographic frameworks like matrix models or integral projection models represent powerful approaches to disentangle mechanisms linking individual life histories and population‐level processes. Recent developments have provided important steps towards their application to study eco‐evolutionary dynamics, but so far individual heterogeneity has largely been ignored. Here, we present a general demographic framework that incorporates individual heterogeneity in a flexible way, by separating static and dynamic traits (discrete or continuous). First, we apply the framework to derive the consequences of ignoring heterogeneity for a range of widely used demographic outputs. A general conclusion is that besides the long‐term growth rate lambda, all parameters can be affected. Second, we discuss how the framework can help advance current demographic models of eco‐evolutionary dynamics, by incorporating individual heterogeneity. For both applications numerical examples are provided, including an empirical example for pike. For instance, we demonstrate that predicted demographic responses to climate warming can be reversed by increased heritability. We discuss how applications of this demographic framework incorporating individual heterogeneity can help answer key biological questions that require a detailed understanding of eco‐evolutionary dynamics.     

Heterogeneity in individual quality in birds: overall patterns and insights from a study on common terns

While life‐history theory predicts a tradeoff between reproduction and survival, positive covariance, indicative of heterogeneity in individual quality, is often reported among individuals from natural populations. We review longitudinal studies of wild bird populations that test the relationship between annual reproductive success and lifespan and find the majority to report a positive correlation, while none reports a negative correlation. Heterogeneity in individual quality in resource acquisition, masking resource‐based tradeoffs, therefore appears to be common in birds. Considering that there is little evidence for heritable variation in fitness, heterogeneity in individual quality among adults may be due to life‐long effects of developmental conditions. In a 20‐year case study on common terns Sterna hirundo, we test for life‐long effects of cohort quality and within‐cohort nest quality, but find no significant effects on long‐term proxies of quality. Since other studies do find strong life‐long effects of developmental conditions, we suggest that the brood reduction strategy adopted by common terns, causing the majority of offspring to die rapidly after hatching, efficiently reduces variation in offspring quality at independence. As such, a brood reduction strategy may contribute to reduced heterogeneity in adult survival in stochastic environments, both suggested to be more common and adaptive in long‐lived species. Further study is required to assess heterogeneity in individual reproduction, especially in relation to environmental stochasticity and species’ life‐history strategies, in order to assess whether the relative strength of selection in early and late life may indeed affect the magnitude of heterogeneity in individual quality over life, and how this is mediated by parent–offspring conflict.     

The evolutionary ecology of alternative migratory tactics in salmonid fishes

Extensive individual variation in spatial behaviour is a common feature among species that exhibit migratory life cycles. Nowhere is this more evident than in salmonid fishes; individual fish may complete their entire life cycle in freshwater streams, others may migrate variable distances at sea and yet others limit their migrations to larger rivers or lakes before returning to freshwater streams to spawn. This review presents evidence that individual variation in migratory behaviour and physiology in salmonid fishes is controlled by developmental thresholds and that part of the variation in proximal traits activating the development of alternative migratory tactics is genetically based. We summarize evidence that alternative migratory tactics co‐exist within populations and that all individuals may potentially adopt any of the alternative phenotypes. Even though intra‐specific genetic divergence of migratory tactics is uncommon, it may occur if female competition for oviposition sites results in spawning segregation of alternative phenotypes. Because of their polygenic nature, alternative migratory tactics are considered as threshold traits. Threshold traits have two characteristics: an underlying 'liability' trait that varies in a continuous fashion, and a threshold value which is responsible for the discreetness observed in phenotypic distribution. We review evidence demonstrating that body size is an adequate proxy for the liability trait controlling the decision to migrate, but that the same phenotypic outcome (anadromy or residency) may be reached by different developmental pathways. The evidence suggesting a significant heritable component in the development of alternative migratory tactics is subsequently reviewed, leading us to conclude that alternative migratory tactics have considerable potential to respond to selection and evolve. We review what is known about the proximal physiological mechanisms mediating the translation of the continuous value of the liability trait into a discontinuous migratory tactic. We conclude by identifying several avenues for future research, including testing the frequency‐dependent selection hypothesis, establishing the relative importance of adaptive phenotypic plasticity in explaining some geographic gradients in migratory behaviour and identifying the physiological and genetic basis of the switching mechanisms responsible for alternative migratory tactics.     

Evolutionary potential of morphological traits across different life‐history stages

Despite accumulating examples of selection acting on heritable traits in the wild, predicted evolutionary responses are often different from observed phenotypic trends. Various explanations have been suggested for these mismatches. These include within‐individual changes across lifespan that can create important variation in genetic architecture of traits and selection acting on them, but also potential problems with the methodological approach used to predict evolutionary responses of traits. Here, we used an 8‐year data set on tree swallow (Tachycineta bicolor) to first assess the effects of differences among three nestling life‐history stages on the genetic (co)variances of two morphological traits (body mass and primary feather length) and the selection acting on them over three generations. We then estimated the evolutionary potential of these traits by predicting their evolutionary responses using the breeder's equation and the secondary theorem of selection approaches. Our results showed variation in strength and direction of selection and slight changes in trait variance across ages. Predicted evolutionary responses differed importantly between both approaches for half of the trait–age combinations we studied, suggesting the presence of environmentally induced correlations between focal traits and fitness possibly biasing breeder's equation predictions. Our results emphasize that predictions of evolutionary potential for morphological traits are likely to be highly variable, both in strength and direction, depending on the life stage and method used, thus mitigating our capacity to predict adaptation and persistence of wild populations.     

The ontogeny of personality traits in the desert funnel‐web spider,Agelenopsis lisa (Araneae: Agelenidae)

Trait consistency over time is one of the cornerstones of animal personality. Behavioral syndromes are the result of correlations between behaviors. While repeatability in behavior is not a requirement for behavioral syndromes, the two concepts studied together provide a more comprehensive understanding of how behavior can change over ontogeny. The roles of ontogenetic processes in the emergence of personality and behavioral syndromes have received much individual attention. However, the characterization of both individual trait consistency and behavioral syndromes across both sexes, as in our study, has been relatively rare. Ontogeny refers to changes that occur from conception to maturation, and juveniles might be expected to undergo different selection pressures than sexually mature individuals and also will experience profound changes in hormones, morphology, and environment during this period. In this study, we test for behavioral trait consistency and behavioral syndromes across six time points during ontogenetic development in the desert funnel‐web spider (Agelenopsis lisa). Our results indicate behavioral traits generally lack consistency (repeatability) within life stages and across ontogeny. However, penultimate males and mature females do exhibit noticeable mean‐level changes, with greater aggressive responses toward prey, shorter latencies to explore their environment and in the exhibition of risk‐averse responses to predatory cues. These traits also show high repeatability. Some trait correlations do exist as well. In particular, a strong correlation between aggressiveness toward prey and exploration factors is observed in mature males. However, because correlations among these factors are unstable across ontogeny and vary in strength over time, we conclude that behavioral syndromes do not exist in this species. Nevertheless, our results indicate that increased consistency, increasing average trait values, and varying correlations between traits may coincide with developmentally important changes associated with sexual maturation, albeit at different time points in males and females. This period of the life cycle merits systematic examination across taxa.     

Among‐individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life‐history traits in the garter snake Thamnophis elegans

Accumulating evidence suggests that within‐individual plasticity of behavioural and physiological traits is limited, resulting in stable among‐individual differences in these aspects of the phenotype. Furthermore, these traits often covary within individuals, resulting in a continuum of correlated phenotypic variation among individuals within populations and species. This heterogeneity, in turn, affects individual fitness and can have cross‐generational effects. Patterns of trait covariation, among‐individual differences, and subsequent fitness consequences have long been recognized in reptiles. Here, we provide a test of patterns of among‐individual heterogeneity in behaviour and physiology and subsequent effects on reproduction and offspring fitness in the garter snake Thamnophis elegans. We find that measures of activity levels vary among individuals and are consistent within individuals in reproductive female snakes, indicating stable behavioural phenotypes. Blood hormone and glucose concentrations are not as stable within individuals, indicating that these traits do not describe consistent physiological phenotypes. Nonetheless, the major axes of variation in maternal traits describe behavioural and physiological phenotypes that interact to predict offspring body condition and mass at birth. This differential allocation of energy to offspring, in turn, strongly influences subsequent offspring growth and survival. This pattern suggests the potential for strong selection on phenotypes defined by behaviour–physiology interactions.     

Dispersal and individual quality in a long lived species

The idea of differences in individual quality has been put forward in numerous long-term studies in long-lived species to explain differences in lifetime production among individuals. Despite the important role of individual heterogeneity in vital rates in demography, population dynamics and life history theory, the idea of "individual quality" is elusive. It is sometimes assumed to be a static or dynamic individual characteristic. When considered as a dynamic trait, it is sometimes assumed to vary deterministically or stochastically, or to be confounded with the characteristics of the habitat. We addressed heterogeneity in reproductive performance among individuals established in higher-quality habitat in a long-lived seabird species. We used approaches to statistical inference based on individual random effects permitting quantification of heterogeneity in populations and assessment of individual variation from the population mean. We found evidence of heterogeneity in breeding probability, not success probability. We assessed the influence of dispersal on individual reproductive potential. Dispersal is likely to be destabilizing in species with high site and mate fidelity. We detected heterogeneity after dispersal, not before. Individuals may perform well regardless of quality before destabilization, including those that recruited in higher-quality habitat by chance, but only higher-quality individuals may be able to overcome the consequences of dispersal. Importantly, results differed when accounting for individual heterogeneity (an increase in mean breeding probability when individuals dispersed), or not (a decrease in mean breeding probability). In the latter case, the decrease in mean breeding probability may result from a substantial decrease in breeding probability in a few individuals and a slight increase in others. In other words, the pattern observed at the population mean level may not reflect what happens in the majority of individuals.     

Beyond the proportional frailty model: Bayesian estimation of individual heterogeneity on mortality parameters

Today, we know that demographic rates can be greatly influenced by differences among individuals in their capacity to survive and reproduce. These intrinsic differences, commonly known as individual heterogeneity, can rarely be measured and are thus treated as latent variables when modeling mortality. Finite mixture models and mixed effects models have been proposed as alternative approaches for inference on individual heterogeneity in mortality. However, in general models assume that individual heterogeneity influences mortality proportionally, which limits the possibility to test hypotheses on the effect of individual heterogeneity on other aspects of mortality such as ageing rates. Here, we propose a Bayesian model that builds upon the mixture models previously developed, but that facilitates making inferences on the effect of individual heterogeneity on mortality parameters other than the baseline mortality. As an illustration, we apply this framework to the Gompertz–Makeham mortality model, commonly used in human and wildlife studies, by assuming that the Gompertz rate parameter is affected by individual heterogeneity. We provide results of a simulation study where we show that the model appropriately retrieves the parameters used for simulation, even for low variances in the heterogeneous parameter. We then apply the model to a dataset on captive chimpanzees and on a cohort life table of 1751 Swedish men, and show how model selection against a null model (i.e., without heterogeneity) can be carried out.     

Phenotypic selection and covariation in the life‐history traits of elephant seals: heavier offspring gain a double selective advantage

Early developmental conditions contribute to individual heterogeneity of both phenotypic traits and fitness components, ultimately affecting population dynamics. Although the demographic consequences of ontogenic growth are best quantified using an integrated measure of fitness, most analyses to date have instead studied individual fitness components in isolation. Here, we estimated phenotypic selection on weaning mass in female southern elephant seals Mirounga leonina by analyzing individual‐based data collected between 1986 and 2016 with capture–recapture and matrix projection models. In support of a hypothesis predicting a gradual decrease of weaning mass effects with time since weaning (the replacement hypothesis), we found that the estimated effects of weaning mass on future survival and recruitment probability was of intermediate duration (rather than transient or permanent). Heavier female offspring had improved odds of survival in early life and a higher probability to recruit at an early age. The positive link between weaning mass and recruitment age is noteworthy, considering that pre‐recruitment mortality already imposed a strong selective filter on the population, leaving only the most ‘robust’ individuals to reproduce. The selection gradient on asymptotic population growth rate, a measure of mean absolute fitness, was weaker than selection on first‐year survival and recruitment probabilities. Weaker selection on mean fitness occurs because weaning mass has little impact on adult survival, the fitness component to which the population growth of long‐lived species is most sensitive. These results highlight the need to interpret individual variation in phenotypic traits in a context that considers the demographic pathways between the trait and an inclusive proxy of individual fitness. Although variation in weaning mass do not translate to permanent survival differences among individuals in adulthood, it explains heterogeneity and positive covariation between survival and breeding in early life, which contribute to between‐individual variation in fitness.     

Ontogeny of robusticity of craniofacial traits in modern humans: A study of South American populations

To date, differences in craniofacial robusticity among modern and fossil humans have been primarily addressed by analyzing adult individuals; thus, the developmental basis of such differentiation remains poorly understood. This article aims to analyze the ontogenetic development of craniofacial robusticity in human populations from South America. Geometric morphometric methods were used to describe cranial traits in lateral view by using landmarks and semilandmarks. We compare the patterns of variation among populations obtained with subadults and adults to determine whether population‐specific differences are evident at early postnatal ontogeny, compare ontogenetic allometric trajectories to ascertain whether changes in the ontogeny of shape contribute to the differentiation of adult morphologies, and estimate the amount of size change that occurs during growth along each population‐specific trajectory. The results obtained indicate that the pattern of interpopulation variation in shape and size is already established at the age of 5 years, meaning that processes acting early during ontogeny contribute to the adult variation. The ontogenetic allometric trajectories are not parallel among all samples, suggesting the divergence in the size‐related shape changes. Finally, the extension of ontogenetic trajectories also seems to contribute to shape variation observed among adults. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Wolf in sheep's clothing: Model misspecification undermines tests of the neutral theory for life histories

Understanding the processes behind change in reproductive state along life‐history trajectories is a salient research program in evolutionary ecology. Two processes, state dependence and heterogeneity, can drive the dynamics of change among states. Both processes can operate simultaneously, begging the difficult question of how to tease them apart in practice. The Neutral Theory for Life Histories (NTLH) holds that the bulk of variations in life‐history trajectories is due to state dependence and is hence neutral: Once previous (breeding) state is taken into account, variations are mostly random. Lifetime reproductive success (LRS), the number of descendants produced over an individual's reproductive life span, has been used to infer support for NTLH in natura. Support stemmed from accurate prediction of the population‐level distribution of LRS with parameters estimated from a state dependence model. We show with Monte Carlo simulations that the current reliance of NTLH on LRS prediction in a null hypothesis framework easily leads to selecting a misspecified model, biased estimates and flawed inferences. Support for the NTLH can be spurious because of a systematic positive bias in estimated state dependence when heterogeneity is present in the data but ignored in the analysis. This bias can lead to spurious positive covariance between fitness components when there is in fact an underlying trade‐off. Furthermore, neutrality implied by NTLH needs a clarification because of a probable disjunction between its common understanding by evolutionary ecologists and its translation into statistical models of life‐history trajectories. Irrespective of what neutrality entails, testing hypotheses about the dynamics of change among states in life histories requires a multimodel framework because state dependence and heterogeneity can easily be mistaken for each other.     

Costs of reproduction can explain the correlated evolution of semelparity and egg size: theory and a test with salmon

Species’ life history traits, including maturation age, number of reproductive bouts, offspring size and number, reflect adaptations to diverse biotic and abiotic selection pressures. A striking example of divergent life histories is the evolution of either iteroparity (breeding multiple times) or semelparity (breed once and die). We analysed published data on salmonid fishes and found that semelparous species produce larger eggs, that egg size and number increase with salmonid body size among populations and species and that migratory behaviour and parity interact. We developed three hypotheses that might explain the patterns in our data and evaluated them in a stage‐structured modelling framework accounting for different growth and survival scenarios. Our models predict the observation of small eggs in iteroparous species when egg size is costly to maternal survival or egg number is constrained. By exploring trait co‐variation in salmonids, we generate new hypotheses for the evolution of trade‐offs among life history traits.     

Individual heterogeneity and capture–recapture models: what,why and how?

Variation between and within individuals in life history traits is ubiquitous in natural populations. When affecting fitness‐related traits such as survival or reproduction, individual heterogeneity plays a key role in population dynamics and life history evolution. However, it is only recently that properly accounting for individual heterogeneity when studying population dynamics of free‐ranging populations has been made possible through the development of appropriate statistical models. We aim here to review case studies of individual heterogeneity in the context of capture–recapture models for the estimation of population size and demographic parameters with imperfect detection. First, we define what individual heterogeneity means and clarify the terminology used in the literature. Second, we review the literature and illustrate why individual heterogeneity is used in capture–recapture studies by focusing on the detection of life‐history tradeoffs, including senescence. Third, we explain how to model individual heterogeneity in capture–recapture models and provide the code to fit these models ( https://github.com/oliviergimenez/indhet_in_CRmodels ). The distinction is made between situations in which heterogeneity is actually measured and situations in which part of the heterogeneity remains unobserved. Regarding the latter, we outline recent developments of random‐effect models and finite‐mixture models. Finally, we discuss several avenues for future research.     

Differences in prey personality mediate trophic cascades

Functional trait approaches in ecology chiefly assume the mean trait value of a population adequately predicts the outcome of species interactions. Yet this assumption ignores substantial trait variation among individuals within a population, which can have a profound effect on community structure and function. We explored individual trait variation through the lens of animal personality to test whether among‐individual variation in prey behavior mediates trophic interactions. We quantified the structure of personalities within a population of generalist grasshoppers and examined, through a number of field and laboratory‐based experiments, how personality types could impact tri‐trophic interactions in a food chain. Unlike other studies of this nature, we used spatial habitat domains to evaluate how personality types mechanistically map to behaviors relevant in predator–prey dynamics and found shy and bold individuals differed in both their habitat use and foraging strategy under predation risk by a sit‐and‐wait spider predator. In the field‐based mesocosm portion of our study, we found experimental populations of personality types differed in their trophic impact, demonstrating that prey personality can mediate trophic cascades. We found no differences in respiration rates or body size between personality types used in the mesocosm experiment, indicating relative differences in trophic impact were not due to variation in prey physiology but rather variation in behavioral strategies. Our work demonstrates how embracing the complexity of individual trait variation can offer mechanistically richer understanding of the processes underlying trophic interactions.     

Causes and consequences of ontogenetic dietary shifts: a global synthesis using fish models

Ontogenetic dietary shifts (ODSs), the changes in diet utilisation occurring over the life span of an individual consumer, are widespread in the animal kingdom. Understanding ODSs provides fundamental insights into the biological and ecological processes that function at the individual, population and community levels, and is critical for the development and testing of hypotheses around key concepts in trophic theory on model organisms. Here, we synthesise historic and contemporary research on ODSs in fishes, and identify where further research is required. Numerous biotic and abiotic factors can directly or indirectly influence ODSs, but the most influential of these may vary spatially, temporally and interspecifically. Within the constraints imposed by prey availability, we identified competition and predation risk as the major drivers of ODSs in fishes. These drivers do not directly affect the trophic ontogeny of fishes, but may have an indirect effect on diet trajectories through ontogenetic changes in habitat use and concomitant changes in prey availability. The synthesis provides compelling evidence that ODSs can have profound ecological consequences for fish by, for example, enhancing individual growth and lifetime reproductive output or reducing the risk of mortality. ODSs may also influence food‐web dynamics and facilitate the coexistence of sympatric species through resource partitioning, but we currently lack a holistic understanding of the consequences of ODSs for population, community and ecosystem processes and functioning. Studies attempting to address these knowledge gaps have largely focused on theoretical approaches, but empirical research under natural conditions, including phylogenetic and evolutionary considerations, is required to test the concepts. Research focusing on inter‐individual variation in ontogenetic trajectories has also been limited, with the complex relationships between individual behaviour and environmental heterogeneity representing a particularly promising area for future research.     

Population and evolutionary dynamics in spatially structured seasonally varying environments

Increasingly imperative objectives in ecology are to understand and forecast population dynamic and evolutionary responses to seasonal environmental variation and change. Such population and evolutionary dynamics result from immediate and lagged responses of all key life‐history traits, and resulting demographic rates that affect population growth rate, to seasonal environmental conditions and population density. However, existing population dynamic and eco‐evolutionary theory and models have not yet fully encompassed within‐individual and among‐individual variation, covariation, structure and heterogeneity, and ongoing evolution, in a critical life‐history trait that allows individuals to respond to seasonal environmental conditions: seasonal migration. Meanwhile, empirical studies aided by new animal‐tracking technologies are increasingly demonstrating substantial within‐population variation in the occurrence and form of migration versus year‐round residence, generating diverse forms of ‘partial migration’ spanning diverse species, habitats and spatial scales. Such partially migratory systems form a continuum between the extreme scenarios of full migration and full year‐round residence, and are commonplace in nature. Here, we first review basic scenarios of partial migration and associated models designed to identify conditions that facilitate the maintenance of migratory polymorphism. We highlight that such models have been fundamental to the development of partial migration theory, but are spatially and demographically simplistic compared to the rich bodies of population dynamic theory and models that consider spatially structured populations with dispersal but no migration, or consider populations experiencing strong seasonality and full obligate migration. Second, to provide an overarching conceptual framework for spatio‐temporal population dynamics, we define a ‘partially migratory meta‐population’ system as a spatially structured set of locations that can be occupied by different sets of resident and migrant individuals in different seasons, and where locations that can support reproduction can also be linked by dispersal. We outline key forms of within‐individual and among‐individual variation and structure in migration that could arise within such systems and interact with variation in individual survival, reproduction and dispersal to create complex population dynamics and evolutionary responses across locations, seasons, years and generations. Third, we review approaches by which population dynamic and eco‐evolutionary models could be developed to test hypotheses regarding the dynamics and persistence of partially migratory meta‐populations given diverse forms of seasonal environmental variation and change, and to forecast system‐specific dynamics. To demonstrate one such approach, we use an evolutionary individual‐based model to illustrate that multiple forms of partial migration can readily co‐exist in a simple spatially structured landscape. Finally, we summarise recent empirical studies that demonstrate key components of demographic structure in partial migration, and demonstrate diverse associations with reproduction and survival. We thereby identify key theoretical and empirical knowledge gaps that remain, and consider multiple complementary approaches by which these gaps can be filled in order to elucidate population dynamic and eco‐evolutionary responses to spatio‐temporal seasonal environmental variation and change.     

Individual heterogeneity in reproductive rates and cost of reproduction in a long‐lived vertebrate

Individual variation in reproductive success is a key feature of evolution, but also has important implications for predicting population responses to variable environments. Although such individual variation in reproductive outcomes has been reported in numerous studies, most analyses to date have not considered whether these realized differences were due to latent individual heterogeneity in reproduction or merely random chance causing different outcomes among like individuals. Furthermore, latent heterogeneity in fitness components might be expressed differently in contrasted environmental conditions, an issue that has only rarely been investigated. Here, we assessed (i) the potential existence of latent individual heterogeneity and (ii) the nature of its expression (fixed vs. variable) in a population of female Weddell seals (Leptonychotes weddellii), using a hierarchical modeling approach on a 30‐year mark–recapture data set consisting of 954 individual encounter histories. We found strong support for the existence of latent individual heterogeneity in the population, with “robust” individuals expected to produce twice as many pups as “frail” individuals. Moreover, the expression of individual heterogeneity appeared consistent, with only mild evidence that it might be amplified when environmental conditions are severe. Finally, the explicit modeling of individual heterogeneity allowed us to detect a substantial cost of reproduction that was not evidenced when the heterogeneity was ignored.