Dispersal polymorphisms from natal phenotype–environment interactions have carry‐over effects on lifetime reproductive success of a tropical parrot

We examined how interactions between an individual's phenotype and its environment affect natal dispersal at multiple scales and the effects on lifetime reproductive success using a 22‐year study of green‐rumped parrotlets (Forpus passerinus). Dispersal increased or decreased lifetime reproductive success depending upon an individual's natal environment and phenotype. Many of the phenotypic traits and environmental conditions that influenced lifetime reproductive success also influenced dispersal, such as clutch size and competition, and this differed with scale. By examining phenotype–environment interactions, we observed both positive and negative effects of rainfall, habitat quality and competition on dispersal depending upon phenotype. The dispersal behaviours of juveniles typically resulted in higher lifetime reproductive success. Thus, individuals commonly exhibit ideal free behaviour and results provide support for the occurrence and maintenance of dispersal polymorphisms. This study highlights the long‐term, carry‐over effects of natal environment, natal phenotype and dispersal tactic on lifetime reproductive success.     

The importance of growing up: juvenile environment influences dispersal of individuals and their neighbours

Dispersal is a key ecological process that is strongly influenced by both phenotype and environment. Here, we show that juvenile environment influences dispersal not only by shaping individual phenotypes, but also by changing the phenotypes of neighbouring conspecifics, which influence how individuals disperse. We used a model system (Tribolium castaneum, red flour beetles) to test how the past environment of dispersing individuals and their neighbours influences how they disperse in their current environment. We found that individuals dispersed especially far when exposed to a poor environment as adults if their phenotype, or even one‐third of their neighbours’ phenotypes, were shaped by a poor environment as juveniles. Juvenile environment therefore shapes dispersal both directly, by influencing phenotype, as well as indirectly, by influencing the external social environment. Thus, the juvenile environment of even a minority of individuals in a group can influence the dispersal of the entire group.     

Dispersing brush mice prefer habitat like home

During natal dispersal, young animals leave their natal area and search for a new area to live. In species in which individuals inhabit different types of habitat, experience with a natal habitat may increase the probability that a disperser will select the same type of habitat post-dispersal (natal habitat preference induction or NHPI). Despite considerable interest in the ecological and the evolutionary implications of NHPI, we lack empirical evidence that it occurs in nature. Here we show that dispersing brush mice (Peromyscus boylii) are more likely to search and settle within their natal habitat type than expected based on habitat availability. These results document the occurrence of NHPI in nature and highlight the relevance of experience-generated habitat preferences for ecological and evolutionary processes.     

Altered natal dispersal at the range periphery: The role of behavior,resources, and maternal condition

Natal dispersal outcomes are an interplay between environmental conditions and individual phenotypes. Peripheral, isolated populations may experience altered environmental conditions and natal dispersal patterns that differ from populations in contiguous landscapes. We document nonphilopatric, sex‐biased natal dispersal in an endangered small mammal, the Mt. Graham red squirrel (Tamiasciurus hudsonicus grahamensis), restricted to a single mountain. Other North American red squirrel populations are shown to have sex‐unbiased, philopatric natal dispersal. We ask what environmental and intrinsic factors may be driving this atypical natal dispersal pattern. We test for the influence of proximate factors and ultimate drivers of natal dispersal: habitat fragmentation, local population density, individual behavior traits, inbreeding avoidance, competition for mates, and competition for resources, allowing us to better understand altered natal dispersal patterns at the periphery of a species’ range. A juvenile squirrel's body condition and its mother's mass in spring (a reflection of her intrinsic quality and territory quality) contribute to individual behavioral tendencies for movement and exploration. Resources, behavior, and body condition have the strongest influence on natal dispersal distance, but affect males and females differently. Male natal dispersal distance is positively influenced by its mother's spring body mass and individual tendency for movement; female natal dispersal distance is negatively influenced by its mother's spring body mass and positively influenced by individual tendency for movement. An apparent feedback between environmental variables and subsequent juvenile behavioral state contributes to an altered natal dispersal pattern in a peripheral population, highlighting the importance of studying ecological processes at the both range center and periphery of species’ distributions.     

Habitat exploration and use in dispersing juvenile flying squirrels

1. Variation in behaviours involved in habitat selection is important for several evolutionary and ecological processes. For example, habitat use during dispersal may differ from breeding habitat use, and for dispersers the scale of habitat familiarity is determined by exploratory behaviour. We studied habitat use and exploration of 56 radio-collared juvenile flying squirrels Pteromys volans L. within natal home range and during dispersal, and compared habitat use between juveniles and 37 adults within breeding home range. 2. Before dispersal, young flying squirrels actively moved around the natal site. Surprisingly, long-distance dispersers explored less than short-distance dispersers, but philopatric individuals explored similar distances as dispersers. Females explored less than males, although females are the more dispersive sex in flying squirrels. 3. For most of the individuals the settlement area was unfamiliar due to long dispersal distance. Consequently, direction and distance of exploration were not very strong predictors of settlement location. However, individuals familiar with the settlement area concentrated exploration to that area. Exploration did not correlate with short-term survival. 4. Dispersers preferred breeding habitat while dispersing, but were found more often in matrix habitat than juveniles within natal, or adults within breeding, home ranges. 5. We conclude that familiarity does not determine settlement as much as, for example, availability of the habitat for flying squirrels. Based on our results, it also seems clear that data on adult habitat use are not enough to predict habitat use of dispersing individuals. In addition, our results support the recent view that short- and long-distance dispersers may need to be analysed separately in ecological and evolutionary analyses.     

Effects of conditionally expressed phenotypes and environment on amphibian dispersal in nature

Individuals vary greatly in the distance they disperse, and in doing so, strongly affect ecological and evolutionary processes. Dispersal, when viewed as a component of phenotype, can be affected independently or jointly by environment. However, among taxa with complex life cycles that occupy different habitats over ontogeny, the effects of environment on dispersal and the interaction between environment and phenotype remains poorly understood. Here, we conducted a field experiment to measure how dispersal distance was affected by phenotype, environment experienced before and after metamorphosis, and their interaction. We manipulated the environment encountered by a pond‐breeding salamander Ambystoma annulatum during the aquatic larval stage and again as dispersing terrestrial juveniles. After assaying juvenile phenotype (exploration behavior, body condition, and morphology), we then measured the initial distance dispersed by juveniles. The distance moved by dispersing salamanders was affected by attributes of both larval and juvenile habitat, with salamanders that encountered low quality habitat in either life stage moving the farthest. However, we did not find support for an interactive effect of phenotype and environment affecting the distance moved by dispersers. Interestingly, exploration behavior explained the distance moved by philopatric animals but not dispersing ones. Our findings indicate that the environment experienced before metamorphosis can affect juvenile dispersal behavior, and demonstrates the need to consider dispersal in species with complex life cycles to understand the coupling between local and regional population dynamics.     

Habitat choice stabilizes metapopulation dynamics by enabling ecological specialization

Dispersal is a key trait responsible for the spread of individuals and genes among local populations, thereby generating eco‐evolutionary interactions. Especially in heterogeneous metapopulations, a tight coupling between dispersal, population dynamics and the evolution of local adaptation is expected. In this respect, dispersal should counteract ecological specialization by redistributing locally selected phenotypes (i.e. migration load). Habitat choice following an informed dispersal decision, however, can facilitate the evolution of ecological specialization. How such informed decisions influence metapopulation size and variability is yet to be determined. By means of individual‐based modelling, we demonstrate that informed decisions about both departure and settlement decouple the evolution of dispersal and that of generalism, selecting for highly dispersive specialists. Choice at settlement is based on information from the entire dispersal range, and therefore decouples dispersal from ecological specialization more effectively than choice at departure, which is only based on local information. Additionally, habitat choice at departure and settlement reduces local and metapopulation variability because of the maintenance of ecological specialization at all levels of dispersal propensity. Our study illustrates the important role of habitat choice for dynamics of spatially structured populations and thus emphasizes the importance of considering that dispersal is often informed.     

Sex‐biased breeding dispersal is predicted by social environment in birds

Sex‐biased dispersal is common in vertebrates, although the ecological and evolutionary causes of sex differences in dispersal are debated. Here, we investigate sex differences in both natal and breeding dispersal distances using a large dataset on birds including 86 species from 41 families. Using phylogenetic comparative analyses, we investigate whether sex‐biased natal and breeding dispersal are associated with sexual selection, parental sex roles, adult sex ratio (ASR), or adult mortality. We show that neither the intensity of sexual selection, nor the extent of sex bias in parental care was associated with sex‐biased natal or breeding dispersal. However, breeding dispersal was related to the social environment since male‐biased ASRs were associated with female‐biased breeding dispersal. Male‐biased ASRs were associated with female‐biased breeding dispersal. Sex bias in adult mortality was not consistently related to sex‐biased breeding dispersal. These results may indicate that the rare sex has a stronger tendency to disperse in order to find new mating opportunities. Alternatively, higher mortality of the more dispersive sex could account for biased ASRs, although our results do not give a strong support to this explanation. Whichever is the case, our findings improve our understanding of the causes and consequences of sex‐biased dispersal. Since the direction of causality is not yet known, we call for future studies to identify the causal relationships linking mortality, dispersal, and ASR.     

Ranking the ecological causes of dispersal in a butterfly

Dispersal, i.e. movements potentially leading to gene flow, is central in evolutionary ecology. Many factors can trigger dispersal, all linked to the social and/or the environmental context. Moreover, it is now widely demonstrated that phenotypes with contrasted dispersal abilities coexist within populations of a same species. The current challenge is to elucidate how social and environmental factors will influence the dispersal decision of individuals with distinct phenotypes. We have used the Metatron, a unique experimental mesocosm dedicated to the study of dispersal within fragmented landscapes, to analyze the relative and interactive roles played by ten potential dispersal triggers in experimental two‐patch metapopulations of butterflies. We demonstrate in our model species that some factors (flight performance and wing length) have direct effects on emigration decision, others act only through interactive effects (sex ratio), while a third class of factors presents both direct and interactive effects (weather conditions, habitat quality and sex). We also show that disperser and resident individuals have distinct behavioral and morphological attributes, revealing the existence of a dispersal syndrome. Finally, our results also suggest that the environmental context, and especially weather conditions and habitat quality, prevails over social factors and individual phenotypes in butterflies' decision to disperse. Our approach is applicable to many species facing medium to strong environmental fluctuations, and constitutes a new way to master the idiosyncrasy of the dispersal process. Our framework should also help prioritize the factors responsible for populations' spatial distribution, which is obviously crucial in the current era of global changes.     

Dispersal capacity explains the evolution of lifespan variability

The evolutionary explanation for lifespan variation is still based on the antagonistic pleiotropy hypothesis, which has been challenged by several studies. Alternative models assume the existence of genes that favor aging and group benefits at the expense of reductions in individual lifespans. Here we propose a new model without making such assumptions. It considers that limited dispersal can generate, through reduced gene flow, spatial segregation of individual organisms according to lifespan. Individuals from subpopulations with shorter lifespan could thus resist collapse in a growing population better than individuals from subpopulations with longer lifespan, hence reducing lifespan variability within species. As species that disperse less may form more homogeneous subpopulations regarding lifespan, this may lead to a greater capacity to maximize lifespan that generates viable subpopulations, therefore creating negative associations between dispersal capacity and lifespan across species. We tested our model with individual‐based simulations and a comparative study using empirical data of maximum lifespan and natal dispersal distance in 26 species of birds, controlling for the effects of genetic variability, body size, and phylogeny. Simulations resulted in maximum lifespans arising from lowest dispersal probabilities, and comparative analyses resulted in a negative association between lifespan and natal dispersal distance, thus consistent with our model. Our findings therefore suggest that the evolution of lifespan variability is the result of the ecological process of dispersal.     

Increased lifetime reproductive success for Siberian jay (Perisoreus infaustus) males with delayed dispersal

In a crowded environment the natal territory could serve as a haven for young and inexperienced offspring until a breeding vacancy emerges. Delayed dispersal and association with kin could then offer adaptive benefits through an individual fitness gain. Here we report that delayed dispersal is associated with a higher lifetime individual fitness in Siberian jay (Perisoreus infaustus) males. Sons bred more successfully and had more reproductive events in life when they delayed dispersal. The higher lifetime reproductive success when sons disperse later in life is sufficient to promote postponement of natal dispersal, suggesting that dispersal is delayed due to ecological constraints on access to high-quality habitats. We argue that the maintenance of this variation in the timing of dispersal and reproductive success can be reconciled with non-genetic mechanisms driving dispersal. Social dominance within broods reflecting environmental conditions during growth is such a mechanism.     

The evolution of an 'intelligent' dispersal strategy: biased, correlated random walks in patchy landscapes

Theoretical work exploring dispersal evolution focuses on the emigration rate of individuals and typically assumes that movement occurs either at random to any other patch or to one of the nearest‐neighbour patches. There is a lack of work exploring the process by which individuals move between patches, and how this process evolves. This is of concern because any organism that can exert control over dispersal direction can potentially evolve efficiencies in locating patches, and the process by which individuals find new patches will potentially have major effects on metapopulation dynamics and gene flow. Here, we take an initial step towards filling this knowledge gap. To do this we constructed a continuous space population model, in which individuals each carry heritable trait values that specify the characteristics of the biased correlated random walk they use to disperse from their natal patch. We explore how the evolution of the random walk depends upon the cost of dispersal, the density of patches in the landscape, and the emigration rate. The clearest result is that highly correlated walks always evolved (individuals tended to disperse in relatively straight lines from their natal patch), reflecting the efficiency of straight‐line movement. In our models, more costly dispersal resulted in walks with higher correlation between successive steps. However, the exact walk that evolved also depended upon the density of suitable habitat patches, with low density habitat evolving more biased walks (individuals which orient towards suitable habitat at quite large distances from that habitat). Thus, low density habitat will tend to develop individuals which disperse efficiently between adjacent habitat patches but which only rarely disperse to more distant patches; a result that has clear implications for metapopulation theory. Hence, an understanding of the movement behaviour of dispersing individuals is critical for robust long‐term predictions of population dynamics in fragmented landscapes.     

The evolution of dispersal – the importance of information about population density and habitat characteristics

The evolution of mobility patterns and dispersal strategies depend on different population, habitat and life history characteristics. The ability to perceive and make use of information about the surrounding environment for dispersal decisions will also differ between organisms. To investigate the evolutionary consequences of such differences, we have used a simulation model with nearest-neighbour dispersal in a metapopulation to study how variation in the ability to obtain and make use of information about habitat quality and conspecific density affects the evolution of dispersal strategies. We found a rather strong influence of variation in information on the overall rate of dispersal in a metapopulation. The highest emigration rate evolved in organisms with no information about either density or habitat quality and the lowest rate was found in organisms with information about both the natal and the neighbouring patches. For organisms that can make use of information about conspecific density, positively density-dependent dispersal evolved in the majority of cases, with the strongest density dependence occurring when an individual only has information about density in the natal patch. However, we also identified situations, involving strong local population fluctuations and frequent local extinctions, where negatively density-dependent dispersal evolved.     

Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations

There is accumulating evidence that individuals leave their natal area and select a breeding habitat non-randomly by relying upon information about their natal and future breeding environments. This variation in dispersal is not only based on external information (condition dependence) but also depends upon the internal state of individuals (phenotype dependence). As a consequence, not all dispersers are of the same quality or search for the same habitats. In addition, the individual's state is characterized by morphological, physiological or behavioural attributes that might themselves serve as a cue altering the habitat choice of conspecifics. These combined effects of internal and external information have the potential to generate complex movement patterns and could influence population dynamics and colonization processes. Here, we highlight three particular processes that link condition-dependent dispersal, phenotype-dependent dispersal and habitat choice strategies: (1) the relationship between the cause of departure and the dispersers' phenotype; (2) the relationship between the cause of departure and the settlement behaviour and (3) the concept of informed dispersal, where individuals gather and transfer information before and during their movements through the landscape. We review the empirical evidence for these processes with a special emphasis on vertebrate and arthropod model systems, and present case studies that have quantified the impacts of these processes on spatially structured population dynamics. We also discuss recent literature providing strong evidence that individual variation in dispersal has an important impact on both reinforcement and colonization success and therefore must be taken into account when predicting ecological responses to global warming and habitat fragmentation.     

Natal habitat effects drive density—dependent scaling of dispersal decisions

The dispersal behavior of a species is critical for the stability and persistence of its populations across a landscape. How population density affects dispersal decisions is important for predicting these dynamics, as the form of density‐dependent dispersal influences the stability and persistence of populations. Natal habitat experience often has strong impacts on individual dispersal behavior as well, but its influence on density‐dependent dispersal behaviors remains unexplored. Here we address this conceptual gap in two experiments separately examining habitat selection and emigration from recently colonized patches for two species of flour beetle Tribolium sp. We found that interactions between the quality of habitat experienced during natal development and current habitat for dispersal capable adults can strongly affect the form of density dependence, including reversing the direction of nonlinearities (accelerating to decelerating), or even negating the influence of population density for individual dispersal decisions. Across heterogeneous landscapes, where individuals from different populations may experience different natal habitats, this altering of density‐dependent relationships is predicted by theory to fundamentally influence regional population dynamics. Our results indicate that species which occur across heterogeneous environments, such as during conservation reintroductions, or as invasive species spread, have much potential for natal experience to interact with density dependence and influence local and regional population dynamics.     

The Influence of Incubation Conditions and Sex on Growth and Dispersal in Hatchling Lizards

Dispersal is a critical process that has profound influence on ecological and evolutionary processes. Many proximate factors influence natal dispersal, but it is currently unclear whether the conditions experienced during incubation play an important role. We manipulated incubation temperature and used mark–recapture of released hatchlings to test this hypothesis. We tested this hypothesis on the prairie lizard (Sceloporus consobrinus) using two experimental islands in a local reservoir. Incubation conditions influenced some aspects of hatchling morphology, but had little influence on the probability of dispersal. As generally predicted for a polygynous species, males were more likely to disperse than females; however, the growth rate of dispersing vs. resident individuals varied depending on sex. Dispersive male lizards did not grow faster than resident males, whereas female dispersers grew significantly slower than resident females. Although our study was not specifically designed to test for differential costs of dispersal for males and females, this pattern is consistent with recent research demonstrating sex‐specific fitness costs of dispersal.     

Evolution of complex dynamics in spatially structured populations

Dynamics of populations depend on demographic parameters which may change during evolution. In simple ecological models given by one-dimensional difference equations, the evolution of demographic parameters generally leads to equilibrium population dynamics. Here we show that this is not true in spatially structured ecological models. Using a multi-patch metapopulation model, we study the evolutionary dynamics of phenotypes that differ both in their response to local crowding, i.e. in their competitive behaviour within a habitat, and in their rate of dispersal between habitats. Our simulation results show that evolution can favour phenotypes that have the intrinsic potential for very complex dynamics provided that the environment is spatially structured and temporally variable. These phenotypes owe their evolutionary persistence to their large dispersal rates. They typically coexist with phenotypes that have low dispersal rates and that exhibit equilibrium dynamics when alone. This coexistence is brought about through the phenomenon of evolutionary branching, during which an initially uniform population splits into the two phenotypic classes.     

Density, social information, and space use in the common lizard (Lacerta vivipara)

Socially acquired information is widespread in the animal kingdom.Many individuals make behavioral decisions based on such socialinformation. In particular, individuals may decide to leaveor select their habitat based on social information. Few studieshave investigated the role of density-related information, apotential social cue about habitat quality in dispersal. Here,we tested for the possibility that the phenotype of intrudercommon lizards (Lacerta vivipara) may inadvertently carry informationabout their natal population density. We found that such informationuse is likely. The behavior of focal lizard was influenced bythe natal population density of the intruder it was interactingwith. This suggests that individuals may use the behavior ofothers to acquire appropriate information about surroundingsand to base spatial decisions on this information. Density-relatedinformation may then affect individual movement decisions andthus metapopulation dynamics.     

A modeling exercise to show why population models should incorporate distinct life histories of dispersers

Dispersal is an important form of movement influencing population dynamics, species distribution and gene flow between populations. In population models, dispersal is often included in a simplified manner by removing a random proportion of the population. Many ecologists now argue that models should be formulated at the level of individuals instead of the population level. To fully understand the effects of dispersal on natural systems, it is therefore necessary to incorporate individual-level differences in dispersal behavior in population models. Here, we parameterized an integral projection model, which allows for studying how individual life histories determine population-level processes, using bulb mites, Rhizoglyphus robini, to assess to what extent dispersal expression (frequency of individuals in the dispersal stage) and dispersal probability affect the proportion of successful dispersers and natal population growth rate. We find that allowing for life-history differences between resident phenotypes and disperser phenotypes shows that multiple combinations of dispersal probability and dispersal expression can produce the same proportion of leaving individuals. Additionally, a given proportion of successful dispersing individuals result in different natal population growth rates. The results highlight that dispersal life histories, and the frequency with which disperser phenotypes occur in the natal population, significantly affect population-level processes. Thus, biological realism of dispersal population models can be increased by incorporating the typically observed life-history differences between resident phenotypes and disperser phenotypes, and we here present a methodology to do so.     

Mating timing,dispersal and local adaptation in patchy environments

Dispersal is a life‐history trait that can evolve under various known selective pressures as identified by a multitude of theoretical and empirical studies. Yet only few of them are considering the succession of mating and dispersal. The sequence of these events influences gene flow and consequently affects the dynamics and evolution of populations. We use individual‐based simulations to investigate the evolution of the timing of dispersal and mating, i.e. mating before or after dispersal. We assume a discrete insect metapopulation in a heterogeneous environment, where populations may adapt to local conditions and only females are allowed to disperse. We run the model assuming different levels of species habitat tolerance, carrying capacity, and temporal environmental variability. Our results show that in species with narrow habitat tolerance, low to moderate dispersal evolves in combination with mating after dispersal (post‐dispersal mating). With such a strategy dispersing females benefit from mating with a resident male, as their offspring will be better adapted to the local habitat conditions. On the contrary, in species with wide habitat tolerance higher dispersal rates in combination with pre‐dispersal mating evolves. In this case individuals are adapted to the ‘average’ habitat where pre‐dispersal mating conveys the benefit of carrying relatives’ genes into a new population. With high dispersal rates and large population size, local adaptation and kin structure both vanish and the temporal sequence of dispersal and mating may become a (nearly) neutral trait.