Conditional dispersal, clines, and the evolution of dispersiveness

Conditional dispersal, in which an individual’s decision over whether to disperse is a response to environmental conditions, features prominently in studies of dispersal evolution. Using models of clines, I examine how one widely discussed cost of dispersal, namely, that dispersal impedes local adaptation, changes with conditional dispersal and what this implies for dispersal evolution. I examine the consequences for dispersal evolution of the responsiveness of dispersal to the environment, the accuracy of any proximal cues that individuals rely upon to assess habitat quality, and whether dispersal responds to fitness itself or only to some fitness components (juvenile survivorship). All of the conditional dispersal behaviors that I consider weaken the indirect cost of dispersal inhibiting local adaptation. However, if individuals rely on imprecise cues to assess habitat quality and base dispersal decisions on juvenile survivorship, then conditional dispersal can incur additional costs by exacerbating overcrowding. Conditional dispersal initially leads to steeper clines in traits under direct selection, but when dispersiveness can itself evolve, conditional dispersal allows sigmoidal clines to persist long after those obtained with unconditional movement would become stepped. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Disturbance induces the contrasting evolution of reinforcement and dispersiveness in directed and random movers

Spatial models commonly assume that dispersal rates are constant across individuals and environments and that movement directions are unbiased. These random-movement assumptions are inadequate to capture the range of dispersal behaviors revealed in diverse case studies. We examine an alternative assumption of directed movement, in which dispersal is a conditional and directional response by individuals to varying environmental conditions. Specifically, we assume individuals bias their movements to climb spatial fitness gradients. We compare the consequences of random and directed movement for local adaptation, the evolution of dispersal, and the reinforcement process. The implications of each movement strategy depend on the nature of environmental disturbance, and we examine the outcomes for undisturbed environments and with uncorrelated and autocorrelated disturbances. Both movement strategies offer advantages over sedentary life histories by allowing colonization of suitable habitats. However, random movement eventually becomes costly in stable environments because it inhibits local adaptation. In contrast, directed movement accelerates local adaptation. In disturbed environments, random movement offers bet-spreading advantages by distributing offspring across habitats. Despite being a more targeted strategy, an intermediate amount of directed movement provides similar bet-spreading benefits. These fitness consequences have implications for the evolution of dispersal. Dispersiveness is lost by random movers in undisturbed environments, is maintained in polymorphism with infrequent disturbances, and evolves when disturbances are uncorrelated. Directed movement becomes selectively neutral in the absence of disturbance, evolves when disturbances are autocorrelated, and is maintained in polymorphism with uncorrelated disturbances. Disturbance also determines the outcome of the reinforcement process for each strategy. For example, directed movers show no progress toward reinforcement in undisturbed environments, evolve random mating with uncorrelated disturbances, and can evolve assortative mating in infrequently disturbed environments.     

Life on the edge: a hybrid zone in AZbinaria hippolyti (Gastropoda: Clausiliidae) from Crete

The hybrid zone between the Greek land snails Albinaria hippolyti aphrodite and Albinaria hippolyti harmonia runs exactly along the edge of a gorge. At two localities, we analysed patterns of variation in three enzyme loci, six conchological characters, and two anatomical characters across the zone. Clines in the various characters are largely coincident and concordant. They are narrow (approximately 30 m wide) where the ecological transition is abrupt, and wider (approximately 120 m wide) where a valley cuts into the gorge, making the environmental change more gradual. In spite of the obvious correlation with an ecological transition, we do not believe the zone is maintained by a selection gradient. Instead, direct and indirect evidence for hybrid disadvantage and evidence for directional dispersal at the edge of the gorge suggest that it is a tension zone, held at the ecotone by differential dispersal of at least one of the parental types. We speculate on the possibility that reinforcement may act in the hybrid zone. Our data on dispersal and reproductive isolating mechanisms lead us to believe that reinforcement may only be possible at localities where the hybrid zone is very narrow.     

Evolution of body condition‐dependent dispersal in metapopulations

Body condition‐dependent dispersal strategies are common in nature. Although it is obvious that environmental constraints may induce a positive relationship between body condition and dispersal, it is not clear whether positive body conditional dispersal strategies may evolve as a strategy in metapopulations. We have developed an individual‐based simulation model to investigate how body condition–dispersal reaction norms evolve in metapopulations that are characterized by different levels of environmental stochasticity and dispersal mortality. In the model, body condition is related to fecundity and determined either by environmental conditions during juvenile development (adult dispersal) or by those experienced by the mother (natal dispersal). Evolutionarily stable reaction norms strongly depend on metapopulation conditions: positive body condition dependency of dispersal evolved in metapopulation conditions with low levels of dispersal mortality and high levels of environmental stochasticity. Negative body condition‐dependent dispersal evolved in metapopulations with high dispersal mortality and low environmental stochasticity. The latter strategy is responsible for higher dispersal rates under kin competition when dispersal decisions are based on body condition reached at the adult life stage. The evolution of both positive and negative body condition‐dependent dispersal strategies is consequently likely in metapopulations and depends on the prevalent environmental conditions.     

Genomics,environment and balancing selection in behaviourally bimodal populations: The caribou case

Selection forces that favour different phenotypes in different environments can change frequencies of genes between populations along environmental clines. Clines are also compatible with balancing forces, such as negative frequency‐dependent selection (NFDS), which maintains phenotypic polymorphisms within populations. For example, NFDS is hypothesized to maintain partial migration, a dimorphic behavioural trait prominent in species where only a fraction of the population seasonally migrates. Overall, NFDS is believed to be a common phenomenon in nature, yet a scarcity of studies were published linking naturally occurring allelic variation with bimodal or multimodal phenotypes and balancing selection. We applied a Pool‐seq approach and detected selection on alleles associated with environmental variables along a North–South gradient in western North American caribou, a species displaying partially migratory behaviour. On 51 loci, we found a signature of balancing selection, which could be related to NFDS and ultimately the maintenance of the phenotypic polymorphisms known within these populations. Yet, remarkably, we detected directional selection on a locus when our sample was divided into two behaviourally distinctive groups regardless of geographic provenance (a subset of GPS‐collared migratory or sedentary individuals), indicating that, within populations, phenotypically homogeneous groups were genetically distinctive. Loci under selection were linked to functional genes involved in oxidative stress response, body development and taste perception. Overall, results indicated genetic differentiation along an environmental gradient of caribou populations, which we found characterized by genes potentially undergoing balancing selection. We suggest that the underlining balancing force, NFDS, plays a strong role within populations harbouring multiple haplotypes and phenotypes, as it is the norm in animals, plants and humans too.     

Clinal variation in Drosophila serrata for stress resistance and body size

Clines for size and stress resistance traits have been described for several Drosophila species and replicable clines across different species may indicate climatic selection. Here we consider clines in stress resistance traits in an Australian endemic species, D. serrata, by comparing levels of variation within and among isofemale lines initiated with flies collected from the eastern coast of Australia. We also consider clinical variation in chill coma recovery, a trait that has recently been shown to exhibit high levels of variation among Drosophila species. Patterns were compared with those in the cosmopolitan species D. melanogaster from the same area. Both desiccation and starvation resistance showed no clinical pattern despite heritable variation among isofemale lines. In contrast chill coma resistance exhibited a linear cline in the anticipated direction, resistance increasing with latitude. Body size was measured as wing length and body weight. Both traits showed geographic variation and strong non-linear clines with a sharp reduction in size in the tropics. These results are discussed in the context of climatic selection and evolutionary processes limiting species borders.     

Dispersal potential impacts size clines of grasshoppers across an elevation gradient

Body size is a life history trait that determines the reproductive success of a variety of organisms. Changes in body size may have a genetic component when persistent conditions such as season length and climate select for individuals of an optimal body size and an environmental component when it is influenced on an ecological scale by factors such as weather, food availability, or maternal effects. Along elevational gradients that experience seasonality, insects commonly become smaller with increases in elevation. In this study we test the hypothesis that dispersal potential, an indicator of gene flow, impacts the type of size clines exhibited by insects along elevational gradients and that these differences in local adaptation should lead to predictable changes in their reproductive potential and output. Using two short winged grasshopper species, Aeropedellus clavatus and Melanoplus boulderensis, and two long winged species, Camnula pellucida and Melanoplus sanguinipes, we showed that species with low dispersal potential are associated with significant declines in body size with increases in elevation while species with high dispersal potential displayed no size clines. Consistent with short winged species being more locally adapted, we show that reproductive potential, as measured by the proportion of ovarioles that become functional, do not differ among populations of short winged species, but decline with elevation in the long winged species. While our study failed to show that dispersal potential impacts reproductive output in a consistent and predictable manner (as measured by clutch and egg sizes), we address the possibility that clutch size may not reflect changes in total reproductive output and that changes in egg size may be a plastic trait. We concluded that studies exploring the evolution of body size, the reproductive capacity and species level responses to environmental change should note the importance of dispersal potential in influencing these patterns.     

Morphological clines in dendritic landscapes

1. In complex landscapes such as river networks, organisms usually face spatio‐temporal heterogeneity and gradients in geomorphological, water, ecological or landscape characteristics are often observed at the catchment scale. These environmental variables determine developmental conditions for larval stages of freshwater insects and influence adult phenotypic characteristics. Environmental clines are therefore expected to generate morphological clines. Such a process has the potential to drive gradual geographical change in morphology‐dependent life history traits, such as dispersal. 2. We studied the influence of aquatic and terrestrial environmental factors on morphological variations in Calopteryx splendens across the Loire drainage. To investigate these effects we took explicitly into account the hierarchical structure of the river network. 3. We analysed eight morphological traits. Results showed significant body size variation between tributaries and the presence of a morphological cline at the drainage scale. We observed an effect of pH and water temperature on body size. Individuals in downstream sites were larger than individuals in upstream sites, and adults whose larval stages were exposed to alkaline pH and high temperatures during summer were larger. 4. Body size affects flight abilities in insects. Thus, our results suggest that morphological clines may generate an asymmetric dispersal pattern along the downstream–upstream axis, downstream populations dispersing farther than upstream ones. Such a process is expected to influence population genetic structure at the drainage scale if larval drift and floods do not balance an asymmetrical dispersal pattern of adults along the downstream–upstream gradient. To assess the influence of environmental gradients on the variation of life history traits it is important to understand the population biology of freshwater insects, and more generally of riverine organisms. It is also essential to integrate such data in conservation or restoration programmes.     

THE JOINT EVOLUTION OF DISPERSAL AND DORMANCY IN A METAPOPULATION WITH LOCAL EXTINCTIONS AND KIN COMPETITION

Dispersal and dormancy are two strategies that allow recolonization of empty patches and escape from kin competition. Because they presumably respond to similar evolutionary forces, it is tempting to consider that these strategies may substitute for each other. Yet in order to predict the outcome of the evolution of dispersal and dormancy, and to characterize the emerging covariation between both traits, it is necessary to consider models where dispersal and dormancy evolve jointly. Here, we analyze the evolution of dispersal and dormancy as a function of direct fitness costs, environmental variation, and competition among relatives. We consider two scenarios depending on whether the rates of dormancy for philopatric and dispersed individuals are constrained to be the same (unconditional dormancy) or allowed to be different (conditional dormancy). We show that only philopatric individuals should enter dormancy, at a rate increasing with increasing rates of local extinction and decreasing population sizes. When dormancy and dispersal evolve jointly, we observe a wide range of evolutionary outcomes. In particular, we find that the pattern of covariation between the evolutionarily stable rates of dispersal and dormancy is molded by the rate of extinction and the local population size.     

Environmental conditions affect spatial genetic structures and dispersal patterns in a solitary rodent

The study of the spatial distribution of relatives in a population under contrasted environmental conditions provides critical insights into the flexibility of dispersal behaviour and the role of environmental conditions in shaping population relatedness and social structure. Yet few studies have evaluated the effects of fluctuating environmental conditions on relatedness structure of solitary species in the wild. The aim of this study was to determine the impact of interannual variations in environmental conditions on the spatial distribution of relatives [spatial genetic structure (SGS)] and dispersal patterns of a wild population of eastern chipmunks (Tamias striatus), a solitary rodent of North America. Eastern chipmunks depend on the seed of masting trees for reproduction and survival. Here, we combined the analysis of the SGS of adults with direct estimates of juvenile dispersal distance during six contrasted years with different dispersal seasons, population sizes and seed production. We found that environmental conditions influences the dispersal distances of juveniles and that male juveniles dispersed farther than females. The extent of the SGS of adult females varied between years and matched the variation in environmental conditions. In contrast, the SGS of males did not vary between years. We also found a difference in SGS between males and females that was consistent with male‐biased dispersal. This study suggests that both the dispersal behaviour and the relatedness structure in a population of a solitary species can be relatively labile and change according to environmental conditions.     

Maintenance of clinal variation for shell colour phenotype in the flat periwinkle Littorina obtusata

Clines can signal spatially varying selection and therefore have long been used to investigate the role of environmental heterogeneity in maintaining genetic variation. However, clinal patterns alone are not sufficient to reject neutrality or to establish the mechanism of selection. Indirect, inferential methods can be used to address neutrality and mechanism, but fully understanding the adaptive significance of clinal variation ultimately requires a direct approach. Ecological model systems such as the rocky intertidal provide a useful context for direct experimentation and can serve as a complement to studies in more traditional genetic model systems. In this study, we use indirect and direct approaches to investigate the role of environmental heterogeneity in the maintenance of shell colour polymorphism in the flat periwinkle snail, Littorina obtusata. We document replicated clines in shell colour morph frequencies over thermal gradients at two spatial scales, contrasting with patterns at previously reported microsatellite loci. In addition, experimental results demonstrate that that shell colour has predictable effects on shell temperature and that these differences in temperature, in turn, coincide with patterns of survivorship under episodic thermal stress. Direct manipulation of shell colour revealed that shell colour, and not a correlated character, was the target of selection. Our study provides evidence that spatially varying selection via thermal regime contributes to the maintenance of shell colour phenotype variation in L. obtusata in the sampled areas of the Gulf of Maine.     

Adaptation to a steep environmental gradient and an associated barrier to gene exchange in Littorina saxatilis

Steep environmental gradients offer important opportunities to study the interaction between natural selection and gene flow. Allele frequency clines are expected to form at loci under selection, but unlinked neutral alleles may pass easily across these clines unless a generalized barrier evolves. Here we consider the distribution of forms of the intertidal gastropod Littorina saxatilis, analyzing shell shape and amplified fragment length polymorphism (AFLP) loci on two rocky shores in Britain. On the basis of previous work, the AFLP loci were divided into differentiated and undifferentiated groups. On both shores, we have shown a sharp cline in allele frequencies between the two morphs for differentiated AFLP loci. This is coincident with a habitat transition on the shore where the two habitats (cliff and boulder field) are immediately contiguous. The allele frequency clines coincide with a cline in shell morphology. In the middle of the cline, linkage disequilibrium for the differentiated loci rises in accordance with expectation. The clines are extremely narrow relative to dispersal, probably as a result of both strong selection and habitat choice. An increase in F(ST) for undifferentiated AFLPs between morphs, relative to within-morph comparisons, is consistent with there being a general barrier to gene flow across the contact zone. These features are consistent either with an episode of allopatric divergence followed by secondary contact or with primary, nonallopatric divergence. Further data will be needed to distinguish between these alternatives.     

Uncertainty and the role of information acquisition in the evolution of context-dependent emigration

There is increasing empirical evidence that individuals utilize social and environmental cues in making decisions as to whether or not to disperse. However, we lack theory exploring the influence of information acquisition and use on the evolution of dispersal strategies and metapopulation dynamics. We used an individual-based, spatially explicit simulation model to explore the evolution of emigration strategies under varying precision of information about the natal patch, cost of information acquisition, and environmental predictability. Our findings show an interesting interplay between information use and the evolved emigration propensity. Lack of information led to higher emigration probabilities in more unpredictable environments but to lower emigration probabilities in constant or highly predictable scenarios. Somewhat-informed dispersal strategies were selected for in most cases, even when the acquisition of information was associated with a moderate reproductive cost. Notably, selection rarely favored investment in acquisition of high-precision information, and the tendency to invest in information acquisition was greatest in predictable environments when the associated cost was low. Our results highlight that information use can affect dispersal in a complex manner and also emphasize that information-acquisition behaviors can themselves come under strong selection, resulting in evolutionary dynamics that are tightly coupled to those of context-dependent behaviors.     

The impact of directed versus random movement on population dynamics and biodiversity patterns

An improved understanding of dispersal behavior is needed to predict how populations and communities respond to habitat fragmentation. Most spatial dynamic theory concentrates on random dispersal, in which movement rates depend neither on the state of an individual nor its environment and movement directions are unbiased. We examine the neglected dispersal component of directed movement in which dispersal is a conditional and directional response of individuals to varying environmental conditions. Specifically, we assume that individuals bias their movements along local gradients in fitness. Random movers, unable to track heterogeneous environmental conditions, face source-sink dynamics, which can result in deterministic extinction or increase their vulnerability to stochastic extinction. Directed movers track environmental conditions closely. In fluctuating environments, random movers "spread their bets" across patches, while directed movers invest offspring in habitats currently enjoying propitious conditions. The autocorrelation in the environment determines each strategy's success. Random movers permeate entire landscapes, but directed movers are more geographically constrained. Local information constraints limit the ranges of directed movers and introduce a role for historical contingency in determining their ultimate distribution. These geographic differences have implications for biodiversity. Random movement maintains biodiversity through local coexistence, but directed movement favors a spatial partitioning of species.     

Evolution of dispersal in open advective environments

We consider a two-species competition model in a one-dimensional advective environment, where individuals are exposed to unidirectional flow. The two species follow the same population dynamics but have different random dispersal rates and are subject to a net loss of individuals from the habitat at the downstream end. In the case of non-advective environments, it is well known that lower diffusion rates are favored by selection in spatially varying but temporally constant environments, with or without net loss at the boundary. We consider several different biological scenarios that give rise to different boundary conditions, in particular hostile and “free-flow” conditions. We establish the existence of a critical advection speed for the persistence of a single species. We derive a formula for the invasion exponent and perform a linear stability analysis of the semi-trivial steady state under free-flow boundary conditions for constant and linear growth rate. For homogeneous advective environments with free-flow boundary conditions, we show that populations with higher dispersal rate will always displace populations with slower dispersal rate. In contrast, our analysis of a spatially implicit model suggest that for hostile boundary conditions, there is a unique dispersal rate that is evolutionarily stable. Nevertheless, both scenarios show that unidirectional flow can put slow dispersers at a disadvantage and higher dispersal rate can evolve.     

Can Diversifying Selection Be Distinguished from History in Geographic Clines? A Population Genomic Study of Killifish (Fundulus heteroclitus)

A common geographical pattern of genetic variation is the one-dimensional cline. Clines may be maintained by diversifying selection across a geographical gradient but can also reflect historical processes such as allopatry followed by secondary contact. To identify loci that may be undergoing diversifying selection, we examined the distribution of geographical variation patterns across the range of the killifish (Fundulus heteroclitus) in 310 loci, including microsatellites, allozymes, and single nucleotide polymorphisms. We employed two approaches to detect loci under strong diversifying selection. First, we developed an automated method to identify clinal variation on a per-locus basis and examined the distribution of clines to detect those that exhibited signifcantly steeper slopes. Second, we employed a classic -outlier method as a complementary approach. We also assessed performance of these techniques using simulations. Overall, latitudinal clines were detected in nearly half of all loci genotyped (i.e., all eight microsatellite loci, 12 of 16 allozyme loci and 44% of the 285 SNPs). With the exception of few outlier loci (notably mtDNA and malate dehydrogenase), the positions and slopes of Fundulus clines were statistically indistinguishable. The high frequency of latitudinal clines across the genome indicates that secondary contact plays a central role in the historical demography of this species. Our simulation results indicate that accurately detecting diversifying selection using genome scans is extremely difficult in species with a strong signal of secondary contact; neutral evolution under this history produces clines as steep as those expected under selection. Based on these results, we propose that demographic history can explain all clinal patterns observed in F. heteroclitus without invoking natural selection to either establish or maintain the pattern we observe today.     

Juvenile Female Aggression in Cooperatively Breeding Pied Babblers: Causes and Contexts

Sex biases in adult aggression have been well studied and commonly arise when resources which affect survival or lifetime reproductive success are less abundant or more valuable for individuals of one sex. Despite the prevalence of sex biases in adult aggression, evidence for sex biases in juvenile aggression is scant. Here, we present evidence for female‐biased juvenile aggression in cooperatively breeding pied babblers (Turdoides bicolor). Unlike most cases of non‐lethal sibling aggression, juvenile aggression in pied babblers does not seem to be determined by food availability. Instead, we found that juvenile aggression was related to adult dispersal patterns. This study shows that females that were more aggressive as juveniles attempted dispersal earlier than less aggressive females. Potential explanations for the association between juvenile aggression and adult dispersal patterns are discussed.     

Evolution of density- and patch-size-dependent dispersal rates

Based on a marginal value approach, we derive a nonlinear expression for evolutionarily stable (ES) dispersal rates in a metapopulation with global dispersal. For the general case of density-dependent population growth, our analysis shows that individual dispersal rates should decrease with patch capacity and-beyond a certain threshold-increase with population density. We performed a number of spatially explicit, individual-based simulation experiments to test these predictions and to explore further the relevance of variation in the rate of population increase, density dependence, environmental fluctuations and dispersal mortality on the evolution of dispersal rates. They confirm the predictions of our analytical approach. In addition, they show that dispersal rates in metapopulations mostly depend on dispersal mortality and inter-patch variation in population density. The latter is dominantly driven by environmental fluctuations and the rate of population increase. These conclusions are not altered by the introduction of neighbourhood dispersal. With patch capacities in the order of 100 individuals, kin competition seems to be of negligible importance for ES dispersal rates except when overall dispersal rates are low.     

A plea for simultaneously considering matrix quality and local environmental conditions when analysing landscape impacts on effective dispersal

Landscape genetics has tremendous potential for enhancing our understanding about landscape effects on effective dispersal and resulting genetic structures. However, the vast majority of landscape genetic studies focus on effects of the landscape among sampling locations on dispersal (i.e. matrix quality), while effects of local environmental conditions are rather neglected. Such local environmental conditions include patch size, habitat type or resource availability and are commonly used in (meta‐) population ecology and population genetics. In our opinion, landscape genetic studies would greatly benefit from simultaneously incorporating both matrix quality and local environmental conditions when assessing landscape effects on effective dispersal. To illustrate this point, we first outline the various ways in which environmental heterogeneity can influence different stages of the dispersal process. We then propose a three‐step approach for assessing local and matrix effects on effective dispersal and review how both types of effects can be considered in landscape genetic analyses. Using simulated data, we show that it is possible to correctly disentangle the relative importance of matrix quality vs. local environmental conditions for effective dispersal. We argue that differentiating local and matrix effects in such a way is crucial for predicting future species distribution and persistence, and for optimal conservation decisions that are based on landscape genetics. In sum, we think it is timely to move beyond purely statistical, pattern‐oriented analyses in landscape genetics and towards process‐oriented approaches that consider the full range of possible landscape effects on dispersal behaviour and resulting gene flow.     

Processes at the origin of similarities in dispersal behaviour among siblings

Processes which generate natal dispersal are largely unknown. This is particularly the case for the sources of differences among families. Three types of processes can generate the variability among families: genetic, prenatal and postnatal. We first tested the family resemblance of dispersal behaviour in the common lizard (Lacerta vivipara). We then experimentally investigated the role of pre‐ and postnatal factors in the variability of dispersal among families. From 1989 to 1992, we studied dispersal of juveniles from pregnant females captured in the field and maintained in laboratory until parturition. We manipulated the conditions of gestation to test for prenatal effects on juvenile dispersal. We tested postnatal effects by releasing siblings of the same family in contrasted environments. We also examined covariances of natal dispersal with maternal and offspring traits. The results showed that: (1) dispersal behaviour was similar among siblings, (2) determinants of offspring dispersal differed between sexes and years, (3) offspring dispersal was related to litter sex‐ratio and offspring corpulence at birth, (4) postnatal conditions influenced male dispersal, (5) short‐term prenatal conditions (i.e. maternal conditions during gestation) influenced juvenile dispersal, varying per year, (6) long‐term prenatal conditions (i.e. maternal conditions during gestation in the previous year) could also influence juvenile dispersal (marginally significant). Thus, several types of processes determine natal dispersal in the common lizard. Resemblance among siblings can partly be explained by both pre‐ and postnatal effects. The environment seems to be the major factor influencing juvenile dispersal in this species, i.e. dispersal essentially appears condition‐dependent. The genetic basis of dispersal in vertebrates remains to be demonstrated by studies controlling for both prenatal and postnatal conditions.