Maintenance of the sexes and persistence of a clonal organism in spatially complex metapopulations

Clonal organisms persist at a range of population sex ratios, from equal numbers of males and females to single-sex systems. When intersexual competition is strong enough to drive one sex locally extinct, the maintenance of the sexes is facilitated by the semi-independent dynamics of populations within a metapopulation. These semi-independent dynamics are influenced by dispersal and recolonization rates, which are affected by the spatial arrangement of populations. To establish the quantitative relationship between spatially complex metapopulations and the maintenance of the sexes, we used a mathematical model of the liverwort Marchantia inflexa. This clonal organism is found in discrete patches on rocks and along the banks of streams, which form single-sex and two-sex metapopulations. In this system, asexual propagules mainly disperse short distances. Long-distance between-patch dispersal and recolonization mainly occurs via sexual propagules, which require both sexes to be present. Dispersal of these two types of propagules could interact with the spatial arrangement of populations to affect the maintenance of the sexes. With our mathematical model, we found that at intermediate distances between populations, metapopulations maintained both sexes, and the spatial arrangement of populations changed the threshold at which one sex was lost. On the other hand, when populations were close to one another, one sex was lost and the single-sex metapopulation persisted through dispersal of asexual propagules. When populations were far apart, one sex was lost, and the metapopulation either went extinct due to lack of recolonization by asexual propagules or persisted because clumped populations facilitated recolonization. These idealized spatial arrangements help clarify the effects of the spatial arrangement on the maintenance of the sexes and the persistence of metapopulations of clonal organisms, which can help explain geographic parthenogenesis and the distribution of asexual populations, the persistence of asexual species, and inform the conservation of clonal organisms.     

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.     

Multilevel selection and neighbourhood effects from individual to metapopulation in a wild passerine

Multilevel selection has rarely been studied in the ecological context of animal populations, in which neighbourhood effects range from competition among territorial neighbours to source-sink effects among local populations. By studying a Dupont's lark Chersophilus duponti metapopulation, we analyze neighbourhood effects mediated by song repertoires on fitness components at the individual level (life-span) and population level (growth rate). As a sexual/aggressive signal with strong effects on fitness, birdsong creates an opportunity for group selection via neighbour interactions, but may also have population-wide effects by conveying information on habitat suitability to dispersing individuals. Within populations, we found a disruptive pattern of selection at the individual level and an opposite, stabilizing pattern at the group level. Males singing the most complex songs had the longest life-span, but individuals with the poorest repertoires lived longer than 'average' males, a finding that likely reflects two male strategies with respect to fitness and sexual trait expression. Individuals from groups with intermediate repertoires had the longest life-span, likely benefitting from conspecific signalling to attract females up to the detrimental spread of competitive interactions in groups with superior vocal skills. Within the metapopulation selection was directional but again followed opposite patterns at the two levels: Populations had the highest growth rate when inhabiting local patches with complex repertoires surrounded by patches with simple repertoires. Here the song may impact metapopulation dynamics by guiding prospecting individuals towards populations advertising habitat quality. Two fitness components linked to viability were therefore influenced by the properties of the group, and birdsong was the target of selection, contributing to linking social/sexual processes at the local scale with regional population dynamics.     

Optimal life‐history schedule in a metapopulation with juvenile dispersal

Previous models have predicted that when mortality increases with age, older individuals should invest more of their resources in reproduction and produce less dispersive offspring, as both their future reproductive value and their prospect of competing with their own sib decline. Those models assumed stable population sizes. We here study for the first time the evolution of age‐specific reproductive effort and of age‐specific offspring dispersal rate in a metapopulation with extinction‐recolonization dynamics and juvenile dispersal. Our model explores the evolutionary consequences of disequilibrium in the age structure of individuals in local populations, generated by disturbances. Life‐history decisions are then shaped both by changes with age in individual performances, and by changes in ecological conditions, as young and old individuals do not live on average in the same environments. Lower juvenile dispersal favours the evolution of higher reproductive effort in young adults in a metapopulation with extinction‐recolonization compared with a well‐mixed population. Contrary to previous predictions for stable structured populations, we find that offspring dispersal should generally increase with maternal age. This is because young individuals, who are overrepresented in recently colonized populations, should allocate more to reproduction and less to dispersal as a strategy to exploit abundant recruitment opportunities in such populations.     

Fitness-dependent dispersal in metapopulations and its consequences for persistence and synchrony

1. We present a novel metapopulation model where dispersal is fitness dependent: the strength of migration from a site is dependent on the expected reproductive fitness of individuals there. Furthermore, individuals continue to migrate until they reach a suitable habitat where their expected fitness is above a threshold value.
2. Fitness-dependent dispersal has a very strong stabilizing effect on population dynamics, even when the intrinsic dynamics of populations in the absence of dispersal exhibit complex high-amplitude oscillations. This stabilizing effect is much stronger than that of the density-independent dispersal normally considered in metapopulation models.
3. Even when fitness-dependent dispersal does not stabilize the dynamics in a formal sense, it generally leads to simplification, with complex or even chaotic fluctuations being reduced to simple cycles.
4. This form of dispersal also has a strong tendency to synchronize local population dynamics across the spatial extent of the metapopulation.
5. These conclusions are robust to the addition of strong stochasticity in the migration threshold.     

Viability analyses with habitat-based metapopulation models

Population viability analysis (PVA) models incorporate spatial dynamics in different ways. At one extreme are the occupancy models that are based on the number of occupied populations. The simplest occupancy models ignore the location of populations. At the other extreme are individual-based models, which describe the spatial structure with the location of each individual in the population, or the location of territories or home ranges. In between these are spatially structured metapopulation models that describe the dynamics of each population with structured demographic models and incorporate spatial dynamics by modeling dispersal and temporal correlation among populations. Both dispersal and correlation between each pair of populations depend on the location of the populations, making these models spatially structured. In this article, I describe a method that expands spatially structured metapopulation models by incorporating information about habitat relationships of the species and the characteristics of the landscape in which the metapopulation exists. This method uses a habitat suitability map to determine the spatial structure of the metapopulation, including the number, size, and location of habitat patches in which subpopulations of the metapopulation live. The habitat suitability map can be calculated in a number of different ways, including statistical analyses (such as logistic regression) that find the relationship between the occurrence (or, density) of the species and independent variables which describe its habitat requirements. The habitat suitability map is then used to calculate the spatial structure of the metapopulation, based on species-specific characteristics such as the home range size, dispersal distance, and minimum habitat suitability for reproduction. Received: April 1, 1999 / Accepted: October 29, 1999     

Classical metapopulation dynamics and eco‐evolutionary feedbacks in dendritic networks

Eco‐evolutionary dynamics are now recognized to be highly relevant for population and community dynamics. However, the impact of evolutionary dynamics on spatial patterns, such as the occurrence of classical metapopulation dynamics, is less well appreciated. Here, we analyse the evolutionary consequences of spatial network connectivity and topology for dispersal strategies and quantify the eco‐evolutionary feedback in terms of altered classical metapopulation dynamics. We find that network properties, such as topology and connectivity, lead to predictable spatio‐temporal correlations in fitness expectations. These spatio‐temporally stable fitness patterns heavily impact evolutionarily stable dispersal strategies and lead to eco‐evolutionary feedbacks on landscape level metrics, such as the number of occupied patches, the number of extinctions and recolonizations as well as metapopulation extinction risk and genetic structure. Our model predicts that classical metapopulation dynamics are more likely to occur in dendritic networks, and especially in riverine systems, compared to other types of landscape configurations. As it remains debated whether classical metapopulation dynamics are likely to occur in nature at all, our work provides an important conceptual advance for understanding the occurrence of classical metapopulation dynamics which has implications for conservation and management of spatially structured populations.     

Sexual systems and population genetic structure in an annual plant: testing the metapopulation model

The need for reproductive assurance during dispersal, along with the pressure of local mate competition, means that the importance of frequent or repeated colonization is implicit in the literature on sexual system evolution. However, there have been few empirical tests of the association between colonization history and sexual system in plants, and none within a single species. Here we use patterns of genetic diversity to provide such a test in the Mercurialis annua species complex, which spans the range of systems from self-compatible monoecy through androdioecy to dioecy. This variation has been hypothesized to result from differing patterns of metapopulation turnover and recolonization. Because monoecy should be favored during colonization, androdioecy and dioecy will be maintained only in regions with low rates of local extinction and recolonization, and these differences should also be reflected in patterns of neutral genetic diversity. We show that monoecious populations of M. annua display lower within-population genetic diversity than androdioecious populations and higher genetic differentiation than dioecious and androdioecious populations, as predicted by metapopulation models. In contrast, regional diversity in M. annua appears to be primarily a product of postglacial range expansion from two refugia in the eastern and western Mediterranean Basin.     

Inbreeding depresses short and long distance dispersal in three congeneric spiders

Dispersal is one of the most important precopulatory inbreeding avoidance mechanisms and subject to landscape related selection pressures. In small populations, inbreeding within and between populations may strongly affect population dynamics if it reduces fitness and gene‐flow. While inbreeding avoidance is generally considered to be a key evolutionary driver of dispersal, potential effects of inbreeding on the dispersal process, are poorly known. Here, I document how inbreeding within a population, so by mating among relatives, affects the survivorship and the dispersal behaviour of three congeneric spider Erigone species (Araneae: Linyphiidae) that differ in habitat preference and regional rarity. The three species were chosen as a model because they allow the assessment of both long and short distance dispersal motivation (respectively ballooning and rappelling) under laboratory conditions. Inbreeding reduced both long and short distance dispersal modes in the three congeneric species. Because survival was depressed after inbreeding, with a tendency of reduced survival loss in the rare and highly stenotopic species, energetic constraints are likely to be the underlying mechanism. Inbreeding consequently depresses silk‐related dispersal in three related spiders. This may induce an inbreeding depression vortex with important consequences for range expansion and metapopulation dynamics of aerially dispersing species from highly fragmented landscapes.     

Landscape dynamics and evolution of colonizer syndromes: interactions between reproductive effortand dispersal in a metapopulation

The evolutionary consequences of changes in landscape dynamics for the evolution of life history syndromes are studied using a metapopulation model. We consider in turn the long-term effects of a change in the local disturbance rate, in the maximal local population persistence, in habitat productivity, and in habitat fragmentation. We examine the consequences of selective interactions between dispersal and reproductive effort by comparing the outcome of joint evolution to a situation where the species has lost the potential to evolve either its reproductive effort or its dispersal rate. We relax the classical assumption that any occupied site in the metapopulation reaches its carrying capacity immediately after recolonization. Our main conclusions are the following: (1) genetic diversity modifies the range of landscape parameters for which the metapopulation is viable, but it alters very little the qualitative evolutionary trends observed for each trait within this range. Although they are both part of a competition/colonization axis, reproductive effort and dispersal are not substitutable traits: their evolution reflects more directly the change in the landscape dynamics, than a selective interaction among them. (2) no general syndrome of covariation between reproductive effort and dispersal can be predicted: the pattern of association between the two traits depends on the type of change in landscape dynamics and on the saturation level. We review empirical evidence on colonizer syndromes and suggest lines for further empirical work. This revised version was published online in July 2006 with corrections to the Cover Date.     

Dispersal evolution in temporally variable environments: implications for plant range dynamics

Dispersal—the movement of an individual from the site of birth to a different site for reproduction—is an ecological and evolutionary driver of species ranges that shapes patterns of colonization, connectivity, gene flow, and adaptation. In plants, the traits that influence dispersal often vary within and among species, are heritable, and evolve in response to the fitness consequences of moving through heterogeneous landscapes. Spatial and temporal variation in the quality and quantity of habitat are important sources of selection on dispersal strategies across species ranges. While recent reviews have evaluated the interactions between spatial variation in habitat and dispersal dynamics, the extent to which geographic variation in temporal variability can also shape range-wide patterns in dispersal traits has not been synthesized. In this paper, we summarize key predictions from metapopulation models that evaluate how dispersal evolves in response to spatial and temporal habitat variability. Next, we compile empirical data that quantify temporal variability in plant demography and patterns of dispersal trait variation across species ranges to evaluate the hypothesis that higher temporal variability favors increased dispersal at plant range limits. We found some suggestive evidence supporting this hypothesis while more generally identifying a major gap in empirical work evaluating plant metapopulation dynamics across species ranges and geographic variation in dispersal traits. To address this gap, we propose several future research directions that would advance our understanding of the interplay between spatiotemporal variability and dispersal trait variation in shaping the dynamics of current and future species ranges.     

Metapopulation persistence in dynamic landscapes: the role of dispersal distance

Species associated with transient habitats need efficient dispersal strategies to ensure their regional survival. Using a spatially explicit metapopulation model, we studied the effect of the dispersal range on the persistence of a metapopulation as a function of the local population and landscape dynamics (including habitat patch destruction and subsequent regeneration). Our results show that the impact of the dispersal range depends on both the local population and patch growth. This is due to interactions between dispersal and the dynamics of patches and populations via the number of potential dispersers. In general, long-range dispersal had a positive effect on persistence in a dynamic landscape compared to short-range dispersal. Long-range dispersal increases the number of couplings between the patches and thus the colonisation of regenerated patches. However, long-range dispersal lost its advantage for long-term persistence when the number of potential dispersers was low due to small population growth rates and/or small patch growth rates. Its advantage also disappeared with complex local population dynamics and in a landscape with clumped patch distribution.     

Colonisation dynamics during range expansion is poorly predicted by dispersal in the core range

The potential ranges of many species are shifting due to changing ecological conditions. Where populations become patchy towards the range edge, the realised distribution emerges from colonisation–persistence dynamics. Therefore, a greater understanding of the drivers of these processes, and the spatial scales over which they operate, presents an opportunity to improve predictions of species range expansion under environmental change. Species reintroductions offer an ideal opportunity to investigate the drivers and spatial scale of colonisation dynamics at the range edge. To this effect, we performed and monitored experimental translocations of water voles to quantify how colonisation and local persistence were influenced by habitat quality and occupancy. We used a novel statistical method to simultaneously consider effects across a range of spatial scales. Densely occupied neighbourhoods were highly persistent and frequently colonised. Persistence was more likely in high quality habitat, whereas the influence of habitat quality on colonisation was less clear. Colonisation of suitable habitat in distant, sparsely occupied areas was much less frequent than expected from the well documented high dispersal ability of the species. Persistence of these distant populations was also low, which we attribute to the absence of a rescue effect in sparsely populated neighbourhoods. Our results illustrate a mismatch between the spatial scales of colonisation dynamics in the core and edge of a species’ range, suggesting that recolonisation dynamics in established populations may be a poor predictor of colonisation dynamics at the range edge. Such a mismatch leads to predictions of long lags between the emergence and colonisation of new habitat, with detrimental consequences for a species’ realised distribution, conservation status and contribution to ecosystem function. Conservation translocations that also reinforce existing populations at the range edge might stimulate the rescue effect and mitigate lags in expansion.     

Size and genetic composition of the colonizing propagules in a butterfly metapopulation

The amount and spatial distribution of genetic variation that is maintained in a metapopulation depends critically on the colonization process. Here, we use molecular markers to determine the number and genetic relatedness of individuals establishing new local populations in a large metapopulation of the Glanville fritillary butterfly Melitaea cinxia. The empirical results are compared with the predictions of a dispersal model based on a diffusion approximation of correlated random walk, which serves as a base‐line hypothesis about the rate and pattern of colonization. The results show that half of the new local populations consisted of a single larval group of full sibs and hence necessarily of the offspring of a single female. If the colonization involved two or more larval groups, these were usually oviposited by two different females that were unrelated to each other. The pattern of colonizations is thus intermediate between the propagule pool and the migrant pool models. These results elucidate the generation of genetic stochasticity, which may influence the dynamics of small populations. The dispersal model predicted well the pattern of habitat occupancy and the pattern of colonizations in relation to landscape structure, though which particular habitat patches became colonized was influenced also by measures of habitat quality not included in the model.     

Interactions between soil habitat and geographic range location affect plant fitness

Populations are often found on different habitats at different geographic locations. This habitat shift may be due to biased dispersal, physiological tolerances or biotic interactions. To explore how fitness of the native plant Chamaecrista fasciculata depends on habitat within, at and beyond its range edge, we planted seeds from five populations in two soil substrates at these geographic locations. We found that with reduced competition, lifetime fitness was always greater or equivalent in one habitat type, loam soils, though early-season survival was greater on sand soils. At the range edge, natural populations are typically found on sand soil habitats, which are also less competitive environments. Early-season survival and fitness differed among source populations, and when transplanted beyond the range edge, range edge populations had greater fitness than interior populations. Our results indicate that even when the optimal soil substrate for a species does not change with geographic range location, the realized niche of a species may be restricted to sub-optimal habitats at the range edge because of the combined effects of differences in abiotic and biotic effects (e.g. competitors) between substrates.     

Metapopulation dynamics of the bog fritillary butterfly: experimental changes in habitat quality induced negative density‐dependent dispersal

Habitat quality and habitat geometry are two crucial factors driving metapopulation dynamics. However, their intricacy has prevented so far a reliable test of their relative impact on local population dynamics and persistence. Here we report on a long‐term study in which we manipulated habitat quality within a butterfly metapopulation, whereas habitat geometry was kept constant. The treatment consisted in lowering the quality of certain habitat patches while others were kept untreated, using the same spatial design over years. The effect of the treatment on metapopulation dynamics was assessed by comparing residence probability and dispersal rates within the same habitat network on 11 and 6 independent butterfly generations before and after treatment, respectively. Results showed that the experimental decrease in habitat quality generated significantly higher emigration rates from treated patches. This increase was associated with a significant decrease in dispersal rates out of untreated patches, and a significant higher residence probability in these patches. The direct relation between lower habitat quality and higher dispersal propensity in treated patches was expected. However, the lower dispersal from untreated patches after treatment was opposite to the expectation of positive density dependent dispersal generally observed in butterflies. Such negative density‐dependent dispersal would allow a rapid fine‐tuning of dispersal rates to changes in habitat quality, particularly when the spatial autocorrelation of the environmental is low. Accordingly, dispersal would promote an ideal free distribution of individuals in the landscape according to their fitness expectation.     

Demographic consequences of population subdivision on the long-furred woolly mouse opossum (Micoureus paraguayanus) from the Atlantic Forest

Habitat destruction and fragmentation severely affected the Atlantic Forest. Formerly contiguous populations may become subdivided into a larger number of smaller populations, threatening their long-term persistence. The computer package VORTEX was used to simulate the consequences of habitat fragmentation and population subdivision on Micoureus paraguayanus, an endemic arboreal marsupial of the Atlantic Forest. Scenarios simulated hypothetical populations of 100 and 2000 animals being partitioned into 1–10 populations, linked by varying rates of inter-patch dispersal, and also evaluated male-biased dispersal. Results demonstrated that a single population was more stable than an ensemble of populations of equal size, irrespective of dispersal rate. Small populations (10–20 individuals) exhibited high instability due to demographic stochasticity, and were characterized by high rates of extinction, smaller values for metapopulation growth and larger fluctuations in population size and growth rate. Dispersal effects on metapopulation persistence were related to the size of the populations and to the sexes that were capable of dispersing. Male-biased dispersal had no noticeable effects on metapopulation extinction dynamics, whereas scenarios modelling dispersal by both sexes positively affected metapopulation dynamics through higher growth rates, smaller fluctuations in growth rate, larger final metapopulation sizes and lower probabilities of extinction. The present study highlights the complex relationships between metapopulation size, population subdivision, habitat fragmentation, rate of inter-patch dispersal and sex-biased dispersal and indicates the importance of gaining a better understanding of dispersal and its interactions with correlations between disturbance events.     

Dynamics of Adaptation in Spatially Heterogeneous Metapopulations

The selection pressure experienced by organisms often varies across the species range. It is hence crucial to characterise the link between environmental spatial heterogeneity and the adaptive dynamics of species or populations. We address this issue by studying the phenotypic evolution of a spatial metapopulation using an adaptive dynamics approach. The singular strategy is found to be the mean of the optimal phenotypes in each habitat with larger weights for habitats present in large and well connected patches. The presence of spatial clusters of habitats in the metapopulation is found to facilitate specialisation and to increase both the level of adaptation and the evolutionary speed of the population when dispersal is limited. By showing that spatial structures are crucial in determining the specialisation level and the evolutionary speed of a population, our results give insight into the influence of spatial heterogeneity on the niche breadth of species.     

Fitness declines towards range limits and local adaptation to climate affect dispersal evolution during climate‐induced range shifts

Dispersal ability will largely determine whether species track their climatic niches during climate change, a process especially important for populations at contracting (low‐latitude/low‐elevation) range limits that otherwise risk extinction. We investigate whether dispersal evolution at contracting range limits is facilitated by two processes that potentially enable edge populations to experience and adjust to the effects of climate deterioration before they cause extinction: (i) climate‐induced fitness declines towards range limits and (ii) local adaptation to a shifting climate gradient. We simulate a species distributed continuously along a temperature gradient using a spatially explicit, individual‐based model. We compare range‐wide dispersal evolution during climate stability vs. directional climate change, with uniform fitness vs. fitness that declines towards range limits (RLs), and for a single climate genotype vs. multiple genotypes locally adapted to temperature. During climate stability, dispersal decreased towards RLs when fitness was uniform, but increased when fitness declined towards RLs, due to highly dispersive genotypes maintaining sink populations at RLs, increased kin selection in smaller populations, and an emergent fitness asymmetry that favoured dispersal in low‐quality habitat. However, this initial dispersal advantage at low‐fitness RLs did not facilitate climate tracking, as it was outweighed by an increased probability of extinction. Locally adapted genotypes benefited from staying close to their climate optima; this selected against dispersal under stable climates but for increased dispersal throughout shifting ranges, compared to cases without local adaptation. Dispersal increased at expanding RLs in most scenarios, but only increased at the range centre and contracting RLs given local adaptation to climate.     

EVOLUTION OF DISPERSAL RATES IN METAPOPULATION MODELS: BRANCHING AND CYCLIC DYNAMICS IN PHENOTYPE SPACE

We study the evolution of dispersal rates in a two patch metapopulation model. The local dynamics in each patch are given by difference equations, which, together with the rate of dispersal between the patches, determine the ecological dynamics of the metapopulation. We assume that phenotypes are given by their dispersal rate. The evolutionary dynamics in phenotype space are determined by invasion exponents, which describe whether a mutant can invade a given resident population. If the resident metapopulation is at a stable equilibrium, then selection on dispersal rates is neutral if the population sizes in the two patches are the same, while selection drives dispersal rates to zero if the local abundances are different. With non-equilibrium metapopulation dynamics, non-zero dispersal rates can be maintained by selection. In this case, and if the patches are ecologically identical, dispersal rates always evolve to values which induce synchronized metapopulation dynamics. If the patches are ecologically different, evolutionary branching into two coexisting dispersal phenotypes can be observed. Such branching can happen repeatedly, leading to polymorphisms with more than two phenotypes. If there is a cost to dispersal, evolutionary cycling in phenotype space can occur due to the dependence of selection pressures on the ecological attractor of the resident population, or because phenotypic branching alternates with the extinction of one of the branches. Our results extend those of Holt and McPeek (1996), and suggest that phenotypic branching is an important evolutionary process. This process may be relevant for sympatric speciation.