Nonequilibrium Metapopulation Research Articles

Demographic inferences and climatic niche modelling shed light on the evolutionary history of the emblematic cold-adapted Apollo butterfly at regional scale.

Cold-adapted species escape climate warming by latitudinal and/or altitudinal range shifts, and currently occur in Southern Europe in isolated mountain ranges within "sky islands". Here, we studied the genetic structure of the Apollo butterfly in five such sky islands (above 1,000m) in France, and infer its demographic history since the last interglacial, using single nucleotide polymorphisms (ddRADseq SNPs). The Auvergne and Alps populations show strong genetic differentiation but not alpine massifs, although separated by deep valleys. Combining three complementary demographic inference methods and species distribution models (SDMs) we show that the LIG period was highly unfavourable for Apollo that probably survived in small population in the highest summits of Auvergne. The population shifted downslope and expanded eastward between LIG and LGM throughout the large climatically suitable Rhône valley between the glaciated summits of Auvergne and Alps. The Auvergne and Alps populations started diverging before the LGM but remained largely connected till the mid-Holocene. Population decline in Auvergne was more gradual but started before (~7kya vs. 800 ya), and was much stronger with current population size ten times lower than in the Alps. In the Alps, the low genetic structure and limited evidence for isolation by distance suggest a nonequilibrium metapopulation functioning. The core Apollo population experienced cycles of contraction-expansion with climate fluctuations with largely interconnected populations overtime according to a "metapopulation-pulsar" functioning. This study demonstrates the power of combining demographic inferences and SDMs to determine past and future evolutionary trajectories of an endangered species at a regional scale.

Estimation of metapopulation colonization rates from disturbance history and occurrence-pattern data.

Occurrence patterns of many sessile species in dynamic landscapes are not in equilibrium due to their slow rates of metapopulation colonization and extinction. Colonization-extinction data enable the estimation of colonization rates for such species, but collecting the necessary data may require long waiting times between sampling years. Methods for estimating colonization rates of nonequilibrium metapopulations from single occurrence-pattern data have so far relied on additional data on patch ages and on past patch connectivities. We present an approach where metapopulation colonization rates are estimated from occurrence-pattern data and from disturbance history data that inform of past patch dynamics and that can be collected together with occurrence-pattern data. We estimated parameter values regulating patch and metapopulation dynamics by simulating patch network and metapopulation histories that result in present-like patch network configurations and metapopulation occurrence patterns. We tested our approach using occurrence-pattern data of the epiphytic lichen Lobaria pulmonaria in Fennoscandian forests, and fire-scar data that inform of the 400-yr history of fires and host tree dynamics in the same landscapes. The estimated model parameters were similar to estimates obtained using colonization-extinction data. The projected L. pulmonaria occupancy into the future also agreed with the respective projections that were made using the model estimated from colonization-extinction data. Our approach accelerates the estimation of metapopulation colonization rates for sessile species that are not in metapopulation equilibrium with the current landscape structure.

Population structure in two geographically sympatric and congeneric ectoparasites (Cimex adjunctusandCimex lectularius) in the North American Great Lakes region

Subdivided populations can be described by different models of population structure that reflect population organization, dynamics, and connectivity. We used genetic data to investigate population structure in two geographically sympatric, congeneric species of generalist ectoparasites of warm-blooded animals. We characterized the spatial genetic structure of the eastern bat bug (Cimex adjunctus Barber, 1939), an understudied and fairly abundant species, using microsatellite markers at a spatial scale representing contemporary dispersal of the species. We found seven genetic clusters, global [Formula: see text] of 0.2, 33% of genetic variation among sites, and nonsignificant isolation-by-distance. We compared these results with the common bed bug (Cimex lectularius L., 1758), a closely related but conversely well-known species, in the same geographic area. We found stronger genetic structuring in C. lectularius than in C. adjunctus, with 11 genetic clusters, [Formula: see text] of 0.7, 57% of genetic variation among sites, and significant but weak isolation-by-distance (R2= 0.09). These results suggest that while both species can be described as having classic metapopulation structure, C. adjunctus leans more towards a patchy population and C. lectularius leans more towards a nonequilibrium metapopulation. The difference in population structure between these species may be attributable to differences in movement potential and extinction–colonization dynamics.

On the role played by the carrying capacity and the ancestral population size during a range expansion.

Most species are structured and various population genetics models have been proposed to investigate their history. For mathematical tractability, most of these models make the simplifying assumption of equilibrium. Here we focus on the properties of a nonequilibrium spatial explicit model, range expansions (REs). Despite their abundance, many details of their genetic consequences need yet to be fully investigated. The model we studied is characterized by four main parameters: the effective population size of each deme (N), the migration rate per generation per deme (m), the time of the expansion (Texp) and the effective size of the deme from which the expansion started (Nanc). By means of extensive coalescent simulations, we focused on two aspects of range expansions for fixed Nm: (1) the separate influence of N and m and (2) the role of Nanc. We compared our results with an equilibrium stepping stone model and found two main features typical of REs: an excess of rare variants for larger N and a complex interaction between N, Texp and Nanc in shaping the degree of population differentiation (which depends only on Nm in the stepping stone model). Finally, we developed an approximate Bayesian computation approach to jointly estimate N and m and to infer Nanc. When applied to pseudo-observed data sets, we could correctly recover both N and m (but not Nanc), provided a large number of demes were sampled. These findings highlight how it will be possible to estimate the dispersal rate in nonequilibrium metapopulations by using population genetics approaches.

Annual survival of Allegheny woodrats in a nonequilibrium metapopulation

Many declining populations of the imperiled Allegheny woodrat ( Neotoma magister ) function as nonequilibrium metapopulations in which rates of subpopulation extirpation exceed recolonization. Quantifying and maximizing survival rates thus becomes critical for the conservation of these spatially structured populations. We used encounter histories of individually marked woodrats from subpopulations in Indiana, monitored annually from 2005 to 2013, to 1) estimate apparent annual survival rates while accounting for imperfect detection, 2) evaluate differences in apparent survival between unaugmented subpopulations and subpopulations reestablished or restored through translocation efforts, and 3) describe the effect of genetic diversity on survival. From Cormack–Jolly–Seber models developed in a Bayesian framework, apparent survival was greater for adults than for juveniles, greater for females than males, and there was a modest negative effect of density dependence. Although heterozygosity rates at 11 microsatellites increased among reinforced subpopulations following translocations, we observed no effect of heterozygosity on apparent survival. However, after translocations, average apparent survival was approximately 14% greater among recipient subpopulations than remnant subpopulations. This suggests that viability of recipient subpopulations was limited by low connectivity and the absence of genetic benefits conveyed by immigration or the potential for patches to be recolonized following local extinction. Under conditions of reduced connectivity, translocation among subpopulations to replicate natural gene flow may be appropriate to facilitate the long-term persistence of this and perhaps other nonequilibrium metapopulations.

WHEN GAPS REALLY ARE GAPS: STATISTICAL PHYLOGEOGRAPHY OF HYDROTHERMAL VENT INVERTEBRATES

The invertebrate animals endemic to deep-sea hydrothermal vents are distributed intermittently along relatively linear oceanic ridge axes. A one-dimensional stepping-stone model, therefore, provides a reasonable starting hypothesis of population structure for these species. Nevertheless, population genetic studies of many species from eastern Pacific vents did not detect the expected signatures of isolation-by-distance (IBD). Instead, distinct patterns of geographical subdivision have been attributed to the unique dispersal modes of individual species, topographical discontinuities of the ridge axes, nonequilibrium metapopulation scenarios and cryptic species. Here, we reexamined these inferences in light of expectations generated by computer simulations of a one-dimensional stepping-stone model. We evaluated whether the previously inferred subdivisions are statistically robust to an alternative explanation that continuous stepping-stone migration has occurred along the ridge axes but discontinuities in the sampling design (gaps) have generated the apparent disjunctions. We found that previous inferences about barriers to gene flow (vicariance) were supported in many cases, but that failures to detect evidence for IBD could be explained by low statistical power associated with the sampling effort. The simulation approaches presented here might be useful for testing the significance of inferred phylogeographic gaps in other species.

Metapopulation Dynamics of Bobolinks Occupying Agricultural Grasslands in the Midwestern United States

ABSTRACT A metapopulation is any set of populations that are patchily distributed and potentially connected by dispersal. This broad definition includes classical, mainland-island, source-sink, patchy and non-equilibrium metapopulations. To ensure long-term regional population viability in a fragmented landscape we need a better understanding of metapopulation dynamics. To determine which metapopulation model applies to a given species, Stith et al. (1996) developed a classification scheme using species-specific estimates of dispersal distance and local extinction risk. We used this scheme to classify bobolink (Dolichonyx oryzivorus) populations occupying fragmented, agricultural grasslands in the Midwestern United States. We estimated the distribution of dispersal distances using mark-recapture techniques and calculated local extinction risk. Dispersal rate and turnover were high, indicating that populations were highly connected. Local extinction probability was 4%, indicating that populations were “mid...

Eurytoma robusta (Hymenoptera: Eurytomidae), a local key factor in the population dynamics of Urophora cardui (Diptera: Tephritidae): a comparative analysis

Eurytoma robusta Mayr (Chalcidoidea) exploits host galls either as a primary or secondary parasitoid, an entomophytophagous inquiline or occasionally even as a predator. We present data on its ecology and impact on gall densities and population trends of the gall fly Urophora cardui (L.) on Cirsium arvense (L.) Scop. Habitat preference, host gall selection, clutch size, and high incidence of superparasitism causing empty gall cells show that E. robusta, a generalist with a broad host spectrum, is relatively poorly adapted to parasitising U. cardui. The influence of E. robusta on U. cardui in the Belfort-Sundgau region (1970-2004), in the Upper Rhine Valley (1973-2004) and in north-eastern Bavaria (1977-2004), differed considerably. In the forests of the Upper Rhine Valley and the Belfort-Sundgau region, where U. cardui has relatively stable source-sink populations, E. robusta is present but not the dominant mortality factor of the gall fly. In most areas of north-eastern Bavaria U. cardui occurs in fragmented populations and short lived non-equilibrium metapopulations. In these systems E. robusta became more abundant over the last five years, which resulted in a high incidence of superparasitism, an increase in the number of empty gall cells and reduced gall quality. The greatly increased degree of parasitism and an excess of empty cells resulted recently in the collapse of most local populations of U. cardui in the study area south of Bayreuth (north-eastern Bavaria). Together with earlier records the data presented here suggest that in north-eastern Bavaria E. robusta cause fluctuations in the abundance of U. cardui, which have a periodicity of 5-7 years. A remarkable feature of the oligophagous E. robusta is its high fidelity to formerly abundant U. cardui populations, which, with declining host densities, leads to overexploitation, resulting in a high incidence of superparasitism and high larval mortality. The possible influence of the habitat structure on the effect of E. robusta on the population dynamics of U. cardui is discussed. Our data plus that of other authors suggest that, with regard to U. cardui, E. robusta can develop a temporary local host specialisation.

Age Structure, Residents, and Transients of Miocene Rodent Communities

The age structures of two successive rodent communities are studied on the basis of a rich record from well-dated Miocene sections (17-10 Ma) in north-central Spain. Community age is defined as the mean of the residence times of the community members at the time of the locality age. Community ages are negatively correlated with the numbers of community members. These members are divided into residents (with continuous membership times > or =1.54 million years) and transients (with membership times <1.54 million years). During episodes of species loss, there is a preferential disappearance of transients while residents are retained, a pattern referred to as the "seniority rule." The residents define the studied communities. They are associated with early successional stages of vegetation, and transients are associated with later stages. Under stable conditions, early arrivals in succession are "transient" and replaced by competitive later arrivals. The reversed roles of transients and residents in the studied fossil record are explained by assuming high degrees of disturbance. We view the system within the context of nonequilibrium metapopulation theory, in which competitively superior species become transients because of their dependence on ephemeral late successional habitats.

Large‐scale spatial dynamics of plants: a response to Freckleton &amp; Watkinson

Metapopulation theory (summarized by Hanski 1999) is one of the most influential developments in ecology of recent decades, for example as a cornerstone of conservation biology, and as a theoretical basis for studies of dispersal and of the distribution and abundance of species. A synthesis of metapopulation theory and landscape ecology has been regarded as a key to analyses of the ecological consequences of ongoing landscape changes (Wiens 1997). Although successfully applied to many regional systems of animal populations, the usefulness of metapopulation theory for studies of plants is still open to debate. As Husband & Barrett (1996) and Eriksson (1996) concluded, rather few studies have documented metapopulations in plants, and the same holds for other forms of regional dynamics, e.g. source-sink populations and remnant populations. In a recent paper, Freckleton & Watkinson (2002) have critically reviewed studies of plant metapopulations, with the objectives of assessing whether regional populations of plants really are metapopulations, and suggesting a new typology for different forms of plant regional dynamics. Freckleton & Watkinson stress, and we agree, that these issues are not merely semantic. The concepts of regional dynamics not only determine the ways in which empirical studies are performed, but also influence the interpretation of data (illustrated by Freckleton & Watkinson with studies claiming, but not showing, the existence of metapopulations) and the modelling of spatial dynamics of plant populations. Freckleton & Watkinson (2002) begin by listing four criteria that must be fulfilled in order to regard a regional population as a metapopulation: (i) suitable habitat occurs as discrete patches that may be occupied or unoccupied; (ii) all local populations have a measurable extinction risk; (iii) habitat patches are interconnected by dispersal, allowing the possibility of re-colonization; and (iv) local populations are not completely synchronized in their dynamics. If these criteria are met, regional dynamics cannot be inferred from local processes, and local dynamics cannot be understood without referring to regional patterns or processes. Freckleton & Watkinson (2002) conclude that, given these criteria, very few cases exist where plant metapopulations have been documented. Indeed, there are a number of reasons why plants may not develop metapopulations in the same way as short-lived mobile animals. The existence of long-lived life cycle stages (e.g. seeds or vegetative ramets) means that a local population may persist for a long time even though the patch has become unsuitable. Successful dispersal and recruitment may be very sporadic, and therefore recolonization is unlikely after local population extinction. Dispersal over long distances may be governed by chance events. The definition of 'long distance' may differ between species, but in many cases it may be no more than a few hundred metres (Cain et al. 2000). Suitable habitat is difficult to define, and suitability is likely to be a continuous function of abiotic and biotic environmental factors. Freckleton & Watkinson propose that, using a metapopulation concept for describing regional populations, many plant regional populations would be described as non-equilibrium metapopulations, a conclusion we also reached for plants in fragmented habitats (Eriksson & Ehrl~n 2001). We agree with Freckleton & Watkinson (2002) that it is difficult to assess whether plants in general fulfil the criteria for metapopulations. However, we disagree with their suggestions on a new typology for regional dynamics. We also believe that their conclusions concerning the difficulties in documenting metapopulations in plants may be interpreted as indicating that local processes are sufficient for understanding regional patterns of plant populations, although we acknowledge that this may not have been their intention. We have three objectives here: (i) to comment on the typology of regional dynamics suggested by Freckleton & Watkinson (2002); (ii) to suggest how regional processes might be of importance to plant distributions irrespective of whether plants have metapopulations; and (iii) to argue that metapopulation theory should be developed further as a tool for studies of plants, rather than being replaced by other concepts.

Are all plant populations metapopulations?

The nature of the regional dynamics of a species is critical to its survival. Imagine, for instance, that we are attempting to design a programme to conserve the regional population of a species. If the regional population is a metapopulation, then conservation needs to be aimed at conserving habitat. This is because, as a consequence of the balance between colonization and extinction, metapopulations do not occupy all suitable habitat. Metapopulation persistence relies on the existence of a certain amount of suitable but currently unoccupied habitat. In contrast, in regional ensembles and non-equilibrium metapopulations, conservation efforts have to be aimed at individual populations, because colonization and the creation of new populations is rare, and the survival of the ensemble would be sensitive to increased extinction. Alternatively, in spatially extended populations the availability of suitable habitat will be the key and populations will be sensitive to factors that change average suitability across large areas, such as fragmentation or climate change. We use this hypothetical example to make the point that different types of populations differ fundamentally and qualitatively in the nature of their regional dynamics. This rationale, we believe, is crucial to the future development and application of plant population ecology at a large scale, and is fundamental to our response to Ehrl~n & Eriksson (2003). In our review of plant regional dynamics (Freckleton & Watkinson 2002) we highlighted these differences as a consequence of different types of regional population structure by reference to a series of case studies. Ehrl~n & Eriksson argue that our distinction between such forms is unnecessary we are not wedded to these typologies but believe it is important to recognize that not all plant populations have a metapopulation structure, even when individuals are distributed across the landscape in a patchy manner. Their critique of our paper is divided into three sections which address the following issues: (i) that the temporal or spatial scale of study may affect whether populations are deemed to be metapopulations or not; (ii) whether regional processes are important and whether positive relationships between occupancy and isolation imply a balance between colonization and extinction; and (iii) that the metapopulation notion may be useful for plants if the theory is modified appropriately. In the following sections we respond to these points in order.

Patch Occupancy and Potential Metapopulation Dynamics of Three Forest Mammals in Fragmented Afromontane Forest in South Africa

Abstract: We investigated the persistence of three medium‐sized (2–9 kg), rare forest mammals in the fragmented mist‐belt Podocarpus forests of the midlands of KwaZulu‐Natal Province, South Africa. We recorded patch occupancy of blue duiker ( Philantomba monticola), tree hyrax ( Dendrohyrax arboreus), and samango monkey (Cercopithecus mitis labiatus) in 199 forest patches. Their rarity is ascribed to the fragmentation and destruction of their forest habitat. Incidence functions, derived from presence and absence data, were formulated as generalized linear models, and environmental effects were included in the fitted logistic models. The small and mostly solitary hyrax and duiker persisted in smaller patches than the large and social monkey. Although this result follows expectations based on relative home‐range sizes of each species, the incidence probability of the samango monkey was invariant with increasing isolation, whereas a gradual decrease with increasing isolation was observed for the hyrax and duiker. Group dynamics may inhibit dispersal and increase the isolation effect in social species such as samango monkeys. A mainland‐island metapopulation model adequately describes patterns of patch occupancy by the hyrax and duiker, but the monkeys' poor dispersal ability and obvious area‐dependent extirpation suggest that they exist in transient, nonequilibrium (declining) metapopulations. Through identification of large forest patches for careful protection and management, the survival of all three species—especially the monkey—could be prolonged. Because no functional metapopulation may exist for the monkey, however, this is an emergency measure. For the duiker and hyrax, larger patches should form part of a network of smaller and closer patches in a natural matrix.

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.

Minimum Viable Metapopulation Size

We define the minimum viable metapopulation (MVM) size as the minimum number of interacting local populations necessary for long-term persistence of a metapopulation in a balance between local extinctions and recolonizations. The minimum amount of suitable habitat (MASH) is defined as the minimum density (or number) of suitable habitat patches necessary for metapopulation persistence. Levins's metapopulation model suggests that MASH can be estimated by the fraction of empty patches in a network in which the metapopulation occurs at a stochastic steady state. We discuss three reasons why this rule of thumb is likely to give an underestimate, and possibly a severe underestimate, of MASH: the rescue effect, colonization-extinction stochasticity, and nonequilibrium (transient) metapopulation dynamics. The assumption that metapopulations occur at a steady state, common to many models, may be frequently violated because of the high rate of habitat loss and fragmentation in many landscapes. Scores of rare and endangered species may already be "living dead," committed to extinction because extinction is the equilibrium toward which their metapopulations are moving in the present fragmented landscapes. To conserve these species we should reverse the process of habitat loss and fragmentation.

Local extinction in a metapopulation context: an empirical evaluation

Metapopulations are classically viewed as sets of populations persisting in a balance between local extinction and colonization. When this is true, regional persistence depends critically upon parameters influencing extinction and colonization rates, e.g. the number of habitat patches and populations, the rates and patterns of interpatch migration, and propagule establishment probabilities. A review of relevant empirical literature identifies few metapopulations which fit this description well. Instead, three qualitatively different situations are found to be more common: (1) mainland-island and source-sink metapopulations, in which persistence depends on the existence of one or more extinction-resistant populations; (2) patchy populations, in which dispersal between patches or sub-populations is so high that the system is effectively a single extinction-resistant population; (3) non-equilibrium metapopulations, in which local extinction occurs in the course of a species' overall regional decline. This suggests a modified view of metapopulation dynamics in which local extinction is more an incidental than a central feature.