Plague dynamics and population genetics of the desert locust: can turnover during recession maintain population genetic structure?

The desert locust (Schistocerca gregaria) undergoes crowding-induced phase transformation from solitary form to gregarious form. The transformations involves changes in behaviour, colour, development, morphometry, fecundity and endocrine physiology. Recession populations of the desert locust exist primarily in the solitary phase as small populations in patchy environments and are prone to extinction because of climatic events. Significant genetic differentiation among recession populations along the Red Sea coast of Eritrea was previously reported. It was hypothesized that despite the mixing effect of recurrent swarms, metapopulation dynamics could have produced genetic divergence among these highly scattered recession populations. A Monte Carlo simulation of the population dynamics of the desert locust in a metapopulation setting, with a realistic range of parameter values clearly demonstrated that this is possible. Population growth was represented by a discrete-time logistic equation. The duration of recessions and swarms was sampled from normal distributions whose means and standard deviations were varied based on reported estimates. An average recession duration of 10 +/- 3 generations and swarm periods half as long but almost twice as variable produced a partitioning of the total genetic variance most similar to that in the empirical study. In conventional metapopulation analysis, whether turnover leads to increased or reduced divergence is dependent on the number of colonists relative to the number of recurrent migrants, and on whether the colonists arise from a single patch or many patches. In the case of locusts, the stochastic boom and bust cycle is the overriding factor. Divergence between patches during recession due to founder effect and recurrent drift is balanced by the high rate of mixing during plagues.     

Determinants of Genetic Structure in a Nonequilibrium Metapopulation of the Plant Silene latifolia

Population genetic differentiation will be influenced by the demographic history of populations, opportunities for migration among neighboring demes and founder effects associated with repeated extinction and recolonization. In natural populations, these factors are expected to interact with each other and their magnitudes will vary depending on the spatial distribution and age structure of local demes. Although each of these effects has been individually identified as important in structuring genetic variance, their relative magnitude is seldom estimated in nature. We conducted a population genetic analysis in a metapopulation of the angiosperm, Silene latifolia, from which we had more than 20 years of data on the spatial distribution, demographic history, and extinction and colonization of demes. We used hierarchical Bayesian methods to disentangle which features of the populations contributed to among population variation in allele frequencies, including the magnitude and direction of their effects. We show that population age, long-term size and degree of connectivity all combine to affect the distribution of genetic variance; small, recently-founded, isolated populations contributed most to increase F _ST in the metapopulation. However, the effects of population size and population age are best understood as being modulated through the effects of connectivity to other extant populations, i.e. F _ST diminishes as populations age, but at a rate that depends how isolated the population is. These spatial and temporal correlates of population structure give insight into how migration, founder effect and within-deme genetic drift have combined to enhance and restrict genetic divergence in a natural metapopulation.     

Testing metapopulation dynamics using genetic, demographic and ecological data

The metapopulation concept is a cornerstone in the recent history of ecology and evolution. However, determining whether a natural system fits a metapopulation model is a complex issue. Extinction-colonization dynamics are indeed often difficult to quantify because species detectability is not always 100%, resulting in an imperfect record of extinctions. Here, we explore whether combining population genetics with demographic and ecological surveys can yield more realistic estimates of metapopulation dynamics. We apply this approach to the freshwater snail Drepanotrema depressissimum in a fragmented landscape of tropical ponds. In addition to studying correlations between genetic diversity and demographical or ecological characteristics, we undertake, for the first time, a detailed search for genetic signatures of extinction-recolonization events using temporal changes in allele frequencies within sites. Surprisingly, genetic data indicate that extinction is much rarer than suggested by demographic surveys. Consequently, this system is better described as a set of populations with different sizes and immigration rates than as a true metapopulation. We identify several cases of apparent extinction owing to nondetection of low-density populations, and of aestivating individuals in desiccated ponds. More generally, we observed a frequent mismatch between genetic and demographical/ecological information at small spatial and temporal scales. We discuss the causes of these discrepancies and show how these two types of data provide complementary information on population dynamics and history, especially when temporal genetic samples are available.     

Coevolution at multiple spatial scales: Linum marginale–Melampsora lini – from the individual to the species

Coevolutionary processes are intrinsically spatial as well as temporal, and occur at many different scales. These range from single populations dominated by demographic and genetic stochasticity, to metapopulations in which colonisation/extinction dynamics have a large influence, and larger geographic regions where phylogenetic patterns and historical events become important. We present data for the genetically and demographically well-characterised plant host–pathogen interaction, the Linum marginale–Melampsora lini system, and use this to demonstrate the varying nature of resistance and virulence structure across these spatial scales. At the within population level, our results indicate considerable variability in resistance and virulence, but little evidence of coordinated changes in host and pathogen. Studies involving comparisons among multiple demes within a single metapopulation show that adjacent populations often have asynchronous disease dynamics and large differences in diversity and frequency of resistance and virulence phenotypes. Nevertheless, at this scale, there is also evidence of spatial structure in that more closely adjacent host populations are significantly more likely to have similar resistance phenotypes and mean levels of resistance. At larger scales, comparisons among adjacent metapopulations indicate that quantitative differences in host mating system and other life history features can have further major consequences for how host and pathogen variation is packaged. Finally, comparisons at continental and among host-species levels show variation consistent with specialisation and speciation in the pathogen. This revised version was published online in July 2006 with corrections to the Cover Date.     

Human‐facilitated metapopulation dynamics in an emerging pest species,Cimex lectularius

The number and demographic history of colonists can have dramatic consequences for the way in which genetic diversity is distributed and maintained in a metapopulation. The bed bug (Cimex lectularius) is a re‐emerging pest species whose close association with humans has led to frequent local extinction and colonization, that is, to metapopulation dynamics. Pest control limits the lifespan of subpopulations, causing frequent local extinctions, and human‐facilitated dispersal allows the colonization of empty patches. Founder events often result in drastic reductions in diversity and an increased influence of genetic drift. Coupled with restricted migration, this can lead to rapid population differentiation. We therefore predicted strong population structuring. Here, using 21 newly characterized microsatellite markers and approximate Bayesian computation (ABC), we investigate simplified versions of two classical models of metapopulation dynamics, in a coalescent framework, to estimate the number and genetic composition of founders in the common bed bug. We found very limited diversity within infestations but high degrees of structuring across the city of London, with extreme levels of genetic differentiation between infestations (F_ST = 0.59). ABC results suggest a common origin of all founders of a given subpopulation and that the numbers of colonists were low, implying that even a single mated female is enough to found a new infestation successfully. These patterns of colonization are close to the predictions of the propagule pool model, where all founders originate from the same parental infestation. These results show that aspects of metapopulation dynamics can be captured in simple models and provide insights that are valuable for the future targeted control of bed bug infestations.     

Evolution of intrahost HIV-1 genetic diversity during chronic infection

HIV-1 is one of the fastest evolving entities known. Given that census population sizes of HIV-1 within individuals are much greater than the inverse mutation rate, every possible single point mutation in the viral genome occurs each generation. This enormous capability to generate genetic variation allows for escape from immune surveillance and antiviral therapy. However, compared to this potential, populations of HIV-1 within individuals exhibit little genetic variation. This discrepancy between the known mutation rate of HIV-1 and the average level of genetic variation in the env gene observed in vivo is reflected in comparisons of the actual numbers of productively infected cells, estimated as 10(7), and the effective population size, estimated as 10(3). Using approximate Bayesian computation, we evaluated several hypotheses based on a variety of selective and demographic processes to explain the low effective population size of HIV-1. Of the models we examined, the metapopulation model, in which HIV-1 evolves within an individual as a large collection of small subpopulations subject to frequent migration, extinction, and recolonization, was most consistent with the observed levels of genetic variation and the average frequencies of those variants. The metapopulation model links previous studies of viral dynamics and population genetics.     

Genetic isolation of a now extinct population of bottlenose dolphins (Tursiops truncatus)

A number of dolphin species, though highly mobile, show genetic structure among parapatric and sometimes sympatric populations. However, little is known about the temporal patterns of population structure for these species. Here, we apply Bayesian inference and data from ancient DNA to assess the structure and dynamics of bottlenose dolphin (Tursiops truncatus) populations in the coastal waters of the UK. We show that regional population structure in UK waters is consistent with earlier studies suggesting local habitat dependence for this species in the Mediterranean Sea and North Atlantic. One genetically differentiated UK population went extinct at least 100 years ago and has not been replaced. The data indicate that this was a local extinction, and not a case of historical range shift or contraction. One possible interpretation is a declining metapopulation and conservation need for this species in the UK.     

Bayesian inference of a historical bottleneck in a heavily exploited marine mammal

Emerging Bayesian analytical approaches offer increasingly sophisticated means of reconstructing historical population dynamics from genetic data, but have been little applied to scenarios involving demographic bottlenecks. Consequently, we analysed a large mitochondrial and microsatellite dataset from the Antarctic fur seal Arctocephalus gazella, a species subjected to one of the most extreme examples of uncontrolled exploitation in history when it was reduced to the brink of extinction by the sealing industry during the late eighteenth and nineteenth centuries. Classical bottleneck tests, which exploit the fact that rare alleles are rapidly lost during demographic reduction, yielded ambiguous results. In contrast, a strong signal of recent demographic decline was detected using both Bayesian skyline plots and Approximate Bayesian Computation, the latter also allowing derivation of posterior parameter estimates that were remarkably consistent with historical observations. This was achieved using only contemporary samples, further emphasizing the potential of Bayesian approaches to address important problems in conservation and evolutionary biology.     

Metapopulation dynamics: Does it help to have more of the same?

With the interest in conservation biology shifting towards processes from patterns, and to populations from communities, the theory of metapopulation dynamics is replacing the equilibrium theory of island biogeography as the population ecology paradigm in conservation biology. The simplest models of metapopulation dynamics make predictions about the effects of habitat fragmentation - size and isolation of habitat patches - on metapopulation persistence. The simple models may be enriched by considerations of the effects of demographic and environmental stochasticity on the size and extinction probability of local populations. Environmental stochasticity affects populations at two levels: it makes local extinctions more probable, and it also decreases metapopulation persistence time by increasing the correlation of extinction events across populations. Some controversy has arisen over the significance of correlated extinctions, and how they may affect the optimal subdivision of metapopulations to maximize their persistence time.     

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.     

Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens)

The delimitation of populations, defined as groups of individuals linked by gene flow, is possible by the analysis of genetic markers and also by spatial models based on dispersal probabilities across a landscape. We combined these two complimentary methods to define the spatial pattern of genetic structure among remaining populations of the threatened Florida scrub-jay, a species for which dispersal ability is unusually well-characterized. The range-wide population was intensively censused in the 1990s, and a metapopulation model defined population boundaries based on predicted dispersal-mediated demographic connectivity. We subjected genotypes from more than 1000 individual jays screened at 20 microsatellite loci to two Bayesian clustering methods. We describe a consensus method for identifying common features across many replicated clustering runs. Ten genetically differentiated groups exist across the present-day range of the Florida scrub-jay. These groups are largely consistent with the dispersal-defined metapopulations, which assume very limited dispersal ability. Some genetic groups comprise more than one metapopulation, likely because these genetically similar metapopulations were sundered only recently by habitat alteration. The combined reconstructions of population structure based on genetics and dispersal-mediated demographic connectivity provide a robust depiction of the current genetic and demographic organization of this species, reflecting past and present levels of dispersal among occupied habitat patches. The differentiation of populations into 10 genetic groups adds urgency to management efforts aimed at preserving what remains of genetic variation in this dwindling species, by maintaining viable populations of all genetically differentiated and geographically isolated populations.     

The applicability of metapopulation theory to large mammals

Metapopulation theory has become a common framework in conservation biology and it is sometimes suggested that a metapopulation approach should be used for management of large mammals. However, it has also been suggested that metapopulation theory would not be applicable to species with long generations compared to those with short ones. In this paper, we review how and on what empirical ground metapopulation terminology has been applied to insects, small mammals and large mammals. The review showed that the metapopulation term sometimes was used for population networks which only fulfilled the broadest possible definition of a metapopulation, i.e. they were subpopulations connected by migrating individuals. We argue that the metapopulation concept should be reserved for networks that also show some kind of metapopulation dynamics. Otherwise it applies to almost all populations and loses its substance. We found much empirical support for metapopulation dynamics in both insects and small mammals, but not in large mammals. A possible reason is the methods used to confirm the existence of metapopulation dynamics. For insects and small mammals, the common approach is to study population turnover through patch occupancy data. Such data is difficult to obtain for large mammals, since longer temporal scales need to be covered to record extinctions and colonizations. Still, many populations of large mammals are exposed to habitat fragmentation and the resulting subpopulations sometimes have high risks of extinction. If there is migration between the subpopulations, the metapopulation framework could provide valuable information on their population dynamics. We suggest that a metapopulation approach can be interesting for populations of large mammals, when there are discrete breeding subpopulations and when these subpopulations have different growth rates and demographic fates. Thus, a comparison of the subpopulations’ demographic fates, rather than subpopulation turnover, can be a feasible alternative for studies of metapopulation dynamics in large mammals.     

Linking extinction-colonization dynamics to genetic structure in a salamander metapopulation

Theory predicts that founder effects have a primary role in determining metapopulation genetic structure. However, ecological factors that affect extinction-colonization dynamics may also create spatial variation in the strength of genetic drift and migration. We tested the hypothesis that ecological factors underlying extinction-colonization dynamics influenced the genetic structure of a tiger salamander (Ambystoma tigrinum) metapopulation. We used empirical data on metapopulation dynamics to make a priori predictions about the effects of population age and ecological factors on genetic diversity and divergence among 41 populations. Metapopulation dynamics of A. tigrinum depended on wetland area, connectivity and presence of predatory fish. We found that newly colonized populations were more genetically differentiated than established populations, suggesting that founder effects influenced genetic structure. However, ecological drivers of metapopulation dynamics were more important than age in predicting genetic structure. Consistent with demographic predictions from metapopulation theory, genetic diversity and divergence depended on wetland area and connectivity. Divergence was greatest in small, isolated wetlands where genetic diversity was low. Our results show that ecological factors underlying metapopulation dynamics can be key determinants of spatial genetic structure, and that habitat area and isolation may mediate the contributions of drift and migration to divergence and evolution in local populations.     

Low RAPD Variation and Female-Biased Sex Ratio Indicate Genetic Drift in Small Populations of the Dioecious Conifer Taxus Baccata in Switzerland

Small populations are prone to genetic drift as a consequence of random sampling effects. We investigated whether we could detect such random sampling effects in the English yew (Taxus baccata), a dioecious conifer species occurring in scattered populations in Switzerland. Seven pairs of small and large populations were analyzed using random amplified polymorphic DNA (RAPD) marker bands from 20 individuals per population. Several genetic parameters (mean marker band frequency deviation, molecular variance, population differentiation) indicated that small populations experienced genetic drift. These genetic differences between small and large populations of yew were paralleled by an increased sex ratio bias towards a higher number of females in the small populations. Our findings support earlier assumptions that the Swiss occurrences of yew may be described as metapopulation dynamics, characterized by local colonization and extinction events leading to the observed genetic drift.     

Importance of solitarious desert locust population dynamics: lessons from historical survey data in Algeria

The desert locust, Schistocerca gregaria (Forskål) (Orthoptera: Acrididae), is a major pest and well known in its gregarious phase. However, it is not well understood during recession periods, when the solitarious phase populations are discrete. Nonetheless, these populations are at the origin of the invasions when ecological conditions become favourable. This lack of knowledge of the solitarious phase individuals impedes effective preventive management of this pest. Archive data collected in Algeria from 1980 to 2011 were used to analyse solitarious population dynamics across the Algerian Sahara where some outbreak areas are located that play a major role in the invasion process. The results confirm previous empirical observations on solitarious population dynamics. First, a clear difference could be documented between the northern and southern Saharan regions of Algeria concerning the locust dynamics and the impact of environmental conditions. The importance of runoff was clear to create suitable habitats over a long period and to very distant places from rainy areas. Second, a link, on an annual basis, between green vegetation and presence of solitarious locusts was found. Third, statistical relationships between various locations demonstrated a clear regional dynamics. Our study confirmed the importance of migrations of solitarious populations among Algerian regions and more generally within the recession area of this species. The operational implications of these findings are multiple. First, they confirm the need of a flexible and scalable preventive system during the year, from 1 year to another and with a clear distinction between the northern and southern Saharan areas of Algeria. Second, they also confirm the necessity for the inclusion of wadis and soil moisture estimations from remote sensing in geographic information systems for preventive management. And third, they clearly illustrate the importance to target solitarious locusts for more efficient preventive survey operations.     

局域种群的Allee效应和集合种群的同步性

从包含Allee效应的局域种群出发,建立了耦合映像格子模型,即集合种群模型.通过分析和计算机模拟表明:(1)当局域种群受到Allee效应强度较大时,集合种群同步灭绝;(2)而当Allee效应强度相对较弱时,通过稳定局域种群动态(减少混沌)使得集合种群发生同步波动,而这种同步波动能够增加集合种群的灭绝风险;(3)斑块间的连接程度对集合种群同步波动的发生有很大的影响,适当的破碎化有利于集合种群的续存.全局迁移和Allee效应结合起来增加了集合种群同步波动的可能,从而增加集合种群的灭绝风险.这些结果对理解同步性的机理、利用同步机理来制定物种保护策略和害虫防治都有重要的意义.     

Breeding system and demography shape population genetic structure across ecological and climatic zones in the African freshwater snail, Bulinus forskalii (Gastropoda, Pulmonata), intermediate host for schistosomes

The role of breeding system and population bottlenecks in shaping the distribution of neutral genetic variation among populations inhabiting patchily distributed, ephemeral water bodies was examined for the hermaphroditic freshwater snail Bulinus forskalii, intermediate host for the medically important trematode Schistosoma guineensis. Levels of genetic variation at 11 microsatellite loci were assessed for 600 individuals sampled from 19 populations that span three ecological and climatic zones (ecozones) in Cameroon, West Africa. Significant heterozygote deficiencies and linkage disequilibria indicated very high selfing rates in these populations. Despite this and the large genetic differentiation detected between populations, high levels of genetic variation were harboured within these populations. The high level of gene flow inferred from assignment tests may be responsible for this pattern. Indeed, metapopulation dynamics, including high levels of gene flow as well as extinction/contraction and recolonization events, are invoked to account for the observed population structuring, which was not a consequence of isolation-by-distance. Because B. forskalii populations inhabiting the northern, Sahelian area are subject to more pronounced annual cycles of drought and flood than the southern equatorial ones, they were expected to be subject to population bottlenecks of increased frequency and severity and, therefore, show reduced genetic variability and elevated population differentiation. Contrary to predictions, the populations inhabiting the most northerly ecozone exhibited higher genetic diversity and lower genetic differentiation than those in the most southerly one, suggesting that elevated gene flow in this region is counteracting genetic drift.     

Patchy population structure in a short-distance migrant: evidence from genetic and demographic data

Species often occur in subdivided populations as a consequence of spatial heterogeneity of the habitat. To describe the spatial organization of subpopulations, existing theory proposes three main population models: patchy population, metapopulation and isolated populations. These models differ in their predicted levels of connectivity among subpopulations, and in the risk that a subpopulation will go extinct. However, spatially discrete subpopulations are commonly considered to be organized as metapopulations, even though explicit tests of metapopulation assumptions are rare. Here, we test predictions of the three models on the basis of demographic and genetic data, a combined approach so far surprisingly little used in mobile organisms. From 2002 to 2005, we studied nine subpopulations of the wetland-restricted reed bunting ( Emberiza schoeniclus ) in the southeastern part of the Canton Zurich (Switzerland), from which local declines of this species have been reported. Here, wetlands are as small as 2.7 ha and separated through intensively used agricultural landscapes. Demographic data consisted of dispersal of colour-banded individuals among subpopulations, immigration rates and extinction-/recolonization dynamics. Genetic data were based on the distribution of genetic variability and gene flow among subpopulations derived from the analysis of nine microsatellite loci. Both demographic and genetic data revealed that the patchy population model best described the spatial organization of reed bunting subpopulations. High levels of dispersal among subpopulations, high immigration into the patchy population, and genetic admixture suggested little risk of extinction of both subpopulations and the entire patchy population. This study exemplifies the idea that spatially discrete subpopulations may be organized in ways other than a metapopulation, and hence has implications for the conservation of subpopulations and species.     

Interactions between environmental factors can hide isolation by distance patterns: a case study of Ctenomys rionegrensis in Uruguay

Identifying the factors responsible for the structuring of genetic diversity is of fundamental importance for biodiversity conservation. However, arriving at such understanding is difficult owing to the many factors involved and the potential interactions between them. Here, we present an example of how such interactions can preclude us from arriving at a complete characterization of the demographic history and genetic structure of a species. Ctenomys rionegrensis is a species with restricted dispersal abilities and, as such, should exhibit an isolation by distance (IBD) pattern, which previous studies were unable to uncover. It was therefore concluded that this species underwent a recent population expansion. Using a novel hierarchical Bayesian method, we show that the inability to detect the IBD pattern is due to the interaction between elevation and geographical distance. We posit that populations in low areas suffer periodic floods that may reduce local population sizes, increasing genetic drift, a process that masks the effect of distance on genetic differentiation. Our results do not refute the possibility that the populations of C. rionegrensis underwent a recent population expansion but they indicate that an alternative scenario described by a metapopulation model at or near migration-drift equilibrium cannot be excluded either.