Fine-Scale Spatial Genetic Structure in Emmer Wheat and the Role of Population Range Position

The extent of spatial genetic structure (SGS) within plant populations depends on seed and pollen dispersal distance, breeding type, level of self-fertilization and effective plant density. Self-fertilizing species with gravity-dispersed seeds are expected to have both small effective population sizes and low pollen movement leading to high genetic structure. Higher SGS can be expected in more patchy and peripheral populations because of lower plant density and population sizes, and lower intensity of gene flow. We tested these predictions analyzing SGS in two core and two peripheral populations of predominantly self-fertilizing emmer wheat. Analysis of SGS with 11 nuclear microsatellites revealed (1) a negative linear relationship between kinship coefficients, calculated for pairs of individuals, and the logarithm of geographical distance between members of the pairs, in all studied populations; and (2) a significant autocorrelation for a distance up to 5 m (core populations) or 20 m (peripheral populations). Pollen flow, estimated from comparison of nuclear and chloroplast variation, was spatially limited, as was seed dispersal. Our results support a hypothesized relationship between SGS intensity and breeding system, the mode of seed dispersal and the population range position (core vs. periphery).     

Multiscale spatial genetic structure within and between populations of wild cherry trees in nuclear genotypes and chloroplast haplotypes

Spatial genetic structure (SGS) of plants mainly depends on the effective population size and gene dispersal. Maternally inherited loci are expected to have higher genetic differentiation between populations and more intensive SGS within populations than biparentally inherited loci because of smaller effective population sizes and fewer opportunities of gene dispersal in the maternally inherited loci. We investigated biparentally inherited nuclear genotypes and maternally inherited chloroplast haplotypes of microsatellites in 17 tree populations of three wild cherry species under different conditions of tree distribution and seed dispersal. As expected, interpopulation genetic differentiation was 6–9 times higher in chloroplast haplotypes than in nuclear genotypes. This difference indicated that pollen flow 4–7 times exceeded seed flow between populations. However, no difference between nuclear and chloroplast loci was detected in within‐population SGS intensity due to their substantial variation among the populations. The SGS intensity tended to increase as trees became more aggregated, suggesting that tree aggregation biased pollen and seed dispersal distances toward shorter. The loss of effective seed dispersers, Asian black bears, did not affect the SGS intensity probably because of mitigation of the bear loss by other vertebrate dispersers and too few tree generations after the bear loss to alter SGS. The findings suggest that SGS is more variable in smaller spatial scales due to various ecological factors in local populations.     

Limited phylogeographic and genetic connectivity in Acacia species of low stature in an arid landscape

Widespread plant species are expected to maintain genetic diversity and gene flow via pollen and seed dispersal. Stature is a key life history trait that affects seed and potentially pollen dispersal, with limited stature associated with limited dispersal and greater genetic differentiation. We sampled Hill’s tabletop wattle (Acacia hilliana) and curry wattle (Acacia spondylophylla), two co‐distributed, widespread, Acacia shrubs of low stature, across the arid Pilbara region of north‐western Australia. Using chloroplast sequence and nuclear microsatellite data we evaluated patterns of population genetic and phylogeographic diversity and structure, demographic signals, ratios of pollen to seed dispersal, evidence for historical refugia, and association between elevation and diversity. Results showed strong phylogeographic (chloroplast, G _ST = 0.831 and 0.898 for A. hilliana and A. spondylophylla, respectively) and contemporary (nuclear, F _ST = 0.260 and 0.349 for A. hilliana and A. spondylophylla, respectively) genetic structure in both species. This indicates limited genetic connectivity via seed and pollen dispersal associated with Acacia species of small stature compared to taller tree and shrub acacias across the Pilbara bioregion. This effect of stature on genetic structure is superimposed on moderate levels of genetic diversity that were expected based on widespread ranges (haplotype diversity h = 25 and 12; nuclear diversity He = 0.60 and 0.47 for A. hilliana and A. spondylophylla, respectively). Contemporary genetic structure was congruent at the greater landscape scale, especially in terms of strong genetic differentiation among geographically disjunct populations in less elevated areas. Measures of diversity and connectivity were associated with traits of greater geographic population proximity, population density, population size, and greater individual longevity, and some evidence for range expansion in A. hilliana. Results illustrate that low stature is associated with limited dispersal and greater patterns of genetic differentiation for congenerics in a common landscape and highlight the complex influence of taxon‐specific life history and ecological traits to seed and pollen dispersal.     

Genetic Isolation and Diffusion of Wild Grapevine Italian and Spanish Populations as Estimated by Nuclear and Chloroplast SSR Analysis

Abstract: Genetic structure of six Italian and five Spanish populations of wild grapevine (Vitis vinifera ssp. silvestris) was investigated using nuclear and chloroplast SSR analysis. Results show that the Italian populations are characterised by high genomic diversity within populations, with a peak of heterozygosity ( Ho = 0.7637) for a population collected in southern Italy. However, the low haplotype richness and the high level of genetic distance detected among the Spanish populations, combined with their low gene flow, shows that these populations suffered from a genetic erosion. Genetic relationship between Italian and Spanish populations was investigated and results showed genetic differentiation between the two populations. Using nuclear and chloroplast SSR markers, the ratio between pollen and seed diffusion was estimated. High pollen flow, as compared with seed flow, suggests that seed diffusion is made difficult, probably due to low germinability and survival of seedlings in the wild. Seed germination and young plant survival must be considered a priority target for in situ conservation programmes. By providing information on population history, genetic structure and gene flow, and by identifying areas harbouring high levels of wild grape variability, this study provides the basis for the preservation of biodiversity of the wild grapevine.     

Habitat loss other than fragmentation per se decreased nuclear and chloroplast genetic diversity in a monoecious tree

Generally, effect of fragmentation per se on biodiversity has not been separated from the effect of habitat loss. In this paper, using nDNA and cpDNA SSRs, we studied genetic diversity of Castanopsis sclerophylla (Lindl. & Paxton) Schotty populations and decoupled the effects of habitat loss and fragmentation per se. We selected seven nuclear and six cpDNA microsatellite loci and genotyped 460 individuals from mainland and island populations, which were located in the impoundment created in 1959. Number of alleles per locus of populations in larger habitats was significantly higher than that in smaller habitats. There was a significant relationship between the number of alleles per locus and habitat size. Based on this relationship, the predicted genetic diversity of an imaginary population of size equaling the total area of the islands was lower than that of the global population on the islands. Re-sampling demonstrated that low genetic diversity of populations in small habitats was caused by unevenness in sample size. Fisher's α index was similar among habitat types. These results indicate that the decreased nuclear and chloroplast genetic diversity of populations in smaller habitats was mainly caused by habitat loss. For nuclear and chloroplast microsatellite loci, values of F(ST) were 0.066 and 0.893, respectively, and the calculated pollen/seed dispersal ratio was 162.2. When separated into pre-and post-fragmentation cohorts, pollen/seed ratios were 121.2 and 189.5, respectively. Our results suggest that habitat loss explains the early decrease in genetic diversity, while fragmentation per se may play a major role in inbreeding and differentiation among fragmented populations and later loss of genetic diversity.     

Genetic Diversity and Population Structure of Acacia senegal (L) Willd. in Kenya

The level of genetic diversity and population structure of Acacia senegal variety kerensis in Kenya was examined using seven polymorphic nuclear microsatellite loci and two chloroplast microsatellite loci. In both chloroplast and nuclear datasets, high levels of genetic diversity were found within all populations and genetic differentiation among populations was low, indicating extensive gene flow. Analysis of population structure provided support for the presence of two groups of populations, although all individuals had mixed ancestry. Groups reflected the influence of geography on gene flow, with one representing Rift Valley populations whilst the other represented populations from Eastern Kenya. The similarities between estimates derived from nuclear and chloroplast data suggest highly effective gene dispersal by both pollen and seed in this species, although population structure appears to have been influenced by distributional changes in the past. The few contrasts between the spatial patterns for nuclear and chloroplast data provided additional support for the idea that, having fragmented in the past, groups are now thoroughly mixed as a result of extensive gene flow. For the purposes of conservation and in situ management of genetic resources, sampling could target a few, large populations ideally distributed among the spatial groups identified. This should ensure the majority of extant variation is preserved, and facilitate the investigation of variation in important phenotypic traits and development of breeding populations.     

Genetic diversity, structure, and demographic change in tanoak, Lithocarpus densiflorus (Fagaceae), the most susceptible species to sudden oak death in California

Knowledge of population genetic structure of tanoak (Lithocarpus densiflorus) is of interest to pathologists seeking natural variation in resistance to sudden oak death disease, to resource managers who need indications of conservation priorities in this species now threatened by the introduced pathogen (Phytophthora ramorum), and to biologists with interests in demographic processes that have shaped plant populations. We investigated population genetic structure using nuclear and chloroplast DNA (cpDNA) and inferred the effects of past population demographic processes and contemporary gene flow. Our cpDNA results revealed a strong pattern of differentiation of four regional groups (coastal California, southern Oregon, Klamath mountains, and Sierra Nevada). The chloroplast haplotype phylogeny suggests relatively deep divergence of Sierra Nevada and Klamath populations from those of coastal California and southern Oregon. A widespread coastal California haplotype may have resulted from multiple refugial sites during the Last Glacial Maximum or from rapid recolonization from few refugia. Analysis of nuclear microsatellites suggests two major groups: (1) central coastal California and (2) Sierra Nevada/Klamath/southern Oregon and an area of admixture in north coastal California. The low level of nuclear differentiation is likely to be due to pollen gene flow among populations during postglacial range expansion.     

The impact of pollination syndrome and habitat on gene flow: a comparative study of two Streptocarpus (Gesneriaceae) species

Gene flow through pollen and seed dispersal is important in terms of population differentiation and eventually speciation. Seed and pollen flow are affected in turn by habitats and pollen vectors. We examined the effect of different pollinators and habitats on gene flow by comparing two species of Streptocarpus, using microsatellite and chloroplast RFLP markers. Populations of the forest-dwelling S. primulifolius were highly differentiated according to nuclear microsatellite data and had mutually exclusive chloroplast haplotypes. This result is congruent with infrequent seed dispersal and limited between-population foraging by the long-tongued fly pollinator Stenobasipteron wiedemanni. In contrast, populations of S. dunnii growing in exposed crags had lower levels of population differentiation according to both nuclear and chloroplast data, congruent with a hypothesis of more effective between population seed dispersal and greater pollen-mediated gene flow due to the sunbird pollinator Nectarinia famosa. The population genetic behavior of these species is reflected in their taxonomy and phylogenetic position; S. primulifolius belongs to a taxonomically complex clade in which recent speciation is evident, while the clade containing S. dunnii is characterized by taxonomically well-defined species on longer phylogenetic branches. Our study shows that pollinator movements and seed dispersal patterns are a major determinant of the evolutionary trajectories of these species.     

Contrasting patterns of pollen and seed flow influence the spatial genetic structure of sweet vernal grass (Anthoxanthum odoratum) populations

The spatial genetic structure of plant populations is determined by a combination of gene flow, genetic drift, and natural selection. Gene flow in most plants can result from either seed or pollen dispersal, but detailed investigations of pollen and seed flow among populations that have diverged following local adaptation are lacking. In this study, we compared pollen and seed flow among 10 populations of sweet vernal grass (Anthoxanthum odoratum) on the Park Grass Experiment. Overall, estimates of genetic differentiation that were based on chloroplast DNA (cpDNA) and, which therefore resulted primarily from seed flow, were lower (average F(ST) = 0.058) than previously published estimates that were based on nuclear DNA (average F(ST) = 0.095). Unlike nuclear DNA, cpDNA showed no pattern of isolation by adaptation; cpDNA differentiation was, however, inversely correlated with the number of additions (nutrients and lime) that each plot had received. We suggest that natural selection is restricting pollen flow among plots, whereas nutrient additions are increasing seed flow and genetic diversity by facilitating the successful germination and growth of immigrant seeds. This study highlights the importance of considering all potential gene flow mechanisms when investigating determinants of spatial genetic structure, and cautions against the widespread assumption that pollen flow is more important than seed flow for population connectivity in wind-pollinated species.     

Contrasting diversity and demographic signals in sympatric narrow‐range endemic shrubs of the south‐west Western Australian semi‐arid zone

Comparative studies of sympatric species that integrate both phylogeographical and population genetic approaches provide insight into how demographic events and life history traits shape adaptive potential and drive species persistence. Such studies are rare for species‐rich and strongly structured environments, especially those of the southern hemisphere. For two sympatric, perennial shrubs of the south‐west Western Australian semi‐arid zone, Grevillea globosa and Mirbelia sp. Bursarioides, we assessed historical and contemporary genetic diversity and structure, demographic processes and ratios of pollen to seed dispersal. Phylogeographical structure was not detected and haplotype networks were star‐like. Number of haplotypes, nucleotide diversity, haplotype diversity, and allelic diversity were statistically significantly lower for G. globosa than for M. sp. Bursarioides. Levels of haplotype divergence and more contemporary genetic divergence and expected heterozygosity were lower for G. globosa than for M. sp. Bursarioides, but differences were not statistically significant. Both species exhibited signals of isolation by distance and low pollen to seed dispersal ratios (5.26:1 and 6.88:1). Grevillea globosa displayed signals of historical and contemporary demographic expansion. Results imply an important role for aspects of seed ecology that impact population demography, as well as direct dispersal and a significant contribution of seed dispersal to genetic connectivity in a semi‐arid landscape.     

Realized gene flow within mixed stands of Quercus robur L. and Q. petraea (Matt.) L. revealed at the stage of naturally established seedling

The estimates of contemporary gene flow assessed based on naturally established seedlings provide information much needed for understanding the abilities of forest tree populations to persist under global changes through migration and/or adaptation facilitated by gene exchange among populations. Here, we investigated pollen‐ and seed‐mediated gene flow in two mixed‐oak forest stands (consisting of Quercus robur L. and Q. petraea [Matt.] Liebl.). The gene flow parameters were estimated based on microsatellite multilocus genotypes of seedlings and adults and their spatial locations within the sample plots using models that attempt to reconstruct the genealogy of the seedling cohorts. Pollen and seed dispersal were modelled using the standard seedling neighbourhood model and a modification—the 2‐component seedling neighbourhood model, with the later allowing separation of the dispersal process into local and long‐distance components. The 2‐component model fitted the data substantially better than the standard model and provided estimates of mean seed and pollen dispersal distances accounting for long‐distance propagule dispersal. The mean distance of effective pollen dispersal was found to be 298 and 463 m, depending on the stand, while the mean distance of effective seed dispersal was only 8.8 and 15.6 m, which is consistent with wind pollination and primarily seed dispersal by gravity in Quercus. Some differences observed between the two stands could be attributed to the differences in the stand structure of the adult populations and the existing understory vegetation. Such a mixture of relatively limited seed dispersal with occasional long distance gene flow seems to be an efficient strategy for colonizing new habitats with subsequent local adaptation, while maintaining genetic diversity within populations.     

Disrupted phylogeographical microsatellite and chloroplast DNA patterns indicate a vicariance rather than long‐distance dispersal origin for the disjunct distribution of the Chilean endemic Dioscorea biloba (Dioscoreaceae) around the Atacama Desert

Aim The Chilean endemic Dioscorea biloba (Dioscoreaceae) is a dioecious geophyte that shows a remarkable 600 km north–south disjunction in the peripheral arid area of the Atacama Desert. Its restricted present‐day distribution and probable Neogene origin indicate that its populations have a history linked to that of the Atacama Desert, making this an ideal model species with which to investigate the biogeography of the region. Location Chile, Atacama Desert and peripheral arid area. Methods Two hundred and seventy‐five individuals from nine populations were genotyped for seven nuclear microsatellite loci, and plastid trnL–F and trnT–L sequences were obtained for a representative subset of these. Analyses included the estimation of genetic diversity and population structure through clustering, Bayesian and analysis of molecular variance analyses, and statistical parsimony networks of chloroplast haplotypes. Isolation by distance was tested against alternative dispersal hypotheses. Results Microsatellite markers revealed moderate to high levels of genetic diversity within populations, with those from the southern Limarí Valley showing the highest values and northern populations showing less exclusive alleles. Bayesian analysis of microsatellite data identified three genetic groups that corresponded to geographical ranges. Chloroplast phylogeography revealed no haplotypes shared between northern and southern ranges, and little haplotype sharing between the two neighbouring southern valleys. Dispersal models suggested the presence of extinct hypothetical populations between the southern and northern ranges. Main conclusions Our results are consistent with prolonged isolation of the northern and southern groups, mediated by the life‐history traits of the species. Significant isolation was revealed at both large and moderate distances as gene flow was not evident even between neighbouring valleys. Bayesian analyses of microsatellite and chloroplast haplotype diversity identified the southern area of Limarí as the probable area of origin of the species. Our data do not support recent dispersal of D. biloba from the southern range into Antofagasta, but indicate the fragmentation of an earlier wider range, concomitant with the Pliocene–Pleistocene climatic oscillations, with subsequent extinctions of the Atacama Desert populations and the divergence of the peripheral ones as a consequence of genetic drift.     

Refugia, dispersal and divergence in a forest archipelago: a study of Streptocarpus in eastern South Africa

We describe a scenario of plant speciation across a relict forest archipelago in South Africa involving Pleistocene habitat expansion-contraction cycles, dispersal and adaptation to lower temperatures. This is the first population level study using molecular data in South African forests and has significant implications for conservation efforts in this area. Populations of the mesophytic forest floor herbs Streptocarpus primulifolius sensu lato and Streptocarpus rexii were sampled throughout their range in the naturally fragmented forests of eastern South Africa in order to investigate population genetic and phylogenetic patterns within the species complex, using nuclear microsatellites, nuclear ribosomal ITS (internal transcribed spacer) sequences and chloroplast genome sequences. S. primulifolius harbours high levels of genetic diversity at both the nuclear (mean HE = 0.50) and the chloroplast level (each population fixed for a unique haplotype). This is consistent with populations of these coastal species being Pleistocene relicts. In contrast, populations of S. rexii in cooler habitats at higher altitudes and lower latitudes harbour little or no nuclear genetic diversity (mean HE = 0.09) and most share a common chloroplast haplotype. The split of S. rexii from populations intermediate between the two species (S. cf. primulifolius) occurred between 0 and 0.44 million years ago according to the calibrated ITS phylogeny of the taxa. The low genetic diversity and homogeneity of S. rexii is congruent with this species having reached its current range during the Holocene. We found no evidence of monophyly of any of the taxa in this study, which we consider a consequence of recent evolution in a fragmented habitat.     

Post-glacial history of Trillium grandiflorum (Melanthiaceae) in eastern North America: inferences from phylogeography

Dispersal and migration are important processes affecting the evolutionary history and genetics of species. Here we investigate post-glacial migration and gene flow in Trillium grandiflorum (Melanthiaceae), a wide-ranging, forest herb from eastern North America. Using phylogeographic approaches, we examined cpDNA and allozyme diversity in 35 populations of T. grandiflorum sampled from throughout the geographic range of the species. Nested clade analysis (NCA) of cpDNA haplotypes indicated that T. grandiflorum likely survived in two refugia in the southeastern US during the last glaciation and that long-distance dispersal characterized the post-glacial recolonization of northern areas. There was no evidence for reduced allozyme diversity in populations from glaciated compared to ice-free regions, probably because of the greater abundance and larger effective size of populations in the north. An analysis of isolation-by-distance based on the allozyme data suggested a pattern of population differentiation consistent with restricted gene flow. Notwithstanding the significance of rare seed dispersal events for migration, a comparison of allozyme and cpDNA genetic structure indicates that pollen flow between populations is more likely than seed dispersal. These results for T. grandiflorum represent the first phylogeographic analysis of a temperate woodland herb in eastern North America and support the importance of occasional long-distance dispersal events in the post-glacial migration of plants.     

Limited seed dispersal and microspatial population structure of an agamospermous grass of West African savannahs, Hyparrhenia diplandra (Poaceae)

We studied the microspatial population structure of the perennial tussock grass, Hyparrhenia diplandra (Poaceae), a facultative agamospermous species of West African savannahs. The microspatial population structure of H. diplandra was investigated by choosing two 100-m(2); quadrats at random from which all individuals were mapped. The genotype of every individual was determined using two highly polymorphic microsatellite loci. A chloroplast locus was also used to investigate the role of seed dispersal on the genetic structure of populations. The genetic diversity index (0.85) was high for a clonal species. Significant genetic differentiation over short distances was detected by F statistics, and spatial autocorrelation analyses within both quadrats showed significant isolation-by-distance patterns, both with the cytoplasmic locus and the nuclear loci. Some clones formed large patches (up to 5 m in diameter) whereas others were more scattered. However, the genetic differentiation between quadrats was much higher when studied with the cytoplasmic locus than with the nuclear loci, indicating that gene flow via pollen, but not seeds, may frequently occur between quadrats. The maintenance of genetic diversity in this facultative agamospermous species most likely results from several factors, such as low seed dispersal ability, nonnegligible gene flow through pollen, and selective pressures induced by regularly occurring fires in this ecosystem.     

Population size,center–periphery,and seed dispersers’ effects on the genetic diversity and population structure of the Mediterranean relict shrub Cneorum tricoccon

The effect of population size on population genetic diversity and structure has rarely been studied jointly with other factors such as the position of a population within the species’ distribution range or the presence of mutualistic partners influencing dispersal. Understanding these determining factors for genetic variation is critical for conservation of relict plants that are generally suffering from genetic deterioration. Working with 16 populations of the vulnerable relict shrub Cneorum tricoccon throughout the majority of its western Mediterranean distribution range, and using nine polymorphic microsatellite markers, we examined the effects of periphery (peripheral vs. central), population size (large vs. small), and seed disperser (introduced carnivores vs. endemic lizards) on the genetic diversity and population structure of the species. Contrasting genetic variation (H_E: 0.04–0.476) was found across populations. Peripheral populations showed lower genetic diversity, but this was dependent on population size. Large peripheral populations showed high levels of genetic diversity, whereas small central populations were less diverse. Significant isolation by distance was detected, indicating that the effect of long‐distance gene flow is limited relative to that of genetic drift, probably due to high selfing rates (F_IS = 0.155–0.887), restricted pollen flow, and ineffective seed dispersal. Bayesian clustering also supported the strong population differentiation and highly fragmented structure. Contrary to expectations, the type of disperser showed no significant effect on either population genetic diversity or structure. Our results challenge the idea of an effect of periphery per se that can be mainly explained by population size, drawing attention to the need of integrative approaches considering different determinants of genetic variation. Furthermore, the very low genetic diversity observed in several small populations and the strong among‐population differentiation highlight the conservation value of large populations throughout the species’ range, particularly in light of climate change and direct human threats.     

Patterns of pollen flow in a dense population of the insect-pollinated canopy tree species Castanopsis sieboldii

Insect pollinations of tree species with high-density populations have rarely been studied. Since the density of adults can affect effective pollen dispersal, short-distance pollination, even by insects, may frequently occur in high-density populations. To test this prediction, we investigated pollination patterns in a high-density population of the insect-pollinated canopy tree species Castanopsis sieboldii by paternity analysis using genotypes at 8 microsatellite loci of 145 adult trees and 439 seeds from 11 seed parents in a 4-ha plot. We then explored their genetic effects on the population by calculating other population genetics parameters. Although C. sieboldii has high potential for long-distance dispersal of pollen (as indicated by a fat-tailed dispersal kernel), the cumulative pollination at the local scale was spatially limited and strongly dependent on the distance between parents due to the high density of adults. Genetic diversity estimates for pollen pools accepted by each seed parent converged on a maximum as the effective number of pollen parents increased. The genetic diversity of pollen pool bulked over all the seed parents from inside the plot did not differ from that of the total pollen pools. Therefore, although pollen flow from distant pollen parents may help to maintain the genetic diversity of offspring, pollen parents neighboring seed parents may be the main contributors to the genetic diversity of the offspring at the seed stage.     

Population differentiation and gene flow within a metapopulation of a threatened tree, Magnolia stellata (Magnoliaceae)

We examined genetic differentiation among eight local populations of a metapopulation of Magnolia stellata using 10 nuclear and three chloroplast microsatellite (nSSR and cpSSR) markers and evaluated the influence of historical gene flow on population differentiation. The coefficient of genetic differentiation among populations for nSSR (F(ST) = 0.053) was less than half that for cpSSR (0.137). An isolation-by-distance pattern was detected for nSSRs, but not cpSSRs. These results suggest that pollen flow, as well as seed dispersal, has significantly reduced genetic differentiation among populations. We also examined patterns of contemporary pollen flow by paternity analysis of seeds from nine seed parents in one of the populations using the nSSR markers and found it to be greatly restricted by the distance between parents. Although most pollen flow occurred within the population, pollen flow from outside the population accounted for 2.5% of the total. When historical and contemporary pollen flows among populations were compared, the levels of pollen flow seem to have declined recently. We conclude that to conserve M. stellata, it is important to preserve the whole population by maintaining its metapopulation structure and the gene flow among its populations.