Evolutionary Dynamics of Wild Populations

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (30 November 2020) | Viewed by 39988

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Guest Editor
Station d’Ecologie Théorique et Expérimentale, UMR 5321, Centre National pour la Recherche Scientifique et Université Paul Sabatier, 09200 Moulis, France
Interests: evolutionary ecology; genomics; dispersal; freshwater microbiology; experimental evolution; metapopulation dynamics

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Guest Editor
Station d’Ecologie Théorique et Expérimentale, UMR 5321, Centre National pour la Recherche Scientifique et Université Paul Sabatier, 09200 Moulis, France
Interests: freshwater biology; evolutionary ecology; host–parasite interactions; non-genetic inheritance; community and ecosystem ecology; eco-evolutionary dynamics
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Special Issue Information

Dear Colleagues,

Wild populations are facing rapid and sometimes extreme environmental changes that are currently exacerbated by pressing human activities. A major scientific endeavor is to unravel the evolutionary processes allowing wild populations to adequately respond to these rapid and drastic environmental changes. In recent decades, the accumulation of empirical data as well as the development of new theories and molecular tools have largely improved our ability to tackle such a major question. In particular, there is now growing evidence that evolutionary processes (gene flow, drift, mutation, and natural selection) interact in sometimes complex ways to shape the rapid responses of organisms to changing environments, and this can lead to unexpected feedback between evolutionary and ecological dynamics. These rapid responses are sustained by genetic determinants in addition to alternative inheritance systems, including epigenetic and/or social avatars of information. Unravelling these underlying molecular mechanisms may change the design of management and conservation plans for wild populations.

In this Special Issue, we aim to present these novel research avenues on the evolutionary dynamics of wild populations so as to generate a general overview of the most up-to-date and fascinating studies. We specifically aim to integrate experimental, observational, and theoretical studies on wild populations that focus on (i) the role of dispersal as a process sustaining metapopulation dynamics in spatially structured landscapes, (ii) the genetic and non-genetic (including epigenetic) bases of adaptation, (iii) the reciprocal links between evolutionary and ecological dynamics over contemporary timescales, and (iv) the genomic and epigenomic conservation of wild populations. 

Dr. Delphine Legrand
Dr. Simon Blanchet
Guest Editors

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Keywords

  • eco-evolutionary dynamics
  • wild populations
  • heritability
  • quantitative genetics
  • dispersal
  • biodiversity
  • global change

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Published Papers (11 papers)

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Editorial

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3 pages, 148 KiB  
Editorial
Evolutionary Dynamics of Wild Populations
by Delphine Legrand and Simon Blanchet
Genes 2021, 12(5), 778; https://doi.org/10.3390/genes12050778 - 19 May 2021
Viewed by 1771
Abstract
Wild populations are facing rapid and sometimes extreme environmental changes that are currently exacerbated by pressing human activities [...] Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)

Research

Jump to: Editorial

14 pages, 2895 KiB  
Article
Associative Overdominance and Negative Epistasis Shape Genome-Wide Ancestry Landscape in Supplemented Fish Populations
by Maeva Leitwein, Hugo Cayuela and Louis Bernatchez
Genes 2021, 12(4), 524; https://doi.org/10.3390/genes12040524 - 3 Apr 2021
Cited by 4 | Viewed by 3022
Abstract
The interplay between recombination rate, genetic drift and selection modulates variation in genome-wide ancestry. Understanding the selective processes at play is of prime importance toward predicting potential beneficial or negative effects of supplementation with domestic strains (i.e., human-introduced strains). In a system of [...] Read more.
The interplay between recombination rate, genetic drift and selection modulates variation in genome-wide ancestry. Understanding the selective processes at play is of prime importance toward predicting potential beneficial or negative effects of supplementation with domestic strains (i.e., human-introduced strains). In a system of lacustrine populations supplemented with a single domestic strain, we documented how population genetic diversity and stocking intensity produced lake-specific patterns of domestic ancestry by taking the species’ local recombination rate into consideration. We used 552 Brook Charr (Salvelinus fontinalis) from 22 small lacustrine populations, genotyped at ~32,400 mapped SNPs. We observed highly variable patterns of domestic ancestry between each of the 22 populations without any consistency in introgression patterns of the domestic ancestry. Our results suggest that such lake-specific ancestry patterns were mainly due to variable associative overdominance (AOD) effects among populations (i.e., potential positive effects due to the masking of possible deleterious alleles in low recombining regions). Signatures of AOD effects were also emphasized by highly variable patterns of genetic diversity among and within lakes, potentially driven by predominant genetic drift in those small isolated populations. Local negative effects such as negative epistasis (i.e., potential genetic incompatibilities between the native and the introduced population) potentially reflecting precursory signs of outbreeding depression were also observed at a chromosomal scale. Consequently, in order to improve conservation practices and management strategies, it became necessary to assess the consequences of supplementation at the population level by taking into account both genetic diversity and stocking intensity when available. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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15 pages, 2016 KiB  
Article
Adaptive Divergence under Gene Flow along an Environmental Gradient in Two Coexisting Stickleback Species
by Thijs M. P. Bal, Alejandro Llanos-Garrido, Anurag Chaturvedi, Io Verdonck, Bart Hellemans and Joost A. M. Raeymaekers
Genes 2021, 12(3), 435; https://doi.org/10.3390/genes12030435 - 18 Mar 2021
Cited by 5 | Viewed by 3323
Abstract
There is a general and solid theoretical framework to explain how the interplay between natural selection and gene flow affects local adaptation. Yet, to what extent coexisting closely related species evolve collectively or show distinctive evolutionary responses remains a fundamental question. To address [...] Read more.
There is a general and solid theoretical framework to explain how the interplay between natural selection and gene flow affects local adaptation. Yet, to what extent coexisting closely related species evolve collectively or show distinctive evolutionary responses remains a fundamental question. To address this, we studied the population genetic structure and morphological differentiation of sympatric three-spined and nine-spined stickleback. We conducted genotyping-by-sequencing and morphological trait characterisation using 24 individuals of each species from four lowland brackish water (LBW), four lowland freshwater (LFW) and three upland freshwater (UFW) sites in Belgium and the Netherlands. This combination of sites allowed us to contrast populations from isolated but environmentally similar locations (LFW vs. UFW), isolated but environmentally heterogeneous locations (LBW vs. UFW), and well-connected but environmentally heterogenous locations (LBW vs. LFW). Overall, both species showed comparable levels of genetic diversity and neutral genetic differentiation. However, for all three spatial scales, signatures of morphological and genomic adaptive divergence were substantially stronger among populations of the three-spined stickleback than among populations of the nine-spined stickleback. Furthermore, most outlier SNPs in the two species were associated with local freshwater sites. The few outlier SNPs that were associated with the split between brackish water and freshwater populations were located on one linkage group in three-spined stickleback and two linkage groups in nine-spined stickleback. We conclude that while both species show congruent evolutionary and genomic patterns of divergent selection, both species differ in the magnitude of their response to selection regardless of the geographical and environmental context. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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16 pages, 1870 KiB  
Article
Congruent Genetic and Demographic Dispersal Rates in a Natural Metapopulation at Equilibrium
by Delphine Legrand, Michel Baguette, Jérôme G. Prunier, Quentin Dubois, Camille Turlure and Nicolas Schtickzelle
Genes 2021, 12(3), 362; https://doi.org/10.3390/genes12030362 - 3 Mar 2021
Cited by 2 | Viewed by 2209
Abstract
Understanding the functioning of natural metapopulations at relevant spatial and temporal scales is necessary to accurately feed both theoretical eco-evolutionary models and conservation plans. One key metric to describe the dynamics of metapopulations is dispersal rate. It can be estimated with either direct [...] Read more.
Understanding the functioning of natural metapopulations at relevant spatial and temporal scales is necessary to accurately feed both theoretical eco-evolutionary models and conservation plans. One key metric to describe the dynamics of metapopulations is dispersal rate. It can be estimated with either direct field estimates of individual movements or with indirect molecular methods, but the two approaches do not necessarily match. We present a field study in a large natural metapopulation of the butterfly Boloria eunomia in Belgium surveyed over three generations using synchronized demographic and genetic datasets with the aim to characterize its genetic structure, its dispersal dynamics, and its demographic stability. By comparing the census and effective population sizes, and the estimates of dispersal rates, we found evidence of stability at several levels: constant inter-generational ranking of population sizes without drastic historical changes, stable genetic structure and geographically-influenced dispersal movements. Interestingly, contemporary dispersal estimates matched between direct field and indirect genetic assessments. We discuss the eco-evolutionary mechanisms that could explain the described stability of the metapopulation, and suggest that destabilizing agents like inter-generational fluctuations in population sizes could be controlled by a long adaptive history of the species to its dynamic local environment. We finally propose methodological avenues to further improve the match between demographic and genetic estimates of dispersal. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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14 pages, 1475 KiB  
Article
Phenotypic Response to Light Versus Shade Associated with DNA Methylation Changes in Snapdragon Plants (Antirrhinum majus)
by Pierick Mouginot, Nelia Luviano Aparicio, Delphine Gourcilleau, Mathieu Latutrie, Sara Marin, Jean-Louis Hemptinne, Christoph Grunau and Benoit Pujol
Genes 2021, 12(2), 227; https://doi.org/10.3390/genes12020227 - 4 Feb 2021
Cited by 6 | Viewed by 3621
Abstract
The phenotypic plasticity of plants in response to change in their light environment, and in particularly, to shade is a schoolbook example of ecologically relevant phenotypic plasticity with evolutionary adaptive implications. Epigenetic variation is known to potentially underlie plant phenotypic plasticity. Yet, little [...] Read more.
The phenotypic plasticity of plants in response to change in their light environment, and in particularly, to shade is a schoolbook example of ecologically relevant phenotypic plasticity with evolutionary adaptive implications. Epigenetic variation is known to potentially underlie plant phenotypic plasticity. Yet, little is known about its role in ecologically and evolutionary relevant mechanisms shaping the diversity of plant populations in nature. Here we used a reference-free reduced representation bisulfite sequencing method for non-model organisms (epiGBS) to investigate changes in DNA methylation patterns across the genome in snapdragon plants (Antirrhinum majus L.). We exposed plants to sunlight versus artificially induced shade in four highly inbred lines to exclude genetic confounding effects. Our results showed that phenotypic plasticity in response to light versus shade shaped vegetative traits. They also showed that DNA methylation patterns were modified under light versus shade, with a trend towards global effects over the genome but with large effects found on a restricted portion. We also detected the existence of a correlation between phenotypic and epigenetic variation that neither supported nor rejected its potential role in plasticity. While our findings imply epigenetic changes in response to light versus shade environments in snapdragon plants, whether these changes are directly involved in the phenotypic plastic response of plants remains to be investigated. Our approach contributed to this new finding but illustrates the limits in terms of sample size and statistical power of population epigenetic approaches in non-model organisms. Pushing this boundary will be necessary before the relationship between environmentally induced epigenetic changes and phenotypic plasticity is clarified for ecologically relevant mechanisms with evolutionary implications. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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18 pages, 1559 KiB  
Article
Patterns of Epigenetic Diversity in Two Sympatric Fish Species: Genetic vs. Environmental Determinants
by Laura Fargeot, Géraldine Loot, Jérôme G. Prunier, Olivier Rey, Charlotte Veyssière and Simon Blanchet
Genes 2021, 12(1), 107; https://doi.org/10.3390/genes12010107 - 16 Jan 2021
Cited by 10 | Viewed by 4265
Abstract
Epigenetic components are hypothesized to be sensitive to the environment, which should permit species to adapt to environmental changes. In wild populations, epigenetic variation should therefore be mainly driven by environmental variation. Here, we tested whether epigenetic variation (DNA methylation) observed in wild [...] Read more.
Epigenetic components are hypothesized to be sensitive to the environment, which should permit species to adapt to environmental changes. In wild populations, epigenetic variation should therefore be mainly driven by environmental variation. Here, we tested whether epigenetic variation (DNA methylation) observed in wild populations is related to their genetic background, and/or to the local environment. Focusing on two sympatric freshwater fish species (Gobio occitaniae and Phoxinus phoxinus), we tested the relationships between epigenetic differentiation, genetic differentiation (using microsatellite and single nucleotide polymorphism (SNP) markers), and environmental distances between sites. We identify positive relationships between pairwise genetic and epigenetic distances in both species. Moreover, epigenetic marks better discriminated populations than genetic markers, especially in G. occitaniae. In G. occitaniae, both pairwise epigenetic and genetic distances were significantly associated to environmental distances between sites. Nonetheless, when controlling for genetic differentiation, the link between epigenetic differentiation and environmental distances was not significant anymore, indicating a noncausal relationship. Our results suggest that fish epigenetic variation is mainly genetically determined and that the environment weakly contributed to epigenetic variation. We advocate the need to control for the genetic background of populations when inferring causal links between epigenetic variation and environmental heterogeneity in wild populations. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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17 pages, 1255 KiB  
Article
Targeted Sequencing of Mitochondrial Genes Reveals Signatures of Molecular Adaptation in a Nearly Panmictic Small Pelagic Fish Species
by Miguel Baltazar-Soares, André Ricardo de Araújo Lima and Gonçalo Silva
Genes 2021, 12(1), 91; https://doi.org/10.3390/genes12010091 - 13 Jan 2021
Cited by 12 | Viewed by 4794
Abstract
Ongoing climatic changes, with predictable impacts on marine environmental conditions, are expected to trigger organismal responses. Recent evidence shows that, in some marine species, variation in mitochondrial genes involved in the aerobic conversion of oxygen into ATP at the cellular level correlate with [...] Read more.
Ongoing climatic changes, with predictable impacts on marine environmental conditions, are expected to trigger organismal responses. Recent evidence shows that, in some marine species, variation in mitochondrial genes involved in the aerobic conversion of oxygen into ATP at the cellular level correlate with gradients of sea surface temperature and gradients of dissolved oxygen. Here, we investigated the adaptive potential of the European sardine Sardina pilchardus populations offshore the Iberian Peninsula. We performed a seascape genetics approach that consisted of the high throughput sequencing of mitochondria’s ATP6, COI, CYTB and ND5 and five microsatellite loci on 96 individuals coupled with environmental information on sea surface temperature and dissolved oxygen across five sampling locations. Results show that, despite sardines forming a nearly panmictic population around Iberian Peninsula, haplotype frequency distribution can be explained by gradients of minimum sea surface temperature and dissolved oxygen. We further identified that the frequencies of the most common CYTB and ATP6 haplotypes negatively correlate with minimum sea surface temperature across the sampled area, suggestive of a signature of selection. With signatures of selection superimposed on highly connected populations, sardines may be able to follow environmental optima and shift their distribution northwards as a response to the increasing sea surface temperatures. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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19 pages, 6823 KiB  
Article
The Role of Microbiome and Genotype in Daphnia magna upon Parasite Re-Exposure
by Lore Bulteel, Shira Houwenhuyse, Steven A. J. Declerck and Ellen Decaestecker
Genes 2021, 12(1), 70; https://doi.org/10.3390/genes12010070 - 7 Jan 2021
Cited by 10 | Viewed by 4802
Abstract
Recently, it has been shown that the community of gut microorganisms plays a crucial role in host performance with respect to parasite tolerance. Knowledge, however, is lacking on the role of the gut microbiome in mediating host tolerance after parasite re-exposure, especially considering [...] Read more.
Recently, it has been shown that the community of gut microorganisms plays a crucial role in host performance with respect to parasite tolerance. Knowledge, however, is lacking on the role of the gut microbiome in mediating host tolerance after parasite re-exposure, especially considering multiple parasite infections. We here aimed to fill this knowledge gap by studying the role of the gut microbiome on tolerance in Daphnia magna upon multiple parasite species re-exposure. Additionally, we investigated the role of the host genotype in the interaction between the gut microbiome and the host phenotypic performance. A microbiome transplant experiment was performed in which three germ-free D. magna genotypes were exposed to a gut microbial inoculum and a parasite community treatment. The gut microbiome inocula were pre-exposed to the same parasite communities or a control treatment. Daphnia performance was monitored, and amplicon sequencing was performed to characterize the gut microbial community. Our experimental results showed that the gut microbiome plays no role in Daphnia tolerance upon parasite re-exposure. We did, however, find a main effect of the gut microbiome on Daphnia body size reflecting parasite specific responses. Our results also showed that it is rather the Daphnia genotype, and not the gut microbiome, that affected parasite-induced host mortality. Additionally, we found a role of the genotype in structuring the gut microbial community, both in alpha diversity as in the microbial composition. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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13 pages, 1048 KiB  
Article
Soft Selective Sweep on Chemosensory Genes Correlates with Ancestral Preference for Toxic Noni in a Specialist Drosophila Population
by Erina A. Ferreira, Sophia Lambert, Thibault Verrier, Frédéric Marion-Poll and Amir Yassin
Genes 2021, 12(1), 32; https://doi.org/10.3390/genes12010032 - 29 Dec 2020
Cited by 7 | Viewed by 3485
Abstract
Understanding how organisms adapt to environmental changes is a major question in evolution and ecology. In particular, the role of ancestral variation in rapid adaptation remains unclear because its trace on genetic variation, known as soft selective sweep, is often hardly recognizable from [...] Read more.
Understanding how organisms adapt to environmental changes is a major question in evolution and ecology. In particular, the role of ancestral variation in rapid adaptation remains unclear because its trace on genetic variation, known as soft selective sweep, is often hardly recognizable from genome-wide selection scans. Here, we investigate the evolution of chemosensory genes in Drosophila yakuba mayottensis, a specialist subspecies on toxic noni (Morinda citrifolia) fruits on the island of Mayotte. We combine population genomics analyses and behavioral assays to evaluate the level of divergence in chemosensory genes and perception of noni chemicals between specialist and generalist subspecies of D. yakuba. We identify a signal of soft selective sweep on a handful of genes, with the most diverging ones involving a cluster of gustatory receptors expressed in bitter-sensing neurons. Our results highlight the potential role of ancestral genetic variation in promoting host plant specialization in herbivorous insects and identify a number of candidate genes underlying behavioral adaptation. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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20 pages, 1362 KiB  
Article
Using Reciprocal Transplants to Assess Local Adaptation, Genetic Rescue, and Sexual Selection in Newly Established Populations
by Jacques Labonne, Aurélie Manicki, Louise Chevalier, Marin Tétillon, François Guéraud and Andrew P. Hendry
Genes 2021, 12(1), 5; https://doi.org/10.3390/genes12010005 - 23 Dec 2020
Cited by 2 | Viewed by 3734
Abstract
Small populations establishing on colonization fronts have to adapt to novel environments with limited genetic variation. The pace at which they can adapt, and the influence of genetic variation on their success, are key questions for understanding intraspecific diversity. To investigate these topics, [...] Read more.
Small populations establishing on colonization fronts have to adapt to novel environments with limited genetic variation. The pace at which they can adapt, and the influence of genetic variation on their success, are key questions for understanding intraspecific diversity. To investigate these topics, we performed a reciprocal transplant experiment between two recently founded populations of brown trout in the sub-Antarctic Kerguelen Islands. Using individual tagging and genetic assignment methods, we tracked the fitness of local and foreign individuals, as well as the fitness of their offspring over two generations. In both populations, although not to the same extent, gene flow occurred between local and foreign gene pools. In both cases, however, we failed to detect obvious footprints of local adaptation (which should limit gene flow) and only weak support for genetic rescue (which should enhance gene flow). In the population where gene flow from foreign individuals was low, no clear differences were observed between the fitness of local, foreign, and F1 hybrid individuals. In the population where gene flow was high, foreign individuals were successful due to high mating success rather than high survival, and F1 hybrids had the same fitness as pure local offspring. These results suggest the importance of considering sexual selection, rather than just local adaptation and genetic rescue, when evaluating the determinants of success in small and recently founded populations. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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20 pages, 5293 KiB  
Article
A Disjunctive Marginal Edge of Evergreen Broad-Leaved Oak (Quercus gilva) in East Asia: The High Genetic Distinctiveness and Unusual Diversity of Jeju Island Populations and Insight into a Massive, Independent Postglacial Colonization
by Eun-Kyeong Han, Won-Bum Cho, Jong-Soo Park, In-Su Choi, Myounghai Kwak, Bo-Yun Kim and Jung-Hyun Lee
Genes 2020, 11(10), 1114; https://doi.org/10.3390/genes11101114 - 23 Sep 2020
Cited by 16 | Viewed by 3379
Abstract
Jeju Island is located at a marginal edge of the distributional range of East Asian evergreen broad-leaved forests. The low genetic diversity of such edge populations is predicted to have resulted from genetic drift and reduced gene flow when compared to core populations. [...] Read more.
Jeju Island is located at a marginal edge of the distributional range of East Asian evergreen broad-leaved forests. The low genetic diversity of such edge populations is predicted to have resulted from genetic drift and reduced gene flow when compared to core populations. To test this hypothesis, we examined the levels of genetic diversity of marginal-edge populations of Quercus gilva, restricted to a few habitats on Jeju Island, and compared them with the southern Kyushu populations. We also evaluated their evolutionary potential and conservation value. The genetic diversity and structure were analyzed using 40 polymorphic microsatellite markers developed in this study. Ecological Niche Modeling (ENM) has been employed to develop our insights, which can be inferred from historical distribution changes. Contrary to our expectations, we detected a similar level of genetic diversity in the Jeju populations, comparable to that of the southern Kyushu populations, which have been regarded as long-term glacial refugia with a high genetic variability of East Asian evergreen trees. We found no signatures of recent bottlenecks in the Jeju populations. The results of STRUCTURE, neighbor-joining phylogeny, and Principal Coordinate Analysis (PCoA) with a significant barrier clearly demonstrated that the Jeju and Kyushu regions are genetically distinct. However, ENM showed that the probability value for the distribution of the trees on Jeju Island during the Last Glacial Maximum (LGM) converge was zero. In consideration of these results, we hypothesize that independent massive postglacial colonization from a separate large genetic source, other than Kyushu, could have led to the current genetic diversity of Jeju Island. Therefore, we suggest that the Jeju populations deserve to be separately managed and designated as a level of management unit (MU). These findings improve our understanding of the paleovegetation of East Asian evergreen forests, and the microevolution of oaks. Full article
(This article belongs to the Special Issue Evolutionary Dynamics of Wild Populations)
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