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      Multiple-Geographic-Scale Genetic Structure of Two Mangrove Tree Species: The Roles of Mating System, Hybridization, Limited Dispersal and Extrinsic Factors

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          Abstract

          Mangrove plants comprise a unique group of organisms that grow within the intertidal zones of tropical and subtropical regions and whose distributions are influenced by both biotic and abiotic factors. To understand how these extrinsic and intrinsic processes influence a more fundamental level of the biological hierarchy of mangroves, we studied the genetic diversity of two Neotropical mangrove trees, Avicenniagerminans and A. schaueriana, using microsatellites markers. As reported for other sea-dispersed species, there was a strong differentiation between A. germinans and A. schaueriana populations sampled north and south of the northeastern extremity of South America, likely due to the influence of marine superficial currents. Moreover, we observed fine-scale genetic structures even when no obvious physical barriers were present, indicating pollen and propagule dispersal limitation, which could be explained by isolation-by-distance coupled with mating system differences. We report the first evidence of ongoing hybridization between Avicennia species and that these hybrids are fertile, although this interspecific crossing has not contributed to an increase in the genetic diversity the populations where A. germinans and A. schaueriana hybridize. These findings highlight the complex interplay between intrinsic and extrinsic factors that shape the distribution of the genetic diversity in these sea-dispersed colonizer species.

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          Most cited references18

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          Mechanisms of long-distance seed dispersal.

          Growing recognition of the importance of long-distance dispersal (LDD) of plant seeds for various ecological and evolutionary processes has led to an upsurge of research into the mechanisms underlying LDD. We summarize these findings by formulating six generalizations stating that LDD is generally more common in open terrestrial landscapes, and is typically driven by large and migratory animals, extreme meteorological phenomena, ocean currents and human transportation, each transporting a variety of seed morphologies. LDD is often associated with unusual behavior of the standard vector inferred from plant dispersal morphology, or mediated by nonstandard vectors. To advance our understanding of LDD, we advocate a vector-based research approach that identifies the significant LDD vectors and quantifies how environmental conditions modify their actions.
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            Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations.

            Understanding the genetic composition and mating systems of edge populations provides important insights into the environmental and demographic factors shaping species' distribution ranges. We analysed samples of the mangrove Avicennia marina from Vietnam, northern Philippines and Australia, with microsatellite markers. We compared genetic diversity and structure in edge (Southeast Asia, and Southern Australia) and core (North and Eastern Australia) populations, and also compared our results with previously published data from core and southern edge populations. Comparisons highlighted significantly reduced gene diversity and higher genetic structure in both margins compared to core populations, which can be attributed to very low effective population size, pollinator scarcity and high environmental pressure at distribution margins. The estimated level of inbreeding was significantly higher in northeastern populations compared to core and southern populations. This suggests that despite the high genetic load usually associated with inbreeding, inbreeding or even selfing may be advantageous in margin habitats due to the possible advantages of reproductive assurance, or local adaptation. The very high level of genetic structure and inbreeding show that populations of A. marina are functioning as independent evolutionary units more than as components of a metapopulation system connected by gene flow. The combinations of those characteristics make these peripheral populations likely to develop local adaptations and therefore to be of particular interest for conservation strategies as well as for adaptation to possible future environmental changes.
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              Postglacial north-south expansion of populations of Rhizophora mangle (Rhizophoraceae) along the Brazilian coast revealed by microsatellite analysis.

              Red mangrove (Rhizophora mangle) dominates tropical tidal areas along both sides of the Atlantic, yet little is known about its degree of population differentiation over large geographical scales. Information on the genetic variability of mangrove species along the Brazilian coast is important not only for understanding the recent gene flow dynamic between populations, but also to evaluate models of evolutionary diversification and develop effective strategies for conservation. We investigated the genetic variability of the red mangrove along the Brazilian coast. Eight microsatellite loci were used to genotype 145 individuals across 10 populations spanning more than 4500 km of coast line. We estimated the genetic variability and structure of the populations and the historical gene flow between them. The level of genetic variability was low, with only 27 different alleles being detected and allele richness between 1.25 and 2.75. On the other hand, there was substantial population differentiation (R(st) = 0.48; P < 0.001), especially between the northern and southern populations. The populations from Pará and Maranhão had significantly greater genetic variability than did the remaining locations. This difference might reflect the older age of the northern mangroves, which likely remained stable during the Quaternary glaciations. The lowest variability observed in the southern populations of the red mangrove most likely reflects their recent age, associated with allelic reduction, resulting from the consecutive founder events that followed subsequent colonization of estuaries during the gradual warming by the end of the last glacial period.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 February 2015
                2015
                : 10
                : 2
                : e0118710
                Affiliations
                [1 ]Center for Molecular Biology and Genetic Engineering, University of Campinas, CP, Campinas, São Paulo, Brazil
                [2 ]São Paulo Agency for Agribusiness Technology, Piracicaba, São Paulo, Brazil
                [3 ]Department of Plant Biology, Institute of Biology, University of Campinas, Campinas, São Paulo, Brazil
                National Cheng-Kung University, TAIWAN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GMM MIZ APS. Performed the experiments: GMM. Analyzed the data: GMM MIZ. Contributed reagents/materials/analysis tools: APS. Wrote the paper: GMM MIZ APS.

                Article
                PONE-D-14-41392
                10.1371/journal.pone.0118710
                4344226
                25723532
                13c14e29-f139-40af-bcb0-7654a5f25581
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 14 September 2014
                : 7 January 2015
                Page count
                Figures: 7, Tables: 4, Pages: 23
                Funding
                The authors gratefully acknowledge the Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP) for financial support (2008/52045-0 and 2010/50178-2) and scholarships to GMM (2007/57021-9 and 2010/50033-4) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research fellowships to APS and MIZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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