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      Non-Density Dependent Pollen Dispersal of Shorea maxwelliana (Dipterocarpaceae) Revealed by a Bayesian Mating Model Based on Paternity Analysis in Two Synchronized Flowering Seasons

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          Abstract

          Pollinator syndrome is one of the most important determinants regulating pollen dispersal in tropical tree species. It has been widely accepted that the reproduction of tropical forest species, especially dipterocarps that rely on insects with weak flight for their pollination, is positively density-dependent. However differences in pollinator syndrome should affect pollen dispersal patterns and, consequently, influence genetic diversity via the mating process. We examined the pollen dispersal pattern and mating system of Shorea maxwelliana, the flowers of which are larger than those of Shorea species belonging to section Mutica which are thought to be pollinated by thrips (weak flyers). A Bayesian mating model based on the paternity of seeds collected from mother trees during sporadic and mass flowering events revealed that the estimated pollen dispersal kernel and average pollen dispersal distance were similar for both flowering events. This evidence suggests that the putative pollinators – small beetles and weevils – effectively contribute to pollen dispersal and help to maintain a high outcrossing rate even during sporadic flowering events. However, the reduction in pollen donors during a sporadic event results in a reduction in effective pollen donors, which should lead to lower genetic diversity in the next generation derived from seeds produced during such an event. Although sporadic flowering has been considered less effective for outcrossing in Shorea species that depend on thrips for their pollination, effective pollen dispersal by the small beetles and weevils ensures outcrossing during periods of low flowering tree density, as occurs in a sporadic flowering event.

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          Most cited references23

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          Rapid isolation of high molecular weight plant DNA.

          A method is presented for the rapid isolation of high molecular weight plant DNA (50,000 base pairs or more in length) which is free of contaminants which interfere with complete digestion by restriction endonucleases. The procedure yields total cellular DNA (i.e. nuclear, chloroplast, and mitochondrial DNA). The technique is ideal for the rapid isolation of small amounts of DNA from many different species and is also useful for large scale isolations.
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            Statistical confidence for likelihood-based paternity inference in natural populations.

            Paternity inference using highly polymorphic codominant markers is becoming common in the study of natural populations. However, multiple males are often found to be genetically compatible with each offspring tested, even when the probability of excluding an unrelated male is high. While various methods exist for evaluating the likelihood of paternity of each nonexcluded male, interpreting these likelihoods has hitherto been difficult, and no method takes account of the incomplete sampling and error-prone genetic data typical of large-scale studies of natural systems. We derive likelihood ratios for paternity inference with codominant markers taking account of typing error, and define a statistic delta for resolving paternity. Using allele frequencies from the study population in question, a simulation program generates criteria for delta that permit assignment of paternity to the most likely male with a known level of statistical confidence. The simulation takes account of the number of candidate males, the proportion of males that are sampled and gaps and errors in genetic data. We explore the potentially confounding effect of relatives and show that the method is robust to their presence under commonly encountered conditions. The method is demonstrated using genetic data from the intensively studied red deer (Cervus elaphus) population on the island of Rum, Scotland. The Windows-based computer program, CERVUS, described in this study is available from the authors. CERVUS can be used to calculate allele frequencies, run simulations and perform parentage analysis using data from all types of codominant markers.
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              Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest.

              Tropical rainforest trees typically occur in low population densities and rely on animals for cross-pollination. It is of conservation interest therefore to understand how rainforest fragmentation may alter the pollination and breeding structure of remnant trees. Previous studies of the Amazonian tree Dinizia excelsa (Fabaceae) found African honeybees (Apis mellifera scutellata) as the predominant pollinators of trees in highly disturbed habitats, transporting pollen up to 3.2 km between pasture trees. Here, using microsatellite genotypes of seed arrays, we compare outcrossing rates and pollen dispersal distances of (i) remnant D. excelsa in three large ranches, and (ii) a population in undisturbed forest in which African honeybees were absent. Self-fertilization was more frequent in the disturbed habitats (14%, n = 277 seeds from 12 mothers) than in undisturbed forest (10%, n = 295 seeds from 13 mothers). Pollen dispersal was extensive in all three ranches compared to undisturbed forest, however. Using a twogener analysis, we estimated a mean pollen dispersal distance of 1509 m in Colosso ranch, assuming an exponential dispersal function, and 212 m in undisturbed forest. The low effective density of D. excelsa in undisturbed forest (approximately 0.1 trees/ha) indicates that large areas of rainforest must be preserved to maintain minimum viable populations. Our results also suggest, however, that in highly disturbed habitats Apis mellifera may expand genetic neighbourhood areas, thereby linking fragmented and continuous forest populations.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                31 December 2013
                : 8
                : 12
                : e82039
                Affiliations
                [1 ]School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
                [2 ]Forestry Division, Japan International Research Center for Agricultural Sciences, Tsukuba, Ibaraki, Japan
                [3 ]Department of Forest Genetics, Forestry and Forest Products Research Institute, Tsukuba, Japan
                [4 ]Forestry Biotechnology Division, Forest Research Institute Malaysia, Kepong, Selangor Darul Ehsan, Malaysia
                [5 ]Graduate School for International Development and Cooperation, Hiroshima University, Higashi-Hiroshima, Hiroshima, Japan
                [6 ]Faculty and Graduate School of Urban Environmental Sciences, Tokyo Metropolitan University, Hachioji, Tokyo, Japan
                Institute of Botany, Chinese Academy of Sciences, China
                Author notes

                Competing Interests: Shinsuke Masuda, is currently working in a private company, Kajima Corporation. However, all research activities were conducted in his previous affiliation, University of Tsukuba. Therefore, this company doesn't have any relationship with the authors' research. The authors declare that there are no competing interests with the company. And all of authors declare that this does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: SM NT YT. Performed the experiments: SM NT SLL NM. Analyzed the data: SM NT. Contributed reagents/materials/analysis tools: SM NT SU SLL NM TK SN YT. Wrote the manuscript: SM NT SU TK YT. Designed the software used in analysis: NT.

                [¤]

                Current address: Kajima Corporation, Motoakasaka, Minato-ku, Tokyo, Japan

                Article
                PONE-D-13-29443
                10.1371/journal.pone.0082039
                3876983
                64cd13c0-f5ab-4cd2-a4b1-608c27818c65
                Copyright @ 2013

                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
                : 16 July 2013
                : 20 October 2013
                Page count
                Pages: 12
                Funding
                The research budget to produce the manuscript was partly provided from agencies listed: Grant No. 18255010 of a Grant-in-Aid for Scientific Research from Japan Society for the Promotion of Science ( http://www.jsps.go.jp/english/index.html), Grant No. E-091 of Environment Research and Technology Development Fund from Ministry of Environment, Japan ( http://www.env.go.jp/policy/kenkyu/suishin/english/index.html). There are no funders to provide research funding to produce the manuscript except the two funders listed above. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Agriculture
                Forestry
                Biology
                Ecology
                Community Ecology
                Species Interactions
                Evolutionary Ecology
                Population Ecology
                Evolutionary Biology
                Population Genetics
                Effective Population Size
                Gene Flow
                Genetics
                Population Genetics
                Effective Population Size
                Gene Flow
                Population Biology
                Population Genetics
                Effective Population Size
                Gene Flow
                Population Ecology

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                Uncategorized

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