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      Genetic diversity and population divergences of an indigenous tree ( Coffea mauritiana) in Reunion Island: role of climatic and geographical factors

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          Abstract

          Oceanic islands are commonly considered as natural laboratories for studies on evolution and speciation. The evolutionary specificities of islands associated with species biology provide unique scenarios to study the role of geography and climate in driving population divergence. However, few studies have addressed this subject in small oceanic islands with heterogeneous climates. Being widely distributed in Reunion Island forest, Coffea mauritiana represents an interesting model case for investigating patterns of within-island differentiation at small spatial scale. In this study, we examined the genetic diversity and population divergences of C. mauritiana using SNP markers obtained from 323 individuals across 34 locations in Reunion Island. Using redundancy analysis, we further evaluated the contribution of geographic and climatic factors to shaping genetic divergence among populations. Genetic diversity analyses revealed that accessions clustered according to the source population, with further grouping in regional clusters. Genetic relationships among the regional clusters underlined a recent process of expansion in the form of step-by-step colonization on both sides of the island. Divergence among source populations was mostly driven by the joint effect of geographic distance and climatic heterogeneity. The pattern of isolation-by-geography was in accordance with the dispersal characteristics of the species, while isolation-by-environment was mostly explained by the heterogeneous rainfall patterns, probably associated with an asynchronous flowering among populations. These findings advance our knowledge on the patterns of genetic diversity and factors of population differentiation of species native to Reunion Island, and will also usefully guide forest management for conservation.

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          Most cited references51

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          Divergent selection and heterogeneous genomic divergence.

          Levels of genetic differentiation between populations can be highly variable across the genome, with divergent selection contributing to such heterogeneous genomic divergence. For example, loci under divergent selection and those tightly physically linked to them may exhibit stronger differentiation than neutral regions with weak or no linkage to such loci. Divergent selection can also increase genome-wide neutral differentiation by reducing gene flow (e.g. by causing ecological speciation), thus promoting divergence via the stochastic effects of genetic drift. These consequences of divergent selection are being reported in recently accumulating studies that identify: (i) 'outlier loci' with higher levels of divergence than expected under neutrality, and (ii) a positive association between the degree of adaptive phenotypic divergence and levels of molecular genetic differentiation across population pairs ['isolation by adaptation' (IBA)]. The latter pattern arises because as adaptive divergence increases, gene flow is reduced (thereby promoting drift) and genetic hitchhiking increased. Here, we review and integrate these previously disconnected concepts and literatures. We find that studies generally report 5-10% of loci to be outliers. These selected regions were often dispersed across the genome, commonly exhibited replicated divergence across different population pairs, and could sometimes be associated with specific ecological variables. IBA was not infrequently observed, even at neutral loci putatively unlinked to those under divergent selection. Overall, we conclude that divergent selection makes diverse contributions to heterogeneous genomic divergence. Nonetheless, the number, size, and distribution of genomic regions affected by selection varied substantially among studies, leading us to discuss the potential role of divergent selection in the growth of regions of differentiation (i.e. genomic islands of divergence), a topic in need of future investigation.
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            Do island populations have less genetic variation than mainland populations?

            R Frankham (1997)
            Island populations are much more prone to extinction than mainland populations. The reasons for this remain controversial. If inbreeding and loss of genetic variation are involved, then genetic variation must be lower on average in island than mainland populations. Published data on levels of genetic variation for allozymes, nuclear DNA markers, mitochondrial DNA, inversions and quantitative characters in island and mainland populations were analysed. A large and highly significant majority of island populations have less allozyme genetic variation than their mainland counterparts (165 of 202 comparisons), the average reduction being 29 per cent. The magnitude of differences was related to dispersal ability. There were related differences for all the other measures. Island endemic species showed lower genetic variation than related mainland species in 34 of 38 cases. The proportionate reduction in genetic variation was significantly greater in island endemic than in nonendemic island populations in mammals and birds, but not in insects. Genetic factors cannot be discounted as a cause of higher extinction rates of island than mainland populations.
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              Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization.

              Empirical population genetic studies have been dominated by a neutralist view, according to which gene flow and drift are the main forces driving population genetic structure in nature. The neutralist view in essence describes a process of isolation by dispersal limitation (IBDL) that generally leads to a pattern of isolation by distance (IBD). Recently, however, conceptual frameworks have been put forward that view local genetic adaptation as an important driver of population genetic structure. Isolation by adaptation (IBA) and monopolization (M) posit that gene flow among natural populations is reduced as a consequence of local genetic adaptation. IBA stresses that effective gene flow is reduced among habitats that show dissimilar ecological characteristics, leading to a pattern of isolation by environment. In monopolization, local genetic adaptation of initial colonizing genotypes results in a reduction in gene flow that fosters the persistence of founder effects. Here, we relate these different processes driving landscape genetic structure to patterns of IBD and isolation by environment (IBE). We propose a method to detect whether IBDL, IBA and M shape genetic differentiation in natural landscapes by studying patterns of variation at neutral and non-neutral markers as well as at ecologically relevant traits. Finally, we reinterpret a representative number of studies from the recent literature by associating patterns to processes and identify patterns associated with local genetic adaptation to be as common as IBDL in structuring regional genetic variation of populations in the wild. Our results point to the importance of quantifying environmental gradients and incorporating ecology in the analysis of population genetics. © 2013 John Wiley & Sons Ltd.
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                Author and article information

                Contributors
                philippe.lashermes@ird.fr
                Journal
                Heredity (Edinb)
                Heredity (Edinb)
                Heredity
                Springer International Publishing (Cham )
                0018-067X
                1365-2540
                26 November 2018
                26 November 2018
                June 2019
                : 122
                : 6
                : 833-847
                Affiliations
                GRID grid.503155.7, IRD, , University of Montpellier, DIADE, ; Montpellier, France
                Author information
                http://orcid.org/0000-0001-5569-0895
                http://orcid.org/0000-0002-0531-5146
                http://orcid.org/0000-0001-7692-9076
                Article
                168
                10.1038/s41437-018-0168-9
                6781115
                30478354
                cb373405-149f-4fae-9ce5-371881939b96
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 8 August 2018
                : 9 November 2018
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                © The Genetics Society 2019

                Human biology
                population genetics,biodiversity
                Human biology
                population genetics, biodiversity

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