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      Extreme seascape drives local recruitment and genetic divergence in brooding and spawning corals in remote north‐west Australia

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          Abstract

          Abstract Management strategies designed to conserve coral reefs threatened by climate change need to incorporate knowledge of the spatial distribution of inter‐ and intra‐specific genetic diversity. We characterized patterns of genetic diversity and connectivity using single nucleotide polymorphisms (SNPs) in two reef‐building corals to explore the eco‐evolutionary processes that sustain populations in north‐west Australia. Our sampling focused on the unique reefs of the Kimberley; we collected the broadcast spawning coral Acropora aspera (n = 534) and the brooding coral Isopora brueggemanni (n = 612) across inter‐archipelago (tens to hundreds of kilometres), inter‐reef (kilometres to tens of kilometres) and within‐reef (tens of metres to a few kilometres) scales. Initial analysis of A. aspera identified four highly divergent lineages that were co‐occurring but morphologically similar. Subsequent population analyses focused on the most abundant and widespread lineage, Acropora asp‐c. Although the overall level of geographic subdivision was greater in the brooder than in the spawner, fundamental similarities in patterns of genetic structure were evident. Most notably, limits to gene flow were observed at scales <35 kilometres. Further, we observed four discrete clusters and a semi‐permeable barrier to dispersal that were geographically consistent between species. Finally, sites experiencing bigger tides were more connected to the metapopulation and had greater gene diversity than those experiencing smaller tides. Our data indicate that the inshore reefs of the Kimberley are genetically isolated from neighbouring oceanic bioregions, but occasional dispersal between inshore archipelagos is important for the redistribution of evolutionarily important genetic diversity. Additionally, these results suggest that networks of marine reserves that effectively protect reefs from local pressures should be spaced within a few tens of kilometres to conserve the existing patterns of demographic and genetic connectivity.

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          Ecological consequences of genetic diversity.

          Understanding the ecological consequences of biodiversity is a fundamental challenge. Research on a key component of biodiversity, genetic diversity, has traditionally focused on its importance in evolutionary processes, but classical studies in evolutionary biology, agronomy and conservation biology indicate that genetic diversity might also have important ecological effects. Our review of the literature reveals significant effects of genetic diversity on ecological processes such as primary productivity, population recovery from disturbance, interspecific competition, community structure, and fluxes of energy and nutrients. Thus, genetic diversity can have important ecological consequences at the population, community and ecosystem levels, and in some cases the effects are comparable in magnitude to the effects of species diversity. However, it is not clear how widely these results apply in nature, as studies to date have been biased towards manipulations of plant clonal diversity, and little is known about the relative importance of genetic diversity vs. other factors that influence ecological processes of interest. Future studies should focus not only on documenting the presence of genetic diversity effects but also on identifying underlying mechanisms and predicting when such effects are likely to occur in nature.
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            Mechanisms of reef coral resistance to future climate change.

            Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years, acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems.
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              Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure.

              Population genetic theory predicts that plant populations will exhibit internal spatial autocorrelation when propagule flow is restricted, but as an empirical reality, spatial structure is rarely consistent across loci or sites, and is generally weak. A lack of sensitivity in the statistical procedures may explain the discrepancy. Most work to date, based on allozymes, has involved pattern analysis for individual alleles, but new PCR-based genetic markers are coming into vogue, with vastly increased numbers of alleles. The field is badly in need of an explicitly multivariate approach to autocorrelation analysis, and our purpose here is to introduce a new approach that is applicable to multiallelic codominant, multilocus arrays. The procedure treats the genetic data set as a whole, strengthening the spatial signal and reducing the stochastic (allele-to-allele, and locus-to-locus) noise. We (i) develop a very general multivariate method, based on genetic distance methods, (ii) illustrate it for multiallelic codominant loci, and (iii) provide nonparametric permutational testing procedures for the full correlogram. We illustrate the new method with an example data set from the orchid Caladenia tentaculata, for which we show (iv) how the multivariate treatment compares with the single-allele treatment, (v) that intermediate frequency alleles from highly polymorphic loci perform well and rare alleles poorly, (vi) that a multilocus treatment provides clearer answers than separate single-locus treatments, and (vii) that weighting alleles differentially improves our resolution minimally. The results, though specific to Caladenia, offer encouragement for wider application.
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                Author and article information

                Contributors
                (View ORCID Profile)
                (View ORCID Profile)
                Journal
                Evolutionary Applications
                Evol Appl
                Wiley
                1752-4571
                1752-4571
                June 22 2020
                Affiliations
                [1 ]Australian Institute of Marine ScienceIndian Oceans Marine Research Centre, Crawley Perth WA Australia
                [2 ]Western Australian Marine Science Institution Indian Ocean Marine Research Centre Crawley WA Australia
                [3 ]Trace and Environmental DNA Laboratory School of Molecular and Life Sciences Curtin University Bentley WA Australia
                [4 ]Department of Aquatic Zoology Western Australian Museum Welshpool WA Australia
                [5 ]CSIRO Oceans and AtmosphereIndian Oceans Marine Research Centre, Crawley Perth WA Australia
                [6 ]Bardi Jawi RangersKimberley Land Council Broome WA Australia
                Article
                10.1111/eva.13033
                fb91dc19-4353-4bbb-8f79-c6030329878f
                © 2020

                http://creativecommons.org/licenses/by/4.0/

                http://doi.wiley.com/10.1002/tdm_license_1.1

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