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      Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic

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          Abstract

          Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self‐sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first‐generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef‐building corals facing a rapidly changing environment.

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          Soft sweeps: molecular population genetics of adaptation from standing genetic variation.

          A population can adapt to a rapid environmental change or habitat expansion in two ways. It may adapt either through new beneficial mutations that subsequently sweep through the population or by using alleles from the standing genetic variation. We use diffusion theory to calculate the probabilities for selective adaptations and find a large increase in the fixation probability for weak substitutions, if alleles originate from the standing genetic variation. We then determine the parameter regions where each scenario-standing variation vs. new mutations-is more likely. Adaptations from the standing genetic variation are favored if either the selective advantage is weak or the selection coefficient and the mutation rate are both high. Finally, we analyze the probability of "soft sweeps," where multiple copies of the selected allele contribute to a substitution, and discuss the consequences for the footprint of selection on linked neutral variation. We find that soft sweeps with weaker selective footprints are likely under both scenarios if the mutation rate and/or the selection coefficient is high.
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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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              Genetic rescue to the rescue.

              Genetic rescue can increase the fitness of small, imperiled populations via immigration. A suite of studies from the past decade highlights the value of genetic rescue in increasing population fitness. Nonetheless, genetic rescue has not been widely applied to conserve many of the threatened populations that it could benefit. In this review, we highlight recent studies of genetic rescue and place it in the larger context of theoretical and empirical developments in evolutionary and conservation biology. We also propose directions to help shape future research on genetic rescue. Genetic rescue is a tool that can stem biodiversity loss more than has been appreciated, provides population resilience, and will become increasingly useful if integrated with molecular advances in population genomics.
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                Author and article information

                Contributors
                baums@psu.edu
                Journal
                Ecol Appl
                Ecol Appl
                10.1002/(ISSN)1939-5582
                EAP
                Ecological Applications
                John Wiley and Sons Inc. (Hoboken )
                1051-0761
                19 August 2019
                December 2019
                : 29
                : 8 ( doiID: 10.1002/eap.v29.8 )
                : e01978
                Affiliations
                [ 1 ] Department of Biology Pennsylvania State University University Park Pennsylvania 16803 USA
                [ 2 ] Department of Marine Biology and Ecology Rosenstiel School of Marine and Atmospheric Science University of Miami Miami Florida 33149 USA
                [ 3 ] Department of Biology Boston University Boston Massachusetts 02215 USA
                [ 4 ] School of Earth Sciences Ohio State University Columbus Ohio 43210 USA
                [ 5 ] Department of Biological Sciences University of Southern California Los Angeles California 90007 USA
                [ 6 ] U.S. Geological Survey 600 4th Street S. St. Petersburg Florida 33701 USA
                [ 7 ] Department of Integrative Biology The University of Texas at Austin Austin Texas 78712 USA
                [ 8 ] SECORE International Miami Florida 33145 USA
                [ 9 ] Department of Integrative Biology University of South Florida Tampa Florida 33620 USA
                Author notes
                [*] [* ]E‐mail: baums@ 123456psu.edu
                Author information
                https://orcid.org/0000-0001-6463-7308
                https://orcid.org/0000-0001-6053-9452
                https://orcid.org/0000-0001-8804-7847
                https://orcid.org/0000-0001-8386-3044
                https://orcid.org/0000-0001-5641-8914
                Article
                EAP1978
                10.1002/eap.1978
                6916196
                31332879
                e997c98d-2e44-4d56-a218-403f46ec12d6
                © 2019 The Authors. Ecological Applications published by Wiley Periodicals, Inc. on behalf of Ecological Society of America

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 25 March 2019
                : 13 June 2019
                : 21 June 2019
                Page count
                Figures: 3, Tables: 3, Pages: 23, Words: 19543
                Categories
                Article
                Articles
                Custom metadata
                2.0
                December 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.3 mode:remove_FC converted:17.12.2019

                adaptive potential,assisted gene flow,biomarkers,coral restoration,genetic diversity,inbreeding,outbreeding,phenotypic resilience,population enhancement,species selection,unintended selection

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