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      Historical Environment Is Reflected in Modern Population Genetics and Biogeography of an Island Endemic Lizard ( Xantusia riversiana reticulata)

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          Abstract

          The restricted distribution and isolation of island endemics often produces unique genetic and phenotypic diversity of conservation interest to management agencies. However, these isolated species, especially those with sensitive life history traits, are at high risk for the adverse effects of genetic drift and habitat degradation by non-native wildlife. Here, we study the population genetic diversity, structure, and stability of a classic “island giant” ( Xantusia riversiana, the Island Night Lizard) on San Clemente Island, California following the removal of feral goats. Using DNA microsatellites, we found that this population is reasonably genetically robust despite historical grazing, with similar effective population sizes and genetic diversity metrics across all sampling locations irrespective of habitat type and degree of degradation. However, we also found strong site-specific patterns of genetic variation and low genetic diversity compared to mainland congeners, warranting continued special management as an island endemic. We identify both high and low elevation areas that remain valuable repositories of genetic diversity and provide a case study for other low-dispersal coastal organisms in the face of future climate change.

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          Most cited references18

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          Detection of reduction in population size using data from microsatellite loci.

          We demonstrate that the mean ratio of the number of alleles to the range in allele size, which we term M, calculated from a population sample of microsatellite loci, can be used to detect reductions in population size. Using simulations, we show that, for a general class of mutation models, the value of M decreases when a population is reduced in size. The magnitude of the decrease is positively correlated with the severity and duration of the reduction in size. We also find that the rate of recovery of M following a reduction in size is positively correlated with post-reduction population size, but that recovery occurs in both small and large populations. This indicates that M can distinguish between populations that have been recently reduced in size and those which have been small for a long time. We employ M to develop a statistical test for recent reductions in population size that can detect such changes for more than 100 generations with the post-reduction demographic scenarios we examine. We also compute M for a variety of populations and species using microsatellite data collected from the literature. We find that the value of M consistently predicts the reported demographic history for these populations. This method, and others like it, promises to be an important tool for the conservation and management of populations that are in need of intervention or recovery.
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            Estimate of the mutation rate per nucleotide in humans.

            Many previous estimates of the mutation rate in humans have relied on screens of visible mutants. We investigated the rate and pattern of mutations at the nucleotide level by comparing pseudogenes in humans and chimpanzees to (i) provide an estimate of the average mutation rate per nucleotide, (ii) assess heterogeneity of mutation rate at different sites and for different types of mutations, (iii) test the hypothesis that the X chromosome has a lower mutation rate than autosomes, and (iv) estimate the deleterious mutation rate. Eighteen processed pseudogenes were sequenced, including 12 on autosomes and 6 on the X chromosome. The average mutation rate was estimated to be approximately 2.5 x 10(-8) mutations per nucleotide site or 175 mutations per diploid genome per generation. Rates of mutation for both transitions and transversions at CpG dinucleotides are one order of magnitude higher than mutation rates at other sites. Single nucleotide substitutions are 10 times more frequent than length mutations. Comparison of rates of evolution for X-linked and autosomal pseudogenes suggests that the male mutation rate is 4 times the female mutation rate, but provides no evidence for a reduction in mutation rate that is specific to the X chromosome. Using conservative calculations of the proportion of the genome subject to purifying selection, we estimate that the genomic deleterious mutation rate (U) is at least 3. This high rate is difficult to reconcile with multiplicative fitness effects of individual mutations and suggests that synergistic epistasis among harmful mutations may be common.
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              Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow.

              Many species have fragmented distribution with small isolated populations suffering inbreeding depression and/or reduced ability to evolve. Without gene flow from another population within the species (genetic rescue), these populations are likely to be extirpated. However, there have been only ~ 20 published cases of such outcrossing for conservation purposes, probably a very low proportion of populations that would potentially benefit. As one impediment to genetic rescues is the lack of an overview of the magnitude and consistency of genetic rescue effects in wild species, I carried out a meta-analysis. Outcrossing of inbred populations resulted in beneficial effects in 92.9% of 156 cases screened as having a low risk of outbreeding depression. The median increase in composite fitness (combined fecundity and survival) following outcrossing was 148% in stressful environments and 45% in benign ones. Fitness benefits also increased significantly with maternal ΔF (reduction in inbreeding coefficient due to gene flow) and for naturally outbreeding versus inbreeding species. However, benefits did not differ significantly among invertebrates, vertebrates and plants. Evolutionary potential for fitness characters in inbred populations also benefited from gene flow. There are no scientific impediments to the widespread use of outcrossing to genetically rescue inbred populations of naturally outbreeding species, provided potential crosses have a low risk of outbreeding depression. I provide revised guidelines for the management of genetic rescue attempts.
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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, CA USA )
                1932-6203
                9 November 2016
                2016
                : 11
                : 11
                : e0163738
                Affiliations
                [1 ]Department of Ecology and Evolutionary Biology, University of Michigan, 1109 Geddes Ave, Ann Arbor, MI, 48103, United States of America
                [2 ]Department of Biology, University of Hawaii at Hilo, Hilo, HI, 96720, United States of America
                [3 ]Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 1156 High St., Santa Cruz, CA, 95064, United States of America
                University of Regina, CANADA
                Author notes

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

                • Conceptualization: ARDR WJM.

                • Data curation: ARDR IAH.

                • Formal analysis: IAH ARDR.

                • Funding acquisition: ARDR WJM.

                • Investigation: ARDR WJM IAH.

                • Methodology: IAH ARDR WJM.

                • Project administration: ARDR.

                • Resources: WJM ARDR.

                • Supervision: ARDR.

                • Visualization: IAH ARDR.

                • Writing – original draft: IAH ARDR.

                • Writing – review & editing: IAH ARDR WJM.

                Author information
                http://orcid.org/0000-0001-6150-6150
                Article
                PONE-D-16-09070
                10.1371/journal.pone.0163738
                5102444
                27828958
                beeab984-e3a9-4c99-86ba-7ebf18fe9e4e
                © 2016 Holmes et al

                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
                : 2 March 2016
                : 13 September 2016
                Page count
                Figures: 2, Tables: 1, Pages: 18
                Funding
                Funded by: STEPS Institute for Innovation in Environmental Research
                Award ID: Davis2012
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100007270, University of Michigan;
                Award ID: Davis2014
                Award Recipient :
                Funding for molecular work was provided by the STEPS Institute for Innovation in Environmental Research at the University of California ( http://www1.ucsc.edu/currents/01-02/04-08/institute.html, Davis2012) Santa Cruz and by start-up funds from the University of Michigan to ARDR ( https://www.lsa.umich.edu/eeb/, Davis2014).
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                Evolutionary Biology
                Population Genetics
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                Genetics
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                Custom metadata
                All sequences have been submitted to GenBank, accession numbers KT696132-KT696166. Microsatellite genotypes are available on Dryad, with DOI doi: 10.5061/dryad.6c7p5.

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