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      Genome-wide estimates of genetic diversity, inbreeding and effective size of experimental and commercial rainbow trout lines undergoing selective breeding

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          Abstract

          Background

          Selective breeding is a relatively recent practice in aquaculture species compared to terrestrial livestock. Nevertheless, the genetic variability of farmed salmonid lines, which have been selected for several generations, should be assessed. Indeed, a significant decrease in genetic variability due to high selection intensity could have occurred, potentially jeopardizing the long-term genetic progress as well as the adaptive capacities of populations facing change(s) in the environment. Thus, it is important to evaluate the impact of selection practices on genetic diversity to limit future inbreeding. The current study presents an analysis of genetic diversity within and between six French rainbow trout ( Oncorhynchus mykiss) experimental or commercial lines based on a medium-density single nucleotide polymorphism (SNP) chip and various molecular genetic indicators: fixation index ( F ST), linkage disequilibrium (LD), effective population size ( N e ) and inbreeding coefficient derived from runs of homozygosity (ROH).

          Results

          Our results showed a moderate level of genetic differentiation between selected lines ( F ST ranging from 0.08 to 0.15). LD declined rapidly over the first 100 kb, but then remained quite high at long distances, leading to low estimates of N e in the last generation ranging from 24 to 68 depending on the line and methodology considered. These results were consistent with inbreeding estimates that varied from 10.0% in an unselected experimental line to 19.5% in a commercial line, and which are clearly higher than corresponding estimates in ruminants or pigs. In addition, strong variations in LD and inbreeding were observed along the genome that may be due to differences in local rates of recombination or due to key genes that tended to have fixed favorable alleles for domestication or production.

          Conclusions

          This is the first report on ROH for any aquaculture species. Inbreeding appeared to be moderate to high in the six French rainbow trout lines, due to founder effects at the start of the breeding programs, but also likely to sweepstakes reproductive success in addition to selection for the selected lines. Efficient management of inbreeding is a major goal in breeding programs to ensure that populations can adapt to future breeding objectives and SNP information can be used to manage the rate at which inbreeding builds up in the fish genome.

          Electronic supplementary material

          The online version of this article (10.1186/s12711-019-0468-4) contains supplementary material, which is available to authorized users.

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          The hitch-hiking effect of a favourable gene

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            The effect of deleterious mutations on neutral molecular variation.

            Selection against deleterious alleles maintained by mutation may cause a reduction in the amount of genetic variability at linked neutral sites. This is because a new neutral variant can only remain in a large population for a long period of time if it is maintained in gametes that are free of deleterious alleles, and hence are not destined for rapid elimination from the population by selection. Approximate formulas are derived for the reduction below classical neutral values resulting from such background selection against deleterious mutations, for the mean times to fixation and loss of new mutations, nucleotide site diversity, and number of segregating sites. These formulas apply to random-mating populations with no genetic recombination, and to populations reproducing exclusively asexually or by self-fertilization. For a given selection regime and mating system, the reduction is an exponential function of the total mutation rate to deleterious mutations for the section of the genome involved. Simulations show that the effect decreases rapidly with increasing recombination frequency or rate of outcrossing. The mean time to loss of new neutral mutations and the total number of segregating neutral sites are less sensitive to background selection than the other statistics, unless the population size is of the order of a hundred thousand or more. The stationary distribution of allele frequencies at the neutral sites is correspondingly skewed in favor of rare alleles, compared with the classical neutral result. Observed reductions in molecular variation in low recombination genomic regions of sufficiently large size, for instance in the centromere-proximal regions of Drosophila autosomes or in highly selfing plant populations, may be partly due to background selection against deleterious mutations.
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              Estimation of effective population size from data on linkage disequilibrium

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                Author and article information

                Contributors
                jonathan.d'ambrosio@inra.fr
                florence.phocas@inra.fr
                pierrick.haffray@inra.fr
                anastasia.bestin@inra.fr
                sophie.brard-fudulea@inra.fr
                charles.poncet@inra.fr
                edwige.quillet@inra.fr
                nicolas.dechamp@inra.fr
                clemence.fraslin@inra.fr
                mathieu.charles@inra.fr
                mathilde.dupont-nivet@inra.fr
                Journal
                Genet Sel Evol
                Genet. Sel. Evol
                Genetics, Selection, Evolution : GSE
                BioMed Central (London )
                0999-193X
                1297-9686
                6 June 2019
                6 June 2019
                2019
                : 51
                : 26
                Affiliations
                [1 ]GRID grid.417961.c, GABI, INRA, AgroParisTech, Université Paris-Saclay, ; 78350 Jouy-en-Josas, France
                [2 ]SYSAAF Section Aquacole, Campus de Beaulieu, 35000 Rennes, France
                [3 ]SYSAAF Section Avicole, Centre INRA Val de Loire, 37380 Nouzilly, France
                [4 ]ISNI 0000 0004 0613 5360, GRID grid.503180.f, GDEC, INRA, Université Clermont-Auvergne, ; 63039 Clermont-Ferrand, France
                Author information
                http://orcid.org/0000-0003-1161-3665
                Article
                468
                10.1186/s12711-019-0468-4
                6554922
                31170906
                bf0f839b-d8f0-4716-8fc4-1ac49bf361c2
                © The Author(s) 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 1 October 2018
                : 22 May 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003199, France AgriMer;
                Award ID: 2015-0638
                Award ID: 2017-0239
                Award Recipient :
                Funded by: European Maritime and Fisheries Fund
                Award ID: RFEA47 0016 FA 1000016
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Genetics
                Genetics

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