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      A Quasi-Exclusive European Ancestry in the Senepol Tropical Cattle Breed Highlights the Importance of the slick Locus in Tropical Adaptation

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          Abstract

          Background

          The Senepol cattle breed (SEN) was created in the early XX th century from a presumed cross between a European (EUT) breed (Red Poll) and a West African taurine (AFT) breed (N’Dama). Well adapted to tropical conditions, it is also believed trypanotolerant according to its putative AFT ancestry. However, such origins needed to be verified to define relevant husbandry practices and the genetic background underlying such adaptation needed to be characterized.

          Methodology/Principal Findings

          We genotyped 153 SEN individuals on 47,365 SNPs and combined the resulting data with those available on 18 other populations representative of EUT, AFT and Zebu (ZEB) cattle. We found on average 89% EUT, 10.4% ZEB and 0.6% AFT ancestries in the SEN genome. We further looked for footprints of recent selection using standard tests based on the extent of haplotype homozygosity. We underlined i) three footprints on chromosome (BTA) 01, two of which are within or close to the polled locus underlying the absence of horns and ii) one footprint on BTA20 within the slick hair coat locus, involved in thermotolerance. Annotation of these regions allowed us to propose three candidate genes to explain the observed signals (TIAM1, GRIK1 and RAI14).

          Conclusions/Significance

          Our results do not support the accepted concept about the AFT origin of SEN breed. Initial AFT ancestry (if any) might have been counter-selected in early generations due to breeding objectives oriented in particular toward meat production and hornless phenotype. Therefore, SEN animals are likely susceptible to African trypanosomes which questions the importation of SEN within the West African tsetse belt, as promoted by some breeding societies. Besides, our results revealed that SEN breed is predominantly a EUT breed well adapted to tropical conditions and confirmed the importance in thermotolerance of the slick locus.

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          Most cited references53

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          A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase.

          Paul Scheet, Matthew Stephens (2006)
          We present a statistical model for patterns of genetic variation in samples of unrelated individuals from natural populations. This model is based on the idea that, over short regions, haplotypes in a population tend to cluster into groups of similar haplotypes. To capture the fact that, because of recombination, this clustering tends to be local in nature, our model allows cluster memberships to change continuously along the chromosome according to a hidden Markov model. This approach is flexible, allowing for both "block-like" patterns of linkage disequilibrium (LD) and gradual decline in LD with distance. The resulting model is also fast and, as a result, is practicable for large data sets (e.g., thousands of individuals typed at hundreds of thousands of markers). We illustrate the utility of the model by applying it to dense single-nucleotide-polymorphism genotype data for the tasks of imputing missing genotypes and estimating haplotypic phase. For imputing missing genotypes, methods based on this model are as accurate or more accurate than existing methods. For haplotype estimation, the point estimates are slightly less accurate than those from the best existing methods (e.g., for unrelated Centre d'Etude du Polymorphisme Humain individuals from the HapMap project, switch error was 0.055 for our method vs. 0.051 for PHASE) but require a small fraction of the computational cost. In addition, we demonstrate that the model accurately reflects uncertainty in its estimates, in that probabilities computed using the model are approximately well calibrated. The methods described in this article are implemented in a software package, fastPHASE, which is available from the Stephens Lab Web site.
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            A note on exact tests of Hardy-Weinberg equilibrium.

            Janis E Wigginton, David Cutler, Gonçalo R Abecasis (2005)
            Deviations from Hardy-Weinberg equilibrium (HWE) can indicate inbreeding, population stratification, and even problems in genotyping. In samples of affected individuals, these deviations can also provide evidence for association. Tests of HWE are commonly performed using a simple chi2 goodness-of-fit test. We show that this chi2 test can have inflated type I error rates, even in relatively large samples (e.g., samples of 1,000 individuals that include approximately 100 copies of the minor allele). On the basis of previous work, we describe exact tests of HWE together with efficient computational methods for their implementation. Our methods adequately control type I error in large and small samples and are computationally efficient. They have been implemented in freely available code that will be useful for quality assessment of genotype data and for the detection of genetic association or population stratification in very large data sets.
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              Development and Characterization of a High Density SNP Genotyping Assay for Cattle

              Lakshmi Matukumalli, Cynthia Lawley, Robert Schnabel … (2009)
              The success of genome-wide association (GWA) studies for the detection of sequence variation affecting complex traits in human has spurred interest in the use of large-scale high-density single nucleotide polymorphism (SNP) genotyping for the identification of quantitative trait loci (QTL) and for marker-assisted selection in model and agricultural species. A cost-effective and efficient approach for the development of a custom genotyping assay interrogating 54,001 SNP loci to support GWA applications in cattle is described. A novel algorithm for achieving a compressed inter-marker interval distribution proved remarkably successful, with median interval of 37 kb and maximum predicted gap of <350 kb. The assay was tested on a panel of 576 animals from 21 cattle breeds and six outgroup species and revealed that from 39,765 to 46,492 SNP are polymorphic within individual breeds (average minor allele frequency (MAF) ranging from 0.24 to 0.27). The assay also identified 79 putative copy number variants in cattle. Utility for GWA was demonstrated by localizing known variation for coat color and the presence/absence of horns to their correct genomic locations. The combination of SNP selection and the novel spacing algorithm allows an efficient approach for the development of high-density genotyping platforms in species having full or even moderate quality draft sequence. Aspects of the approach can be exploited in species which lack an available genome sequence. The BovineSNP50 assay described here is commercially available from Illumina and provides a robust platform for mapping disease genes and QTL in cattle.
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                Author and article information

                Contributors
                : Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2012
                Publication date (Electronic): 9 May 2012
                Publication date (Corrected, electronic): 15 May 2012
                Volume: 7
                Issue: 5
                Electronic Location Identifier: e36133
                Affiliations
                [1 ]INRA, UMR 1313 GABI, F-78350 Jouy-en-Josas, France
                [2 ]CIRAD, UMR INTERTRYP, Montpellier, France
                [3 ]Departamento de Biología Celular, Universidad Simón Bolívar, Caracas, Venezuela
                [4 ]INRA, UMR CBGP, Montferrier-sur-Lez, France
                University of Florence, Italy
                Author notes

                Conceived and designed the experiments: MG LF PMA. Performed the experiments: MIG PMA LF ST DB IC JP. Analyzed the data: LF MG. Wrote the paper: LF MG.

                Article
                Publisher ID: PONE-D-12-02815
                DOI: 10.1371/journal.pone.0036133
                PMC ID: 3366548
                PubMed ID: 22675421
                SO-VID: bb24d430-d12b-4c66-a4c8-e66cbc5db66c
                Copyright © Flori 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
                Date received : 22 January 2012
                Date accepted : 26 March 2012
                Page count
                Pages: 10
                Categories
                Subject: Research Article
                Subject: Biology
                Subject: Evolutionary Biology
                Subject: Evolutionary Genetics
                Subject: Genetics
                Subject: Heredity
                Subject: Genotypes
                Subject: Population Genetics
                Subject: Haplotypes
                Subject: Natural Selection
                Subject: Animal Genetics
                Subject: Genomics
                Subject: Genome Analysis Tools
                Subject: Genome Scans
                Subject: Population Biology
                Subject: Population Genetics
                Subject: Genetic Polymorphism
                Subject: Haplotypes
                Subject: Natural Selection

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