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S12711-018-0421-Y.Pdf Bertolini et al. Genet Sel Evol (2018) 50:57 https://doi.org/10.1186/s12711-018-0421-y Genetics Selection Evolution RESEARCH ARTICLE Open Access Signatures of selection and environmental adaptation across the goat genome post‑domestication Francesca Bertolini1,2* , Bertrand Servin3, Andrea Talenti4, Estelle Rochat5, Eui Soo Kim6, Claire Oget3, Isabelle Palhière3, Alessandra Crisà7, Gennaro Catillo7, Roberto Steri7, Marcel Amills8, Licia Colli9,10, Gabriele Marras11, Marco Milanesi9,12, Ezequiel Nicolazzi11, Benjamin D. Rosen13, Curtis P. Van Tassell13, Bernt Guldbrandtsen14, Tad S. Sonstegard6, Gwenola Tosser‑Klopp3, Alessandra Stella10, Max F. Rothschild1, Stéphane Joost5, Paola Crepaldi4 and the AdaptMap consortium Abstract Background: Since goat was domesticated 10,000 years ago, many factors have contributed to the diferentiation of goat breeds and these are classifed mainly into two types: (i) adaptation to diferent breeding systems and/or purposes and (ii) adaptation to diferent environments. As a result, approximately 600 goat breeds have developed worldwide; they difer considerably from one another in terms of phenotypic characteristics and are adapted to a wide range of climatic conditions. In this work, we analyzed the AdaptMap goat dataset, which is composed of data from more than 3000 animals collected worldwide and genotyped with the CaprineSNP50 BeadChip. These animals were partitioned into groups based on geographical area, production uses, available records on solid coat color and environmental variables including the sampling geographical coordinates, to investigate the role of natural and/or artifcial selection in shaping the genome of goat breeds. Results: Several signatures of selection on diferent chromosomal regions were detected across the diferent breeds, sub-geographical clusters, phenotypic and climatic groups. These regions contain genes that are involved in impor‑ tant biological processes, such as milk-, meat- or fber-related production, coat color, glucose pathway, oxidative stress response, size, and circadian clock diferences. Our results confrm previous fndings in other species on adaptation to extreme environments and human purposes and provide new genes that could explain some of the diferences between goat breeds according to their geographical distribution and adaptation to diferent environments. Conclusions: These analyses of signatures of selection provide a comprehensive frst picture of the global domesti‑ cation process and adaptation of goat breeds and highlight possible genes that may have contributed to the diferen‑ tiation of this species worldwide. *Correspondence: [email protected]; [email protected] 1 Department of Animal Science, Iowa State University, Ames, IA 50011, USA Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/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://creat​iveco​mmons​.org/ publi​cdoma​in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Bertolini et al. Genet Sel Evol (2018) 50:57 Page 2 of 24 Background genetic diversity, including signatures left by selection Te goat (Capra hircus) is considered one of the earli- processes [7]. est domesticated livestock species. Te domestication In spite of the major economic importance of goats, process started around 10,000 years ago in the Fertile high-throughput genomic resources for this species Crescent area from a unique wild and still living ances- have become available only recently. In 2011, the Inter- tor, the bezoar or Capra aegagrus [1]. At present, there national Goat Genome Consortium developed and are more than one billion of goats that inhabit all types released the frst high-throughput SNP chip with more of ecological areas across the globe [2]. Compared with than 50,000 SNPs (Illumina CaprineSNP50 BeadChip), the other major livestock species such as pigs, cattle which was built using 10 biologically and geographi- and sheep, goats have undergone the largest increase cally diferent breeds [8]. Te frst complete assembly (+34%) in population since 2000, i.e. larger than pigs of the goat genome was released in 2013 by Dong et al. (+15%), cattle (+14%) and sheep (+14%) (http://www. [9] and a second version of the reference genome that fao.org/faost at/en/). Today, over 90% of the goats are exploits single-molecule long read sequencing (PacBio) distributed across Asia and Africa, followed by the has just been released (ARS1; [10]). With this new ver- Americas, Europe, and Oceania [3]. In the most rural sion, gene annotation has improved considerably and the areas of the world, goats are often considered the poor position of the SNPs on the CaprineSNP50 BeadChip has person’s cow. In fact, goats can be used for milk, meat, been updated. With the availability of genomic and high- fber, and leather production [4], as well as transport. throughput SNP tools, there is an increased interest in Moreover, they are easy to house and manage; goats can identifying and exploring signatures of selection and the be raised by small families, women, and children and genomic diversity resulting from adaptation to environ- provide a fundamental source of food for millions of ment and human selective pressure. Tese genomic tools people. Several factors have contributed to the diferen- were used to identify signatures of selection in circum- tiation of goat breeds, which are classifed mainly into scribed datasets. Te CaprineSNP50 BeadChip was used two types: (i) adaptation to diferent breeding systems to investigate and compare several Swiss goat breeds and and/or purposes, i.e. in some countries, breeds have genomic signatures of selection were detected in regions been selected for specifc production traits such as milk that afect variation in coat color, growth, and milk com- (e.g. Saanen and Alpine), meat (e.g. Landrace and Boer) position [11]. Te combination of analyses of runs of and fber (e.g. Angora and Cashmere); and (ii) adapta- homozygosity (ROH), FST (fxation index), XP-EHH tion to diferent environments, i.e. goats have adapted (cross population extended haplotype homozygosity), to various agro-climatic conditions. In addition, goat and the use of Bayesian methods allowed the detection breeds have undergone diferentiation through founder of signatures of selection in a region that contains genes efects, and the processes of admixture and genetic related to the immune system in another mountain breed drift. Tus, about 600 breeds have been developed and raised in the North of Italy, the Valdostana Italian goat are distributed worldwide [5]. Tey difer from one breed [12]. Other analyses of signatures of selection were another in terms of many phenotypic characteristics performed in a reduced number of breeds, thus detecting such as size, color, horn shape and dimension, repro- regions that are linked to production and reproduction ductive and productive traits and are adapted to a wide traits [13] and in the Barki Egyptian goat breed, which is range of bioclimatic conditions. Directional natural and raised and adapted to hot/dry environments [14]. In the artifcial selection events have left footprints across latter study, analyses of iHS (integrated haplotype score) the genome, which are known as signatures of selec- and pairwise FST that identifed selective sweeps led to tion. Signatures of selection are defned as the reduc- the identifcation of genes related to thermotolerance, tion, elimination or change of genetic variation in body size, energy metabolism and nervous and auto- genomic regions that are adjacent to causative variants immune response [14]. Furthermore, signatures of selec- in response to natural or artifcial selective pressure. tion that were linked to dry and hot conditions and to Such variants usually afect several traits and contrib- metabolic traits were identifed by using whole-genome ute to shaping a breed [6]. Te process by which the sequence (WGS) data from Moroccan goat breeds frequency of a selectively favored variant increases in through XP-CLR analysis [15]. WGS information was a population is termed a selective sweep. Te recent also successfully used to detect regions that are under development of species-specifc genomic tools (such diferent selection pressures in Chinese and Mongolian as single nucleotide polymorphism (SNP) arrays) have goats and are related to breeding or reproductive traits allowed researchers to extend whole-genome analy- [16, 17]. ses to livestock species, which cover many aspects of Genomic changes that result from climate changes and are linked to adaptation to diferent environments can be Bertolini et al. Genet Sel Evol (2018) 50:57 Page 3 of 24 analyzed with a landscape genomic approach, which was software [24] and the most recent version of the goat successfully applied in other livestock species, for exam- genome assembly (ARS1; [10]). ple in Ugandan cattle [18]. To date in goats, this approach was applied only on a reduced number of SNPs or ampli- Signatures of selection based on genetic diversity fed fragment length polymorphism (AFLP) markers [19, of subcontinental populations
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