Signatures of Selection and Interspecies Introgression in the Genome of Chinese Domestic Pigs.
ABSTRACT: Chinese domestic pigs have experienced strong artificial selection for thousands of years. However, the molecular mechanisms underlying the selection-causing phenotypic changes in Chinese domestic pigs are still largely unknown. Here we used whole-genome resequencing data of 54 pigs from 9 Chinese diverse breeds and 16 wild boars from 7 localities across China to identify genes that show evidence of positive selection in the process of domestication. A total of 14 candidate domestication regions were detected by selective sweep analyses of genetic differentiation and variability, and a set of genes in these candidate domestication regions were found to be related to metabolic process, development, reproduction, olfactory, behavior, and nervous system. The most promising candidate gene under selection - TBX19 - probably underlies the metabolic alteration and developmental traits, and may also associate with timidity of Chinese domestic pigs. Intriguingly, we found that the haplotype at TBX19 locus shared by nearly all Chinese domestic pigs was possibly introgressed from another Sus species. We also revealed the AHR gene associated with female reproduction is under strong positive selection. These results advance our understanding of the evolutionary history of Chinese domestic pigs and shed insights into identifying functionally important genes/mutations contributing to the phenotypic diversity in pigs.
Project description:Since 10,000 BC, continuous human selection has led to intense genetic and phenotypic changes in pig (Sus scrofa) domestication. Through whole genome analysis of 257 individuals, we demonstrated artificial unidirectional and bidirectional selection as the primary force to shape the convergent and divergent changes between Chinese domestic pigs (CHD) and European domestic pigs (EUD). We identified 31 genes in unidirectional selection regions that might be related to fundamental domestication requirements in pigs. And these genes belong predominantly to categories related to the nervous system, muscle development, and especially to metabolic diseases. In addition, 35 genes, representing different breeding preference, were found under bidirectional selection for the distinct leanness and reproduction traits between CHD and EUD. The convergent genetic changes, contributing physical and morphological adaption, represent the common concerns on pig domestication. And the divergent genetic changes reflect distinct breeding goals between Chinese and European pigs. Using ITPR3, AHR and NMU as examples, we explored and validated how the genetic variations contribute to the phenotype changes.
Project description:Domestication of wild boar (Sus scrofa) and subsequent selection have resulted in dramatic phenotypic changes in domestic pigs for a number of traits, including behavior, body composition, reproduction, and coat color. Here we have used whole-genome resequencing to reveal some of the loci that underlie phenotypic evolution in European domestic pigs. Selective sweep analyses revealed strong signatures of selection at three loci harboring quantitative trait loci that explain a considerable part of one of the most characteristic morphological changes in the domestic pig--the elongation of the back and an increased number of vertebrae. The three loci were associated with the NR6A1, PLAG1, and LCORL genes. The latter two have repeatedly been associated with loci controlling stature in other domestic animals and in humans. Most European domestic pigs are homozygous for the same haplotype at these three loci. We found an excess of derived nonsynonymous substitutions in domestic pigs, most likely reflecting both positive selection and relaxed purifying selection after domestication. Our analysis of structural variation revealed four duplications at the KIT locus that were exclusively present in white or white-spotted pigs, carrying the Dominant white, Patch, or Belt alleles. This discovery illustrates how structural changes have contributed to rapid phenotypic evolution in domestic animals and how alleles in domestic animals may evolve by the accumulation of multiple causative mutations as a response to strong directional selection.
Project description:Copy number variations (CNVs) refer to large insertions, deletions and duplications in the genomic structure ranging from one thousand to several million bases in size. Since the development of next generation sequencing technology, several methods have been well built for detection of copy number variations with high credibility and accuracy. Evidence has shown that CNV occurring in gene region could lead to phenotypic changes due to the alteration in gene structure and dosage. However, it still remains unexplored whether CNVs underlie the phenotypic differences between Chinese and Western domestic pigs. Based on the read-depth methods, we investigated copy number variations using 49 individuals derived from both Chinese and Western pig breeds. A total of 3,131 copy number variation regions (CNVRs) were identified with an average size of 13.4 Kb in all individuals during domestication, harboring 1,363 genes. Among them, 129 and 147 CNVRs were Chinese and Western pig specific, respectively. Gene functional enrichments revealed that these CNVRs contribute to strong disease resistance and high prolificacy in Chinese domestic pigs, but strong muscle tissue development in Western domestic pigs. This finding is strongly consistent with the morphologic characteristics of Chinese and Western pigs, indicating that these group-specific CNVRs might have been preserved by artificial selection for the favored phenotypes during independent domestication of Chinese and Western pigs. In this study, we built high-resolution CNV maps in several domestic pig breeds and discovered the group specific CNVs by comparing Chinese and Western pigs, which could provide new insight into genomic variations during pigs' independent domestication, and facilitate further functional studies of CNV-associated genes.
Project description:Identification of genomic signatures that help reveal mechanisms underlying desirable traits in domesticated pigs is of significant biological, agricultural and medical importance. To identify the genomic footprints left by selection during domestication of the Enshi black pig, a typical native and meat-lard breed in China, we generated about 72-fold coverage of the pig genome using pools of genomic DNA representing three different populations of Enshi black pigs from three different locations. Combining this data with the available whole genomes of 13 Chinese wild boars, we identified 417 protein-coding genes embedded in the selected regions of Enshi black pigs. These genes are mainly involved in developmental and metabolic processes, response to stimulus, and other biological processes. Signatures of selection were detected in genes involved in body size and immunity (RPS10 and VASN), lipid metabolism (GSK3), male fertility (INSL6) and developmental processes (TBX19). These findings provide a window into the potential genetic mechanism underlying development of desirable phenotypes in Enshi black pigs during domestication and subsequent artificial selection. Thus, our results illustrate how domestication has shaped patterns of genetic variation in Enshi black pigs and provide valuable genetic resources that enable effective use of pigs in agricultural production.
Project description:Pigs were domesticated independently in Eastern and Western Eurasia early during the agricultural revolution, and have since been transported and traded across the globe. Here, we present a worldwide survey on 60K genome-wide single nucleotide polymorphism (SNP) data for 2093 pigs, including 1839 domestic pigs representing 122 local and commercial breeds, 215 wild boars, and 39 out-group suids, from Asia, Europe, America, Oceania and Africa. The aim of this study was to infer global patterns in pig domestication and diversity related to demography, migration, and selection.A deep phylogeographic division reflects the dichotomy between early domestication centers. In the core Eastern and Western domestication regions, Chinese pigs show differentiation between breeds due to geographic isolation, whereas this is less pronounced in European pigs. The inferred European origin of pigs in the Americas, Africa, and Australia reflects European expansion during the sixteenth to nineteenth centuries. Human-mediated introgression, which is due, in particular, to importing Chinese pigs into the UK during the eighteenth and nineteenth centuries, played an important role in the formation of modern pig breeds. Inbreeding levels vary markedly between populations, from almost no runs of homozygosity (ROH) in a number of Asian wild boar populations, to up to 20% of the genome covered by ROH in a number of Southern European breeds. Commercial populations show moderate ROH statistics. For domesticated pigs and wild boars in Asia and Europe, we identified highly differentiated loci that include candidate genes related to muscle and body development, central nervous system, reproduction, and energy balance, which are putatively under artificial selection.Key events related to domestication, dispersal, and mixing of pigs from different regions are reflected in the 60K SNP data, including the globalization that has recently become full circle since Chinese pig breeders in the past decades started selecting Western breeds to improve local Chinese pigs. Furthermore, signatures of ongoing and past selection, acting at different times and on different genetic backgrounds, enhance our insight in the mechanism of domestication and selection. The global diversity statistics presented here highlight concerns for maintaining agrodiversity, but also provide a necessary framework for directing genetic conservation.
Project description:Animal domestication involved drastic phenotypic changes driven by strong artificial selection and also resulted in new populations of breeds, established by humans. This study aims to identify genes that show evidence of recent artificial selection during pig domestication.Whole-genome resequencing of 30 individual pigs from domesticated breeds, Landrace and Yorkshire, and 10 Asian wild boars at ~16-fold coverage was performed resulting in over 4.3 million SNPs for 19,990 genes. We constructed a comprehensive genome map of directional selection by detecting selective sweeps using an F ST-based approach that detects directional selection in lineages leading to the domesticated breeds and using a haplotype-based test that detects ongoing selective sweeps within the breeds. We show that candidate genes under selection are significantly enriched for loci implicated in quantitative traits important to pig reproduction and production. The candidate gene with the strongest signals of directional selection belongs to group III of the metabolomics glutamate receptors, known to affect brain functions associated with eating behavior, suggesting that loci under strong selection include loci involved in behaviorial traits in domesticated pigs including tameness.We show that a significant proportion of selection signatures coincide with loci that were previously inferred to affect phenotypic variation in pigs. We further identify functional enrichment related to behavior, such as signal transduction and neuronal activities, for those targets of selection during domestication in pigs.
Project description:The domestic pigs have been undergone intense selection pressures for these development of interested traits following domestication and modern breeding. This has altered many traits in most of pig breeds, such as growth rate, body weight, fertility, and immunity. Thus, the objectives of this study were to (1) detect these selection signatures and identify the candidate genes that show evidences of recent artificial selection at the level of whole genome, (2) be beneficial to understand the relationship between genomic structure and phenotypic diversity, and (3) highlight the key roles of these candidate genes in growth and development in the two breeds. The data consisted of total raw number of 345570 single nucleotide polymorphisms (SNPs) in 1200 individuals from the Chinese Landrace pigs (L, n = 600) and Yorkshire pigs (Y, n = 600). Based on these SNPs data, two complementary methods, population differentiation (Fst) and composite likelihood ratio test (CLR), were carried out to detect the selection signatures in this study. A total of 540 potential selection regions (50 kb) which contained 111 candidate genes were detected for Landrace-Yorkshire pair (L-Y) by Fst. In addition, 73 and 125 candidate genes were found for Landrace pigs and Yorkshire pigs by CLR test based on 321 and 628 potential selection regions, respectively. Some candidate genes are associated with important traits and signaling pathways including the ACACA, MECR, COL11A1, GHR, IGF1R, IGF2R, IFNG, and MTOR gene. The ACACA and MECR gene are related to fatty acid biosynthesis. The COL11A1 gene is essential for the development of the normal differentiation. The GHR, IGF1R, and IGF2R gene are significant candidate genes which play major roles in the growth and development in animals. The IFNG gene is associated with some aspects of immune response. The MTOR gene regulates many signaling pathways and signaling transduction pathway.
Project description:BACKGROUND:Identification of selection signatures can provide a direct insight into the mechanism of artificial selection and allow further disclosure of the candidate genes related to the animals' phenotypic variation. Domestication and subsequent long-time selection have resulted in extensive phenotypic changes in domestic pigs, involving a number of traits, like behavior, body composition, disease resistance, reproduction and coat color. In this study, based on genotypes obtained from PorcineSNP60 Illumina assay we attempt to detect both diversifying and within-breed selection signatures in 530 pigs belonging to four breeds: Polish Landrace, Pu?awska, Z?otnicka White and Z?otnicka Spotted, of which the last three are a subject of conservative breeding and substantially represent the native populations. RESULTS:A two largely complementary statistical methods were used for signatures detection, including: pairwise FST and relative extended haplotype homozygosity (REHH) test. Breed-specific diversifying selection signals included several genes involved in processes connected with fertility, growth and metabolism which are potentially responsible for different phenotypes of the studied breeds. The diversifying selection signals also comprised PPARD gene that was previously found to have a large effect on the shape of the external ear in pigs or two genes encoding neuropeptide Y receptors (Y2 and Y5) involved in fat deposition and stress response which are important features differentiating the studied breeds. REHH statistics allowed detecting several within-breed selection signatures overlapping with genes connected with a range of functions including, among others: metabolic pathways, immune system response or implantation and development of the embryo. CONCLUSIONS:The study provides many potential candidate genes with implication for traits selected in the individual breeds and gives strong basis for further studies aiming at identification of sources of variation among the studied pig breeds.
Project description:Pigs have experienced long-term selections, resulting in dramatic phenotypic changes. Structural variants (SVs) are reported to exert extensive impacts on phenotypic changes. We built a high resolution and informative SV map based on high-depth sequencing data from 66 Chinese domestic and wild pigs. We inferred the SV formation mechanisms in the pig genome and used SVs as materials to perform a population-level analysis. We detected the selection signals on chromosome X for northern Chinese domestic pigs, as well as the differentiated loci across the whole genome. Analysis showed that these loci differ between southern and northern Chinese domestic pigs. Our results based on SVs provide new insights into genetic differences in Chinese pigs.
Project description:Copy number variable regions (CNVRs) can result in drastic phenotypic differences and may therefore be subject to selection during domestication. Studying copy number variation in relation to domestication is highly relevant in pigs because of their very rich natural and domestication history that resulted in many different phenotypes. To investigate the evolutionary dynamic of CNVRs, we applied read depth method on next generation sequence data from 16 individuals, comprising wild boars and domestic pigs from Europe and Asia.We identified 3,118 CNVRs with an average size of 13 kilobases comprising a total of 39.2 megabases of the pig genome and 545 overlapping genes. Functional analyses revealed that CNVRs are enriched with genes related to sensory perception, neurological process and response to stimulus, suggesting their contribution to adaptation in the wild and behavioral changes during domestication. Variations of copy number (CN) of antimicrobial related genes suggest an ongoing process of evolution of these genes to combat food-borne pathogens. Likewise, some genes related to the omnivorous lifestyle of pigs, like genes involved in detoxification, were observed to be CN variable. A small portion of CNVRs was unique to domestic pigs and may have been selected during domestication. The majority of CNVRs, however, is shared between wild and domesticated individuals, indicating that domestication had minor effect on the overall diversity of CNVRs. Also, the excess of CNVRs in non-genic regions implies that a major part of these variations is likely to be (nearly) neutral. Comparison between different populations showed that larger populations have more CNVRs, highlighting that CNVRs are, like other genetic variation such as SNPs and microsatellites, reflecting demographic history rather than phenotypic diversity.CNVRs in pigs are enriched for genes related to sensory perception, neurological process, and response to stimulus. The majority of CNVRs ascertained in domestic pigs are also variable in wild boars, suggesting that the domestication of the pig did not result in a change in CNVRs in domesticated pigs. The majority of variable regions were found to reflect demographic patterns rather than phenotypic.