Identification of Selection Signals on the X-Chromosome in East Adriatic Sheep: A New Complementary Approach

. 2022 ; 13 () : 887582. [epub] 20220411

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35615375

Sheep are one of the most important livestock species in Croatia, found mainly in the Mediterranean coastal and mountainous regions along the East Adriatic coast, well adapted to the environment and mostly kept extensively. Our main objective was therefore to map the positive selection of the X-chromosome (18,983 SNPs that passed quality control), since nothing is known about the adaptation genes on this chromosome for any of the breeds from the Balkan cluster. Analyses were performed on a sample of eight native Croatian breeds (101 females and 100 males) representing the East Adriatic metapopulation and on 10 mouflons (five females and males), all sampled in Croatia. Three classical within-population approaches (extreme Runs of Homozygosity islands, integrated Haplotype Score, and number of Segregating Sites by Length) were applied along with our new approach called Haplotype Richness Drop (HRiD), which uses only the information contained in male haplotypes. We have also shown that phylogenetic analyses, such as the Median-joining network, can provide additional information when performed with the selection signals identified by HRiD. Our new approach identifies positive selection signals by searching for genomic regions that exhibit a sudden decline in haplotype richness. In total, we identified 14 positive selection signals, 11 using the classical approach and three using the HRiD approach, all together containing 34 annotated genes. The most reliable selection signal was mapped by all four approaches in the same region, overlapping between 13.17 and 13.60 Mb, and assigned to the CA5B, ZRSR2, AP1S2, and GRPR genes. High repeatability (86%) of results was observed, as 12 identified selection signals were also confirmed in other studies with sheep. HRiD offers an interesting possibility to be used complementary to other approaches or when only males are genotyped, which is often the case in genomic breeding value estimations. These results highlight the importance of the X-chromosome in the adaptive architecture of domestic ruminants, while our novel HRiD approach opens new possibilities for research.

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Allendorf F. W., Luikart G., Aitken S. N. (2013). Conservation and the Genetics of Populations. Hoboken: John Wiley & Sons.

Álvarez I., Fernández I., Traoré A., Pérez-Pardal L., Menéndez-Arias N. A., Goyache F. (2020). Genomic Scan of Selective Sweeps in Djallonké (West African Dwarf) Sheep Shed Light on Adaptation to Harsh Environments. Sci. Rep. 10, 1–13. 10.1038/s41598-020-59839-x PubMed DOI PMC

Bandelt H. J., Forster P., Röhl A. (1999). Median-joining Networks for Inferring Intraspecific Phylogenies. Mol. Biol. Evol. 16, 37–48. 10.1093/oxfordjournals.molbev.a026036 PubMed DOI

Blaya C., Moorjani P., Salum G. A., Gonçalves L., Weiss L. A., Leistner-Segal S., et al. (2009). Preliminary Evidence of Association between EFHC2, a Gene Implicated in Fear Recognition, and Harm Avoidance. Neurosci. Lett. 452, 84–86. 10.1016/j.neulet.2009.01.036 PubMed DOI

Blommaert E., Péanne R., Cherepanova N. A., Rymen D., Staels F., Jaeken J., et al. (2019). Mutations in MAGT1 lead to a Glycosylation Disorder with a Variable Phenotype. Proc. Natl. Acad. Sci. U.S.A. 116, 9865–9870. 10.1073/pnas.1817815116 PubMed DOI PMC

Boyko A. R., Quignon P., Li L., Schoenebeck J. J., Degenhardt J. D., Lohmueller K. E., et al. (2010). A Simple Genetic Architecture Underlies Morphological Variation in Dogs. Plos Biol. 8, e1000451. 10.1371/journal.pbio.1000451 PubMed DOI PMC

Cesarani A., Gaspa G., Correddu F., Dimauro C., Macciotta N. P. P. (2022). Unravelling the Effect of Environment on the Genome of Sarda Breed Ewes Using Runs of Homozygosity. J. Anim. Breed. Genet. [Epub Online ahead of print]. 10.1111/jbg.12666 PubMed DOI

Chang C. C., Chow C. C., Tellier L. C., Vattikuti S., Purcell S. M., Lee J. J. (2015). Second-generation Plink: Rising to the challenge of Larger and Richer Datasets. GigaSci 4, s13742. 10.1186/s13742-015-0047-8 PubMed DOI PMC

Chen Z.-H., Zhang M., Lv F.-H., Ren X., Li W.-R., Liu M.-J., et al. (2018). Contrasting Patterns of Genomic Diversity Reveal Accelerated Genetic Drift but Reduced Directional Selection on X-Chromosome in Wild and Domestic Sheep Species. Gen. Biol. Evol. 10, 1282–1297. 10.1093/gbe/evy085 PubMed DOI PMC

Choi B., Ryu K., Bong J., Lee J., Choy Y., Son S., et al. (2010). Comparison of Steroid Hormone Concentrations and mRNA Levels of Steroid Receptor Genes in Longissimus Dorsi Muscle and Subcutaneous Fat between Bulls and Steers and Association with Carcass Traits in Korean Cattle. Livestock Sci. 131, 218–226. 10.1016/j.livsci.2010.04.004 DOI

Choi Y., Chan A. P., Kirkness E., Telenti A., Schork N. J. (2018). Comparison of Phasing Strategies for Whole Human Genomes. Plos Genet. 14, e1007308. 10.1371/journal.pgen.1007308 PubMed DOI PMC

Ciani E., Mastrangelo S., Mastrangelo S., Da Silva A., Marroni F., Ferenčaković M., et al. (2020). On the Origin of European Sheep as Revealed by the Diversity of the Balkan Breeds and by Optimizing Population-Genetic Analysis Tools. Genet. Sel. Evol. 52, 1–14. 10.1186/s12711-020-00545-7 PubMed DOI PMC

Curik I., Ferenčaković M., Sölkner J. (2014). Inbreeding and Runs of Homozygosity: a Possible Solution to an Old Problem. Livestock Sci. 166, 26–34. 10.1016/j.livsci.2014.05.034 DOI

Curik I., Sölkner J., Stipic N. (2002). Effects of Models with Finite Loci, Selection, Dominance, Epistasis and Linkage on Inbreeding Coefficients Based on Pedigree and Genotypic Information. J. Anim. Breed. Genet. 119, 101–115. 10.1046/j.1439-0388.2002.00329.x DOI

Delaneau O., Marchini J. (2014). Integrating Sequence and Array Data to Create an Improved 1000 Genomes Project Haplotype Reference Panel. Nat. Commun. 5, 3934. 10.1038/ncomms4934 PubMed DOI PMC

Ding Q., Zhang J. (2012). seqRFLP: Simulation and Visualization of Restriction Enzyme Cutting Pattern from DNA Sequences. R Package Version 1.0.1. Available at: https://cran.r-project.org/web/packages/seqRFLP/index.html (Acessed January 25, 2022).

Druet T., Gautier M. (2017). A Model-Based Approach to Characterize Individual Inbreeding at Both Global and Local Genomic Scales. Mol. Ecol. 26, 5820–5841. 10.1111/mec.14324 PubMed DOI

Duman E., Özmen Ö., Kul S. (2021). Oar-miR-16b and Oar-miR-27a: Negatively Correlated with Milk Yield and Milk Protein in Sheep. Anim. Biotechnol. [Epub Online ahead of print]. 10.1080/10495398.2021.1908317 PubMed DOI

Excoffier L., Lischer H. E. L. (2010). Arlequin Suite Ver 3.5: a New Series of Programs to Perform Population Genetics Analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567. 10.1111/j.1755-0998.2010.02847.x PubMed DOI

Ferenčaković M., Sölkner J., Curik I. (2013). Estimating Autozygosity from High-Throughput Information: Effects of SNP Density and Genotyping Errors. Genet. Sel. Evol. 45, 42. 10.1186/1297-9686-45-42 PubMed DOI PMC

Ferrer-Admetlla A., Liang M., Korneliussen T., Nielsen R. (2014). On Detecting Incomplete Soft or Hard Selective Sweeps Using Haplotype Structure. Mol. Biol. Evol. 31, 1275–1291. 10.1093/molbev/msu077 PubMed DOI PMC

Gao X., Starmer J., Martin E. R. (2008). A Multiple Testing Correction Method for Genetic Association Studies Using Correlated Single Nucleotide Polymorphisms. Genet. Epidemiol. 32, 361–369. 10.1002/gepi.20310 PubMed DOI

Gautier M., Vitalis R. (2012). Rehh: an R Package to Detect Footprints of Selection in Genome-wide SNP Data from Haplotype Structure. Bioinformatics 28, 1176–1177. 10.1093/bioinformatics/bts115 PubMed DOI

Genolet O., Monaco A. A., Dunkel I., Boettcher M., Schulz E. G. (2021). Identification of X-Chromosomal Genes that Drive Sex Differences in Embryonic Stem Cells through a Hierarchical CRISPR Screening Approach. Genome Biol. 22, 1–41. 10.1186/s13059-021-02321-2 PubMed DOI PMC

Gorssen W., Meyermans R., Janssens S., Buys N. (2021). A Publicly Available Repository of ROH Islands Reveals Signatures of Selection in Different Livestock and Pet Species. Genet. Sel. Evol. 53, 1–10. 10.1186/s12711-020-00599-7 PubMed DOI PMC

Greenbaum G., Templeton A. R., Zarmi Y., Bar-David S. (2014). Allelic Richness Following Population Founding Events - A Stochastic Modeling Framework Incorporating Gene Flow and Genetic Drift. PLoS One 9, e115203. 10.1371/journal.pone.0115203 PubMed DOI PMC

Guo J., Fan X., Yang Y., Liang G., Tang Z. (2021). Sequence Characteristics and Expression Analysis of CA5B Gene in Pigs. Act. Vet. Zoot. Sin. 52, 322–330. 10.11843/j.issn.0366-6964.2021.02.005 DOI

Jiang Y., Xie M., Chen W., Talbot R., Maddox J. F., Faraut T., et al. (2014). The Sheep Genome Illuminates Biology of the Rumen and Lipid Metabolism. Science 344, 1168–1173. 10.1126/science.1252806 PubMed DOI PMC

Joyce H., Burmeister L. M., Wright H., Fleming L., Oliver J. A. C., Mellersh C. (2021). Identification of a Variant in NDP Associated with X-Linked Retinal Dysplasia in the English Cocker Spaniel Dog. PLoS One 16, e0251071. 10.1371/journal.pone.0251071 PubMed DOI PMC

Kammoun M., Maas E., Criem N., Gribnau J., Zwijsen A., Vermeesch J. R. (2018). RLIM Enhances BMP Signalling Mediated Fetal Lung Development in Mice. bioRxiv. [Preprint]. 10.1101/507921 DOI

Karasu M. E., Keeney S. (2019). Cyclin B3 Is Dispensable for Mouse Spermatogenesis. Chromosoma 128, 473–487. 10.1007/s00412-019-00725-5 PubMed DOI PMC

Kardos M., Luikart G., Bunch R., Dewey S., Edwards W., McWilliam S., et al. (2015). Whole‐genome Resequencing Uncovers Molecular Signatures of Natural and Sexual Selection in Wild Bighorn Sheep. Mol. Ecol. 24, 5616–5632. 10.1111/mec.13415 PubMed DOI

Kardos M., Qvarnström A., Ellegren H. (2017). Inferring Individual Inbreeding and Demographic History from Segments of Identity by Descent in Ficedula Flycatcher Genome Sequences. Genetics 205, 1319–1334. 10.1534/genetics.116.198861 PubMed DOI PMC

Kim E.-S., Cole J. B., Huson H., Wiggans G. R., Van Tassell C. P., Crooker B. A., et al. (2013). Effect of Artificial Selection on Runs of Homozygosity in U.S. Holstein Cattle. PLoS One 8, e80813. 10.1371/journal.pone.0080813 PubMed DOI PMC

Kimura M., Crow J. F. (1964). The Number of Alleles that Can Be Maintained in a Finite Population. Genetics 49, 725–738. 10.1093/genetics/49.4.725 PubMed DOI PMC

Kumar S., Stecher G., Tamura K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 33, 1870–1874. 10.1093/molbev/msw054 PubMed DOI PMC

Leigh J. W., Bryant D. (2015). Popart : Full‐feature Software for Haplotype Network Construction. Methods Ecol. Evol. 6, 1110–1116. 10.1111/2041-210X.12410 DOI

Lencz T., Lambert C., DeRosse P., Burdick K. E., Morgan T. V., Kane J. M., et al. (2007). Runs of Homozygosity Reveal Highly Penetrant Recessive Loci in Schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 104, 19942–19947. 10.1073/pnas.0710021104 PubMed DOI PMC

Liu Z., Ji Z., Wang G., Chao T., Hou L., Wang J. (2016). Genome-wide Analysis Reveals Signatures of Selection for Important Traits in Domestic Sheep from Different Ecoregions. BMC Genomics 17, 1–14. 10.1186/s12864-016-3212-2 PubMed DOI PMC

Lv F.-H., Cao Y.-H., Liu G.-J., Luo L.-Y., Lu R., Liu M.-J., et al. (2022). Whole-Genome Resequencing of Worldwide Wild and Domestic Sheep Elucidates Genetic Diversity, Introgression, and Agronomically Important Loci. Mol. Biol. Evol. 39, msab353. 10.1093/molbev/msab353 PubMed DOI PMC

Lv F.-H., Peng W.-F., Yang J., Zhao Y.-X., Li W.-R., Liu M.-J., et al. (2015). Mitogenomic Meta-Analysis Identifies Two Phases of Migration in the History of Eastern Eurasian Sheep. Mol. Biol. Evol. 32, 2515–2533. 10.1093/molbev/msv139 PubMed DOI PMC

Ma Z., Zhang Y., Su J., Li X., Yang S., Qiao W., et al. (2018). Distribution of the Pig Gastrin-Releasing Peptide Receptor and the Effect of GRP on Porcine Leydig Cells. Peptides 99, 142–152. 10.1016/j.peptides.2017.09.015 PubMed DOI

Manzari Z., Mehrabani‐Yeganeh H., Nejati‐Javaremi A., Moradi M. H., Gholizadeh M. (2019). Detecting Selection Signatures in Three Iranian Sheep Breeds. Anim. Genet. 50, 298–302. 10.1111/age.12772 PubMed DOI

McManus C., Paiva S. R., Araújo R. O. d. (2010). Genetics and Breeding of Sheep in Brazil. R. Bras. Zootec. 39, 236–246. 10.1590/S1516-35982010001300026 DOI

Moradi M. H., Nejati-Javaremi A., Moradi-Shahrbabak M., Dodds K. G., McEwan J. C. (2012). Genomic Scan of Selective Sweeps in Thin and Fat Tail Sheep Breeds for Identifying of Candidate Regions Associated with Fat Deposition. BMC Genet. 13, 10–15. 10.1186/1471-2156-13-10 PubMed DOI PMC

Muigai A. W., Hanotte O. (2013). The Origin of African Sheep: Archaeological and Genetic Perspectives. Afr. Archaeol. Rev. 30, 39–50. 10.1007/s10437-013-9129-0 PubMed DOI PMC

Nadachowska‐Brzyska K., Burri R., Ellegren H. (2019). Footprints of Adaptive Evolution Revealed by Whole Z Chromosomes Haplotypes in Flycatchers. Mol. Ecol. 28, 2290–2304. 10.1111/mec.15021 PubMed DOI PMC

Nel C., Gurman P., Swan A., van der Werf J., Snyman M., Dzama K., et al. (2022). The Genomic Structure of Isolation across Breed, Country and Strain for Important South African and Australian Sheep Populations. BMC Genomics 23, 1–19. 10.1186/s12864-021-08020-3 PubMed DOI PMC

Nothnagel M., Lu T. T., Kayser M., Krawczak M. (2010). Genomic and Geographic Distribution of SNP-Defined Runs of Homozygosity in Europeans. Hum. Mol. Genet. 19, 2927–2935. 10.1093/hmg/ddq198 PubMed DOI

Peterson E. K. (2020). Novel Polymorphisms of ZRSR2 and GPM6B Gene Homologs and Their Use in Sex Identification of Bovine and Porcine Species. Doctoral dissertation. Logan, UT: Utah State University. 10.26076/d919-facd DOI

Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M. A. R., Bender D., et al. (2007). PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses. Am. J. Hum. Genet. 81, 559–575. 10.1086/519795 PubMed DOI PMC

Qanbari S., Simianer H. (2014). Mapping Signatures of Positive Selection in the Genome of Livestock. Livestock Sci. 166, 133–143. 10.1016/j.livsci.2014.05.003 DOI

Ramón M., Carabaño M. J., Díaz C., Kapsona V. V., Banos G., Sánchez-Molano E. (2021). Breeding Strategies for Weather Resilience in Small Ruminants in Atlantic and Mediterranean Climates. Front. Genet. 12, 692121. 10.3389/fgene.2021.692121 PubMed DOI PMC

Rozas J., Ferrer-Mata A., Sánchez-DelBarrio J. C., Guirao-Rico S., Librado P., Ramos-Onsins S. E., et al. (2017). DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Mol. Biol. Evol. 34, 3299–3302. 10.1093/molbev/msx248 PubMed DOI

Saravanan K. A., Panigrahi M., Kumar H., Bhushan B., Dutt T., Mishra B. P., et al. (2020). Selection Signatures in Livestock Genome: A Review of Concepts, Approaches and Applications. Livestock Sci. 241, 104257. 10.1016/j.livsci.2020.104257 DOI

Schaffner S. F. (2004). The X Chromosome in Population Genetics. Nat. Rev. Genet. 5, 43–51. 10.1038/nrg1247 PubMed DOI

Solé M., Gori A.-S., Faux P., Bertrand A., Farnir F., Gautier M., et al. (2017). Age-based Partitioning of Individual Genomic Inbreeding Levels in Belgian Blue Cattle. Genet. Sel. Evol. 49, 1–18. 10.1186/s12711-017-0370-x PubMed DOI PMC

Starokadomskyy P., Escala Perez-Reyes A., Burstein E. (2021). Immune Dysfunction in Mendelian Disorders of POLA1 Deficiency. J. Clin. Immunol. 41, 285–293. 10.1007/s10875-020-00953-w PubMed DOI PMC

Stella A., Ajmone-Marsan P., Lazzari B., Boettcher P. (2010). Identification of Selection Signatures in Cattle Breeds Selected for Dairy Production. Genetics 185, 1451–1461. 10.1534/genetics.110.116111 PubMed DOI PMC

Szpiech Z. A., Hernandez R. D. (2014). Selscan: an Efficient Multithreaded Program to Perform EHH-Based Scans for Positive Selection. Mol. Biol. Evol. 31, 2824–2827. 10.1093/molbev/msu211 PubMed DOI PMC

Thorne J. W., Murdoch B. M., Freking B. A., Redden R. R., Murphy T. W., Taylor J. B., et al. (2021). Evolution of the Sheep Industry and Genetic Research in the United States: Opportunities for Convergence in the Twenty‐first century. Anim. Genet. 52, 395–408. 10.1111/age.13067 PubMed DOI PMC

Utsunomiya Y. T., Pérez O'Brien A. M., Sonstegard T. S., Sölkner J., Garcia J. F. (2015). Genomic Data as the “hitchhiker’s guide” to Cattle Adaptation: Tracking the Milestones of Past Selection in the Bovine Genome. Front. Genet. 6, 36. 10.3389/fgene.2015.00036 PubMed DOI PMC

Vicoso B., Charlesworth B. (2006). Evolution on the X Chromosome: Unusual Patterns and Processes. Nat. Rev. Genet. 7, 645–653. 10.1038/nrg1914 PubMed DOI

Voight B. F., Kudaravalli S., Wen X., Pritchard J. K. (2006). A Map of Recent Positive Selection in the Human Genome. PLoS Biol. 4, e72. 10.1371/journal.pbio.0040072 PubMed DOI PMC

Wang F., Gervasi M. G., Bošković A., Sun F., Rinaldi V. D., Yu J., et al. (2021). Deficient Spermiogenesis in Mice Lacking Rlim. Elife 10, e63556. 10.7554/eLife.63556 PubMed DOI PMC

Witt K. E., Huerta-Sánchez E. (2019). Convergent Evolution in Human and Domesticate Adaptation to High-Altitude Environments. Phil. Trans. R. Soc. B 374, 20180235. 10.1098/rstb.2018.0235 PubMed DOI PMC

Wu H., Liu Y.-H., Wang G.-D., Yang C.-T., Otecko N. O., Liu F., et al. (2016). Identifying Molecular Signatures of Hypoxia Adaptation from Sex Chromosomes: A Case for Tibetan Mastiff Based on Analyses of X Chromosome. Sci. Rep. 6, 35004. 10.1038/srep35004 PubMed DOI PMC

Zeder M. A. (2008). Domestication and Early Agriculture in the Mediterranean Basin: Origins, Diffusion, and Impact. Proc. Natl. Acad. Sci. U.S.A. 105, 11597–11604. 10.1073/pnas.0801317105 PubMed DOI PMC

Zhu C., Fan H., Yuan Z., Hu S., Zhang L., Wei C., et al. (2015). Detection of Selection Signatures on the X Chromosome in Three Sheep Breeds. Ijms 16, 20360–20374. 10.3390/ijms160920360 PubMed DOI PMC

Zhu C., Li M., Qin S., Zhao F., Fang S. (2020). Detection of Copy Number Variation and Selection Signatures on the X Chromosome in Chinese Indigenous Sheep with Different Types of Tail. Asian-australas J. Anim. Sci. 33, 1378–1386. 10.5713/ajas.18.0661 PubMed DOI PMC

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