Genetic aspects of polledness in sheep (review)
Abstract
The analysis of the genetic mechanisms underlying the presence or absence of horns is of interest both for understanding evolutionary processes and for realizing the economic benefits of breeding polled animals. The creation of polled sheep breeds has become an important breeding goal in many countries with developed sheep breeding industries, as these breeds are more technologically efficient to manage and require less feed. Mapping genetic variability to specific candidate loci allows the most accurate assessment of the influence of individual alleles and the genotype-phenotype relationship of hornedness and polledness. This review analyzes the current state of research aimed at identifying genes and genomic regions associated with polledness in sheep, and explores the potential of using genomic approaches in breeding programs for polled breeds. The inheritance of polledness is complex, as its expression differs between sexes, and no single-locus model with complete penetrance can fully explain the observed phenotypic variability within and between breeds. The RXFP2 (relaxin/insulin-like family peptide receptor 2) marker gene is shown to be promising for further study in different breeds for use in breeding programmes. Genome editing and transcriptome analysis are promising approaches to fully understand the mechanism by which different *RXFP2* alleles influence horn morphology and to develop polled animals. Accumulating knowledge in this area will enable a more complete understanding of the genetic mechanisms underlying the polled phenotype in sheep.
Supporting agencies: The work was carried out within the framework of the project “Scientific Frontier” under the State Program for Supporting Universities “Priority 2030” (topic: “Genetic technologies and biotechnological methods in selection, nutrition and ensuring animal welfare to improve the efficiency of animal husbandry”).
About the Authors
M. I. Selionova
Russian State Agrarian University – Moscow Timiryazev Agricultural Academy
Russian Federation
Russian Federation
Marina I. Selionova, DSc (Bio), Professor of the Russian Academy of Sciences, Vice-Rector for Research
49 Timiryazevskaya St., Moscow, 127550
D. D. Evlagina
North Caucasian Federal Scientific Agrarian Center
Russian Federation
Russian Federation
Daria D. Evlagina, CSc (Bio), Senior Research Associate
49 Nikonova St., Mikhailovsk, Shpakovsky district, Stavropol Krai, 356241
References
1. Deniskova I.E., Dotsev A.V., Petrov S.N., Zinovieva N.A. Search for QTL and functional candidate genes as an important step in the implementation of genomic breeding in sheep breeding. XIV mezhdunarodnyy biotekhnologicheskiy forum ‘Rosbiotekh-2020’. November 17-19, 2020. Moscow, Russia: V.M. Gorbatov Federal Research Center for Food Systems of Russian Academy of Sciences. 2020;174-175. (In Russ.)
2. Zhumadillaev N.K., Yuldashbaev Y.A., Karynbaev A.K. Effect of hornless on the productivity of Etti Merino sheep. Agrarian Science. 2020;(5):56-59. (In Russ.) https://doi.org/10.32634/0869-8155-2020-338-5-56-59
3. Feyzullaev F.R., Shaidullin I.N., Kirillova K.E., Timoshenko Yu.I. et al. Meat productivity of horned and polled sheep of the Volgograd breed. Ovtsy, kozy, sherstyanoye delo. 2015;(4):27-28. (In Russ.) EDN: VQEGXT
4. Arkell T.R., Davenport C.B. The nature of the inheritance of horns in sheep. Science. 1912;35(911):927. https://doi.org/10.1126/science.35.911.927
5. Beraldi D., McRae A.F., Gratten J.J. et al. Pemberton development of a linkage map and mapping of phenotypic polymorphisms in a free-living population of Soay sheep (Ovis aries). Genetics. 2006;173(3):1521-537. https://doi.org/10.1534/genetics.106.057141
6. Castle W.E. Are horns in sheep a sex-limited character? Science. 1912;35(902):574-575. https://doi.org/10.1126/science.35.902.574
7. Cheng H., Zhang Z., Wen J., Lenstra J. et al. Long divergent haplotypes introgressed from wild sheep are associated with distinct morphological and adaptive characteristics in domestic sheep. PLoS Genet. 2023;19(2): e1010615. https://doi.org/10.1371/journal.pgen.1010615
8. Council Directive 98/59/EC concering the protection of animals kept for farming purpose: 98/58/EC. CELEX-EUR. CELEX-EUR Off. J. L 221. 1998:23-27. URL: https://www.fao.org/faolex/results/details/en/c/LEX-FAOC025031/ (accessed: January 15, 2024)
9. Cozzi G., Prevedello P., Boukha A. et al. Alternatives to Castration and Dehorning. Report on Dehorning Practices across EU Member States. ALCASDE. APPENDIX 20. 2009:1-140. URL: http://www.vuzv.sk/DB-Welfare/telata/calves_alcasde_D-2-1-1.pdf (accessed: January 28, 2024)
10. Dolling C. Hornedness and polledness in sheep.: IV. Triple alleles affecting horn growth in the Merino. Aust. J. Agric. Res. 1961;12(2):353-361. https://doi.org/10.1071/AR9610535
11. Dominik S., Henshall J.M., Hayes B.J. A single nucleotide polymorphism on chromosome 10 is highly predictive for the polled phenotype in Australian Merino sheep. Animal Genetics. 2012;43(4):468-470. https://doi.org/10.1111/j.1365-2052.2011.02271.x
12. Doudna J.A., Charpentier E. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science. 2014;346:1258096. https://doi.org/10.1126/science.1258096
13. Duijvesteijn N., Bolormaa S., Daetwyler H.D., van der Werf J.H.J. Genomic prediction of the polled and horned phenotypes in Merino sheep. Genetics Selection Evolution. 2018;50(28):1-11. https://doi.org/10.1186/s12711-018-0398-6
14. EuGH Vorlage zur Vorabentscheidung-Absichtliche Freisetzung genetisch veränderter Organismen in die Umwelt-Mutagenese-Richtlinie 2001/18/EG-Art. 2 und 3–Anhänge I A und I B. Urteil vom 25.072018 – rechtssache c-528/16 urteil des gerichtshofs (Große Kammer). URL: https://www.regierung. oberbayernbayern.de/mam/dokumente/eugh-urteil_c-528-16.pdf (accessed: March 13, 2024)
15. Feng S., Ferlin A., Truong A., Bathgate R. et al. INSL3/RXFP2 signaling in testicular descent: mice and men. Annals of the New York Academy of Sciences. 2009;1160(1):197-204. https://doi.org/10.1111/j.1749-6632.2009.03841.x
16. Ferlin A., Pepe A., Gianesello L., Garolla A. et al. Mutations in the insulin-like factor 3 receptor are associated with osteoporosis. Journal of Bone and Mineral Research. 2008;23(5):683-693. https://doi.org/10.1359/jbmr.080204
17. Greyvenstein O.F.C., Reich C.M., van Marle-Koster E., Riley D.G. et al. Polyceraty (multi-horns) in Damara sheep maps to ovine chromosome 2. Animal Genetics. 2016;47(2):263-266. https://doi.org/10.1111/age.12411
18. Ren X., Yang G.L., Peng W.F., Zhao Y.X. et al. A genome-wide association study identifies a genomic region for the polycerate phenotype in sheep (Ovis aries). Sci Rep. 2016;6:21111. https://doi.org/10.1038/srep21111
19. He X., Zhou Z., Pu Y., Chen X. et al. Mapping the four-horned locus and testing the polled locus in three Chinese sheep breeds. Anim Genet. 2016;47(5):623-627. https://doi.org/10.1111/age.12464
20. Hu X.J., Yang J., Xie X.L., Lv F.H. et al. The genome landscape of Tibetan sheep reveals adaptive introgression from Argali and the history of early human settlements on the Qinghai-Tibetan plateau. Molecular Biology and Evolution. 2019;36(2):283-303. https://doi.org/10.1093/molbev/msy208
21. Hu Z.L., Park C.A., Reecy J.M. Developmental progress and current status of the Animal QTLdb. Nucleic Acids Res. 2016;44(1):827-833. https://doi.org/10.1093/nar/gkv1233
22. Jewell P.A. Survival and behaviour of castrated Soay sheep (Ovis aries) in a feral island population on Hirta St. Kilda, Scotland. Journal of Zoology. 1997;243(3):623-636. https://doi.org/10.1111/j.1469-7998.1997.tb02806.x
23. Jinek M., Chylinski K., Fonfara I. et al. Charpentier A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816-821. https://doi.org/10.1126/science.1225829
24. Johnston S., McEwan J., Pickering N. et al. Genome-wide association mapping identifies the genetic basis of discrete and quantitative variation in sexual weaponry in a wild sheep population. Molecular Ecology. 2011;20(12):2555-2566. https://doi.org/10.1111/j.1365-294X.2011.05076.x
25. Johnston S.E., Beraldi D., McRae A.F. et al. Slate Horn type and horn length genes map to the same chromosomal region in Soay sheep. Heredity. 2010;104(2):196-205. https://doi.org/10.1038/hdy.2009.109
26. Johnston S.E., Gratten J., Berenos C. et al. Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature. 2013;502(7469):93-95. https://doi.org/10.1038/nature12489
27. KaldsP., Zhou S., Gao Y. et al. Genetics of the phenotypic evolution in sheep: a molecular look at diversity-driving genes. Genetics Selection Evolution. 2022;54(1):61. https://doi.org/10.1186/s12711-022-00753-3
28. Kijas J.W., Lenstra J.A., Hayes B. et al. Genome-wide analysis of the world’s sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biology. 2012;10(2): e1001258. https://doi.org/10.1371/journal.pbio.1001258
29. Li X., Yang J., Shen M. et al. Whole-genome resequencing of wild and domestic sheep identifies genes associated with morphological and agronomic traits. Nature Communications. 2020;11(1):2815. https://doi.org/10.1038/s41467-020-16485-1
30. Luan Y., Wu S., Wang M. et al. Identification of critical genes for ovine horn development based on transcriptome during the embryonic period. Biology. 2023;12(4):591. https://doi.org/10.3390/biology12040591
31. Lühken G., Krebs S., Rothammer S. et al. The 1.78-kb insertion in the 3′-untranslated region of RXFP2 does not segregate with horn status in sheep breeds with variable horn status. Genet Sel Evol. 2016;48:1-14. https://doi.org/10.1186/s12711-016-0256-3
32. Montgomery G.W., Henry H.M., Dodds K.G. et al. Mapping the horns (Ho) locus in sheep: a further locus controlling horn development in domestic animals. Journal of Heredity. 1996;87(5):358-363. https://doi.org/10.1093/oxfordjournals.jhered.a023014
33. Pan Z., Li S., Liu Q. et al. Whole-genome sequences of 89 Chinese sheep suggest role of RXFP2 in the development of unique horn phenotype as response to semi-feralization. GigaScience. 2018;7(4):1-15. https://doi.org/10.1093/gigascience/giy019
34. Picard K., Thomas D.W., Festa-Bianchiet M. et al. Differences in thermal conductivity of tropical and 420 temperate bovid horns. Ecoscience. 1999;6(2):148-158. https://doi.org/10.1080/11956860.1999.11682515
35. Pickering N.K., Johnson P.L., Auvray B. et al. Mapping the horns locus in sheep. Proc Assoc Advmt Anim Breed Genet. 2009;18:88-91.
36. Robinson M.R., Pilkington J.G., Clutton-Brock T.H. Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep. Evolution. 2006;60(10):2168-2181. https://doi.org/10.1111/j.0014-3820.2006.tb01854.x
37. Ruan J., Xu J., Chen-Tsai R.Y. et al. Genome editing in livestock: Are we ready for a revolution in animal breeding industry? Transgenic Research. 2017;26:715-726. https://doi.org/10.1007/s11248-017-0049-7
38. Simon R., Drögemüller C., Lühken G. The complex and diverse genetic architecture of the absence of horns (Polledness) in domestic ruminants, including goats and sheep. Genes. 2022;13(5):832. https://doi.org/10.3390/genes13050832
39. Van Eenennaam A.L. The contribution of transgenic and genome-edited animals to agricultural and industrial applications. Revue Scientifique et Technique (International Office of Epizootics). 2018;37(1):97-112. https://doi.org/10.20506/rst.37.1.2743
40. Wang X.L., Zhou G.X., Li Q. Discovery of SNPs in RXFP2 related to horn types in sheep. Small Ruminant Research. 2014;116(2-3):133-136. https://doi.org/10.1016/j.smallrumres.2013.10.022
41. Wang Y., Zhang C., Wang N. et al. Genetic basis of ruminant headgear and rapid antler regeneration. Science. 2019;364(6446): eaav6335. https://doi.org/10.1126/science.aav633
42. Wiedemar N., Wiedemar N., Drögemüller C. A 1.8-kb insertion in the 3′-UTR of RXFP2 is associated with polledness in sheep. Animal Genetics. 2015;46(4):457-461. https://doi.org/10.1111/age.12309
43. Yuan F.P., Li X., Lin J. et al. The role of RXFP2 in mediating androgen-induced inguinoscrotal testis descent in LH receptor knockout mice. Reproduction (Cambridge, England). 2010;139(4):759-769. https://doi.org/10.1530/REP-09-0518.
Review
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Selionova M.I., Evlagina D.D. Genetic aspects of polledness in sheep (review). IZVESTIYA OF TIMIRYAZEV AGRICULTURAL ACADEMY. 2025;(3):151-166. (In Russ.)
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