OMIA 000483-9940 : Polled/Horns in Ovis aries

In other species: cattle , goat , water buffalo , bighorn sheep , kouprey , domestic yak

Possibly relevant human trait(s) and/or gene(s) (MIM number): 110100

Mendelian trait/disorder: yes

Considered a defect: yes

Key variant known: yes

Year key variant first reported: 2011

Cross-species summary: There is substantial variation in the extent of horn growth, making classification difficult. However, in general, the presence or absence of horns can be attributed to the action of two alleles at an autosomal locus. The type of gene action varies considerably between and among species.

Species-specific symbol: Ho

Species-specific description: A fascinating evolutionary story concerning the polled/horns locus in Soay sheep was uncovered by Johnston et al. (2013), who showed that the polymorphism at the polled/horns locus in Soay sheep "is maintained by a trade-off between natural and sexual selection . . . We found that an allele conferring larger horns, Ho+, is associated with higher reproductive success, whereas a smaller horn allele, HoP, confers increased survival, resulting in a net effect of overdominance (that is, heterozygote advantage) for fitness at RXFP2."

History: A comprehensive review of the inheritance of horns in sheep was provided by Dolling (1970), while Tibau i Font et al. (1982) compiled a bibliography.

Inheritance: In his series of papers in 1960 and 1961 on the inheritance of polled/horns in Australian sheep, Dolling reported that polled is dominant to horns in Merino, with the effect of the horns allele being greater in males than in females; that the Dorset Horn breed is homozygous for the dominant polled allele; and that polled is dominant to horns in the Border Leicester breed, with dominance being "complete in the female and partially so in the male".

In their report on mapping the polled/horns locus in their New Zealand Romney x Merino population, Pickering et al. (2009) cited the Soay mode of inheritance for polled/horns, namely that polled is recessive, as described by Clutton-Brock and Pemberton (2004). The most recent summary of the type of gene action in Soay sheep is by Johnston et al. (2011): in females, the two alleles are additive (Ho+/Ho+ = horned; Ho+/HoP = scurred; HoP/HoP = polled); and in males, the horned allele is dominant (Ho+/Ho+ and Ho+/HoP = horned, and HoP/HoP are either horned or scurred with roughly equal frequency). It is, of course, quite possible for the type of gene action to vary between breeds.

Mapping: Vaiman et al. (1996) discovered that the horns locus in goats is located in the distal region of goat chromosome 1. Since this chromosome of goats is homologous to one of the arms of sheep chromosome 1, it seemed possible that the horns gene in sheep is located on sheep chromosome 1. Interestingly, the horns gene in cattle is located on cattle chromosome 1, which is homologous to goat chromosome 1. However, the locations of the bovine and caprine horns genes are not homologous (Vaiman et al., 1996). The debate was settled by Montgomery et al. (1996; next paragraph) who showed that the horns locus in sheep is actually located on chromosome 10. Thus the horns loci of sheep, cattle and goats all appear to be different.

Montgomery et al. (1996) mapped this locus to the proximal end of OAR10 in a Romney-Merino cross flock, showing no recombinants with microsatellite AGLA226, whose location is OAR10q13. Beraldi et al. (2006) confirmed this location, in Soay sheep. Johnston et al. (2010) narrowed the region to 7.4cM in Soay sheep. Pickering et al. (2009) narrowed the region in domestic (New Zealand Romney x Merino backcross) sheep to 200kb. The OAR10 location of horns/polled in sheep bears no homology to the BTA1 location of horns/polled in cattle, suggesting that the same trait in the two species is determined by different genes.

In a genome-wide association study (GWAS) on 486 Soay sheep, each genotyped with the Ovine SNP50 BeadChip (yielding 35,831 informative SNPs) and phenotyped into normal, scurred and polled, Johnston et al. (2011) narrowed down the location of the horns/polled locus in Soay sheep to a 250kb region at around 29.4Mb on chromosome OVA10. A GWAS analysis on EBV for horn length on 160 of the above sheep confirmed this location.

In Australian Merino sheep, Dominik et al. (2012) genotyped each of 10 phenotyped rams and 918 of their phenotyped offspring with the Illumina ovine 50k SNP chip, yielding 48,640 informative SNPs. A linkage-disequilibrium analysis mapped the trait to "a SNP located at Mb position 29.38 on sheep chromosome [OVA]10", the nearest gene being RXFP2.

Also in 2012, when Kijas et al. genotyped each of 2,819 sheep from 74 different breeds with the Illumina Ovine 50K SNP chip and searched for signatures of selection by calculating FST for each of the 49,034 informative SNPs, they discovered that "the strongest selection signal was identified immediately adjacent to RXFP2 [at Mb position 29.54 on chromosome OVA10] . . . Strong evidence supports that RXFP2 was targeted by breeding for the removal of horns, likely to be one of the oldest morphological modifications that accompanied domestication".

Molecular basis: The gene nearest to the SNPs with the strongest association in the candidate region on OVA10 is the gene for Relaxin-like receptor 2 (RXFP2). Johnston et al. (2011) provided strong evidence for this gene's primary involvement in horn development. Specifically, they designated the two alleles of a C>T SNP in the 3' UTR of RXFP2 as alleles Ho+ (wild type) and HoP (polled or scurred), respectively.

Gene expression studies of RXFP2 by Allais-Bonnet et al. (2013) showed differential expression in horn-bud tissues from polled and horned cattle, thereby establishing a link between polledness in sheep and cattle.

By sequencing the candidate RXFP2 region in seven Swiss sheep breeds, Wiedemar and Drögemüller (2015) discovered a "1833-bp genomic insertion located in the 3'-UTR region of RXFP2 present in polled animals only". Interestingly, they provided "evidence that the polled-associated insertion adds a potential antisense RNA sequence of EEF1A1 to the 3'-end of RXFP2 transcripts".

He et al. (2016) reported that "a PCR analysis for the detection of the 1.8-kb insertion associated with polled sheep in other breeds failed to verify the association with polledness in the three Chinese breeds"

Following a large-scale investigation, Lühken et al. (2016) reported that "Multiplex PCR genotyping of 489 sheep from 34 breeds and some crosses between sheep breeds showed a nearly perfect segregation of the insertion polymorphism with horn status in sheep breeds of Central and Western European origin. In these breeds and their crossings, heterozygous males were horned and heterozygous females were polled." However, "in breeds with sex-dependent and/or variable horn status, especially in sheep that originated from even more southern European regions and from Africa . . . we observed almost all possible combinations of genotype, sex and horn status phenotype". Thus, the insertion appears to be causal except in breeds "with sex-dependent and/or variable horn status".

Associated gene:

Symbol Description Species Chr Location OMIA gene details page Other Links
RXFP2 relaxin/insulin-like family peptide receptor 2 Ovis aries - no genomic information (-..-) RXFP2 Homologene, Ensembl, NCBI gene

Variants

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Breed(s) Variant Phenotype Gene Allele Type of Variant Reference Sequence Chr. g. or m. c. or n. p. Verbal Description EVA ID Year Published PubMed ID(s) Acknowledgements
Numerous breeds Polled RXFP2 insertion, gross (>20) "1833-bp genomic insertion located in the 30-UTR region of RXFP2 present in polled animals only" 2015 26103004

References


Note: the references are listed in reverse chronological order (from the most recent year to the earliest year), and alphabetically by first author within a year.
2018 Pan, Z., Li, S., Liu, Q., Wang, Z., Zhou, Z., Di, R., Miao, B., Hu, W., Wang, X., Hu, X., Xu, Z., Wei, D., He, X., Yuan, L., Guo, X., Liang, B., Wang, R., Li, X., Cao, X., Dong, X., Xia, Q., Shi, H., Hao, G., Yang, J., Luosang, C., Zhao, Y., Jin, M., Zhang, Y., Lv, S., Li, F., Ding, G., Chu, M., Li, Y. :
Whole-genome sequences of 89 Chinese sheep suggest role of RXFP2 in the development of unique horn phenotype as response to semi-feralization. Gigascience 7:, 2018. Pubmed reference: 29668959. DOI: 10.1093/gigascience/giy019.
2016 He, X., Zhou, Z., Pu, Y., Chen, X., Ma, Y., Jiang, L. :
Mapping the four-horned locus and testing the polled locus in three Chinese sheep breeds. Anim Genet 47:623-7, 2016. Pubmed reference: 27427781. DOI: 10.1111/age.12464.
Lühken, G., Krebs, S., Rothammer, S., Küpper, J., Mioč, B., Russ, I., Medugorac, I. :
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 48:78, 2016. Pubmed reference: 27760516. DOI: 10.1186/s12711-016-0256-3.
2015 Wiedemar, N., Drögemüller, C. :
A 1.8-kb insertion in the 3'-UTR of RXFP2 is associated with polledness in sheep. Anim Genet 46:457-61, 2015. Pubmed reference: 26103004. DOI: 10.1111/age.12309.
2013 Allais-Bonnet, A., Grohs, C., Medugorac, I., Krebs, S., Djari, A., Graf, A., Fritz, S., Seichter, D., Baur, A., Russ, I., Bouet, S., Rothammer, S., Wahlberg, P., Esquerré, D., Hoze, C., Boussaha, M., Weiss, B., Thépot, D., Fouilloux, M.N., Rossignol, M.N., van Marle-Köster, E., Hreiðarsdóttir, G.E., Barbey, S., Dozias, D., Cobo, E., Reversé, P., Catros, O., Marchand, J.L., Soulas, P., Roy, P., Marquant-Leguienne, B., Le Bourhis, D., Clément, L., Salas-Cortes, L., Venot, E., Pannetier, M., Phocas, F., Klopp, C., Rocha, D., Fouchet, M., Journaux, L., Bernard-Capel, C., Ponsart, C., Eggen, A., Blum, H., Gallard, Y., Boichard, D., Pailhoux, E., Capitan, A. :
Novel insights into the bovine polled phenotype and horn ontogenesis in Bovidae. PLoS One 8:e63512, 2013. Pubmed reference: 23717440. DOI: 10.1371/journal.pone.0063512.
Callaway, E. :
Big horns clash with longevity in sheep. Nature 500:387, 2013. Pubmed reference: 23969439. DOI: 10.1038/500387a.
Johnston, S.E., Gratten, J., Berenos, C., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M., Slate, J. :
Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature :, 2013. Pubmed reference: 23965625. DOI: 10.1038/nature12489.
Wang, X., Zhou, G., li, Q., Zhao, D., Chen, Y. :
Discovery of SNPs in RXFP2 related to horn types in sheep. Small Ruminant Research :, 2013. DOI: 10.1016/j.smallrumres.2013.10.022.
2012 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. Anim Genet 43:468-70, 2012. Pubmed reference: 22497244. DOI: 10.1111/j.1365-2052.2011.02271.x.
Kijas, J.W., Lenstra, J.A., Hayes, B., Boitard, S., Porto Neto, L.R., San Cristobal, M., Servin, B., McCulloch, R., Whan, V., Gietzen, K., Paiva, S., Barendse, W., Ciani, E., Raadsma, H., McEwan, J., Dalrymple, B. :
Genome-wide analysis of the world's sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biol 10:e1001258, 2012. Pubmed reference: 22346734. DOI: 10.1371/journal.pbio.1001258.
2011 Johnston, S.E., McEwan, J.C., Pickering, N.K., Kijas, J.W., Beraldi, D., Pilkington, J.G., Pemberton, J.M., Slate, J. :
Genome-wide association mapping identifies the genetic basis of discrete and quantitative variation in sexual weaponry in a wild sheep population. Mol Ecol 20:2555-66, 2011. Pubmed reference: 21651634. DOI: 10.1111/j.1365-294X.2011.05076.x.
McCairns, R.J., Merilä, J. :
Heritability not missing—genetic basis of sexual weaponry uncovered. Mol Ecol 20:, 2011. Pubmed reference: 21800446.
2010 Johnston, SE., Beraldi, D., McRae, AF., Pemberton, JM., Slate, J. :
Horn type and horn length genes map to the same chromosomal region in Soay sheep. Heredity 104:196-205, 2010. Pubmed reference: 19690581. DOI: 10.1038/hdy.2009.109.
2009 Pickering, N.K., Johnson, P.L., Auvray, B., Dodds, K.G., Mcewan, J.C. :
Mapping the horns locus in sheep Proceedings of the Association for the Advancement of Animal Breeding and Genetics 18:88-91, 2009.
2007 Robinson, M.R., Kruuk, L.E. :
Function of weaponry in females: the use of horns in intrasexual competition for resources in female Soay sheep. Biol Lett 3:651-4, 2007. Pubmed reference: 17711817. DOI: 10.1098/rsbl.2007.0278.
2006 Beraldi, D., McRae, AF., Gratten, J., Slate, J., Visscher, PM., Pemberton, JM. :
Development of a linkage map and mapping of phenotypic polymorphisms in a free-living population of Soay sheep (Ovis aries). Genetics 173:1521-37, 2006. Pubmed reference: 16868121. DOI: 10.1534/genetics.106.057141.
Robinson, M.R., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M., Kruuk, L.E. :
Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep. Evolution 60:2168-81, 2006. Pubmed reference: 17133873.
2004 Clutton-Brock, T., Pemberton, J. :
Soay sheep dynamics and selection in an island population. Cambridge University Press, Cambridge. :, 2004.
1997 Cluttonbrock, T.H., Wilson, K., Stevenson, I.R. :
Density-dependent selection on horn phenotype in soay sheep Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences 352:839-850, 1997.
1996 Montgomery, G.W., Henry, H.M., Dodds, K.G., Beattle, A.E., Wuliji, T., Crawford, A.M. :
Mapping the horns (ho) locus in sheep - a further locus controlling horn development in domestic animals Journal of Heredity 87:358-363, 1996. Pubmed reference: 8904835.
Picard, K., Festabianchet, M., Thomas, D. :
The cost of horniness - heat loss may counter sexual selection for large horns in temperate bovids Ecoscience 3:280-284, 1996.
Roberts, S.C. :
The evolution of hornedness in female ruminants [Review] Behaviour 133:399-442, 1996.
Vaiman, D., Koutita, O., Oustry, A., Elsen, J.M., Manfredi, E., Fellous, M., Cribiu, E.P. :
Genetic mapping of the autosomal region involved in XX sex-reversal and horn development in goats Mammalian Genome 7:133-137, 1996. Pubmed reference: 8835530.
1982 Tibau i Font, J., Lauvergne, J.J., Boitard, M., Bougler, J., Chabert, Y. :
[Inheritance of horns in sheep: a computer-generated microform bibliography] Bulletin Technique du Department de Genetique Animale :83 pp, 1982.
1970 Dolling, C.H.S. :
Breeding Merinos. Rigby Ltd, Adelaide. :, 1970.
1969 Singh, L.B., Dolling, C.H.S., Singh, O.N. :
Inheritance of horns and occurrence of cryptorchidism in indigenous, Rambouillet and crossbred sheep in India Australian Journal of Experimental Agriculture and Animal Husbandry 9:262-266, 1969.
1968 Dolling, C.H.S. :
Hornedness and polledness in sheep VI. The inheritance of polledness in the Border Leicester Australian Journal of Agricultural Research 19:649-655, 1968.
1961 Dolling, C.H.S. :
Hornedness and polledness in sheep. IV. Triple alleles affecting horn growth in the Merino Australian Journal of Agricultural Research 12:353-361, 1961.
Dolling, C.H.S., Carter, N.B. :
Hornedness and polledness in sheep. V. Some effects of the horn alleles on characters in the Merino Australian Journal of Agricultural Research 12:438-497, 1961.
1960 Dolling, C.H.S. :
Hornedness and polledness in sheep. II. The inheritance of horns in Merino ewes Australian Journal of Agricultural Research 11:618-627, 1960.
Dolling, C.H.S. :
Hornedness and polledness in sheep. I. The inheritance of polledness in the Merino Australian Journal of Agricultural Research 11:427-438, 1960.
Dolling, C.H.S. :
Hornedness and polledness in sheep. III. The inheritance of horns in Dorset Horn ewes Australian Journal of Agricultural Research 11:845-850, 1960.
1959 Dolling, C.H.S. :
The Poll Merino Journal of the Australian Institute of Agricultural Science 25:109-116, 1959.
1956 Dolling, C.H.S. :
The inheritance of horns in sheep Proceedings of the Australian Society of Animal Production 1:161-164, 1956.
1951 Kelley, R.B. :
Polledness in domestic animals with special reference to sheep. Aust Vet J 27:8-15, 1951. Pubmed reference: 14800845.
1940 Castle, W.E. :
Genetics of horns in sheep Journal of Heredity 31:486-487, 1940.
1912 Arkell, T.R., Davenport, C.B. :
Horns in sheep as a typical sex-limited character. Science 35:375-7, 1912. Pubmed reference: 17796242. DOI: 10.1126/science.35.897.375.
Arkell, T.R., Davenport, C.B. :
The nature of the inheritance of horns in sheep. Science 35:927, 1912. Pubmed reference: 17781688. DOI: 10.1126/science.35.911.927.
Castle, W.E. :
Are horns in sheep a sex-limited character? Science 35:574-5, 1912. Pubmed reference: 17817039. DOI: 10.1126/science.35.902.574.
1911 Castle, W.E. :
Heredity in Relation to Evolution and Animal Breeding. D. Appleton and Co., New York. :, 1911.

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