Edinburgh Research Explorer Scrapie-resistant sheep show certain coat colour characteristics Citation for published version: Sawalha, RM, Bell, L, Brotherstone, S, White, I, Wilson, AJ & Villanueva, B 2009, 'Scrapie-resistant sheep show certain coat colour characteristics', Genetics Research, vol. 91, no. 1, pp. 39-46. https://doi.org/10.1017/S0016672308009968 Digital Object Identifier (DOI): 10.1017/S0016672308009968 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: Genetics Research Publisher Rights Statement: RoMEO green General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 01. Oct. 2021 Genet. Res., Camb. (2009), 91, pp. 39–46. f 2009 Cambridge University Press 39 doi:10.1017/S0016672308009968 Printed in the United Kingdom Scrapie-resistant sheep show certain coat colour characteristics R. M. SAWALHA1*, L. BELL2,S.BROTHERSTONE3,I.WHITE3,A.J.WILSON3 AND B. VILLANUEVA1 1 Scottish Agricultural College, Sustainable Livestock Systems, West Mains Road, Edinburgh EH9 3JG, UK 2 Shetland Sheep Society, Caldronlea, Eaglesfield, Dumfriesshire DG11 3AQ, UK 3 Institute of Evolutionary Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK (Received 1 September 2008 and in revised form 24 November 2008) Summary Susceptibility to scrapie is known to be associated with polymorphisms at the prion protein (PrP) gene, and this association is the basis of current selective programmes implemented to control scrapie in many countries. However, these programmes might have unintended consequences for other traits that might be associated with PrP genotype. The objective of this study was to investigate the relationship between PrP genotype and coat colour characteristics in two UK native sheep breeds valued for their distinctive coat colour patterns. Coat colour pattern, darkness and spotting and PrP genotype records were available for 11 674 Badgerfaced Welsh Mountain and 2338 Shetland sheep. The data were analysed with a log–linear model using maximum likelihood. Results showed a strong significant association of PrP genotype with coat colour pattern in Badgerfaced Welsh Mountain and Shetland sheep and with the presence of white spotting in Shetland sheep. Animals with the ARR/ARR genotype (the most scrapie resistant) had higher odds of having a light dorsum and a dark abdomen than the reverse pattern. The implication of these associations is that selection to increase resistance to scrapie based only on PrP genotype could result in change in morphological diversity and affect other associated traits such as fitness. 1. Introduction et al., 2002). These programmes have increased the frequency of the ARR allele and reduced the fre- Scrapie is the sheep and goat form of transmissible quency of the VRQ allele (e.g. Warner et al., 2006), spongiform encephalopathy. Susceptibility to classi- but there is a risk that such selection may have nega- cal scrapie has been shown to be associated with five tive consequences on other valuable sheep character- alleles of the PrP gene (ARR, AHQ, ARH, ARQ and istics if the PrP gene has pleiotropic effects or is linked VRQ) that result from polymorphisms at codons 136, to genes affecting these characteristics. 154 and 171 (Goldmann et al., 1994; Hunter et al., Sweeney & Hanrahan (2008) reviewed recently 1996). While the ranking of these alleles with respect published studies of associations between PrP gene to scrapie susceptibility varies among breeds, the and commonly recorded performance traits in sheep ARR allele is generally considered as the most resist- and found no convincing evidence of associations ant and the VRQ allele as the most susceptible (Belt between PrP gene and most performance traits. et al., 1995; Baylis et al., 2004). Scrapie control pro- However, based on quantitative trait locus (QTL) and grammes are being implemented in many countries gene mapping studies, they suggested that possible based on selective breeding to eradicate those PrP associations with coat colour, health and survival alleles associated with scrapie susceptibility (Arnold traits are highly likely. Furthermore, some native UK sheep breeders have claimed that the most resistant PrP genotype (ARR/ARR) tends to be more frequent * Corresponding author. Sir Stephen Watson Building, Bush Estate, Penicuik, EH26 0PH, UK. e-mail: rami.sawalha@sac. in sheep with certain coat colour patterns (Bell et al., ac.uk 2005). Although the genetic basis of these putative R. M. Sawalha et al. 40 (a) (b) (c) (d) Fig. 1. Coat colour patterns in Badgerfaced Welsh Mountain and Shetland sheep. Torddu Welsh Mountain (a) and katmoget Shetland (c) are coat colour patterns with light colour on the dorsal and dark on the abdominal areas. Torwen Welsh Mountain (b) and gulmoget Shetland (d) are coat colour patterns with dark colour on the dorsal and light on the abdominal areas. associations is unknown, one of the major genes phenotypes of coat colour pattern, colour darkness controlling coat colour pattern, the Agouti gene, is and spotting were tested. located on the same chromosome as the PrP gene (Parsons et al., 1999b; Beraldi et al., 2006) such that 2. Materials and methods linkage disequilibrium between Agouti and PrP is possible. Coat characteristics (colour pattern, colour darkness Coat characteristics such as colour and pattern are and spotting) and PrP genotype data were obtained linked to fitness in wild mammalian populations for animals of two native breeds of sheep (Badger- (Moorcroft et al., 1996; Hoekstra & Nachman, 2003; faced Welsh Mountain and Shetland), raised on com- Gratten et al., 2008), and are also of economic im- mercial farms. Information on the sex, age and farm portance in wool-producing sheep breeds (Renieri was also available. Badgerfaced Welsh Mountain et al., 2008). Also, coat characteristics constitute a animals have two colour patterns named the ‘torddu’ major factor in breed characterization of native sheep (light dorsal and dark abdominal areas) and the breeds (Klungland & Va˚ ge, 2003; Beraldi et al., 2006). ‘torwen’ (dark dorsal and light abdominal areas) as In fact, it is precisely the phenotypic diversity found shown in Fig. 1a and b. within these breeds that makes them of interest to Shetland sheep are more phenotypically diverse, breeders and conservationists. Consequently, any loss based on coat characteristics. Animals with white, of diversity associated with selection on PrP genotype grey,‘katmoget’,‘gulmoget’,darkbrown,lightbrown, could have serious implications for their future exist- black and spotted coats were all present in the data. ence. Here, the objective is to investigate whether The katmoget and gulmoget patterns (Fig. 1c and d) selective breeding for scrapie eradication purposes correspond, respectively, to the torddu and the tor- could lead to a change in phenotypic diversity for wen patterns of Badgerfaced Welsh Mountain sheep. coat characteristics in two native UK sheep breeds. Spotting is defined as having white spots on a col- To do this, associations between PrP genotypes and oured background coat. PrP genotype and coat colour in sheep 41 Coat pattern is under combined non-epistatic con- Table 1. Distribution of Badgerfaced Welsh trol of both the Agouti and the Extension genes (Va˚ ge Mountain animals (and expected numbers) by et al., 2003). Coat colour darkness (dark versus light) PrP genotype and coat colour patterna has been shown to be under the control of the Brown gene (Beraldi et al., 2006). Spotting is believed to be Coat colour patternb controlled by the Spotting gene (Renieri et al., 2008). Shetland sheep were thus classified based on the cur- Genotype Torddu Torwen rently known underlying inheritance of coat colour ARR/ARR 3088 (2726.10) 405 (766.88) variations into (i) five categories for coat colour pat- ARR/AHQ 1460 (1382.20) 311 (388.82) tern (white, grey, katmoget, gulmoget and solid); (ii) ARR/ARQ 2499 (2520.90) 731 (709.14) two categories for coat colour darkness classes (dark ARR/VRQ 334 (397.25) 175 (111.75) . brown and light brown); and (iii) two categories for AHQ/AHQ 213 (211 50) 58 (59 497) AHQ/ARQ 638 (710.99) 273 (200.01) white spotting (spotted and non-spotted). The cat- AHQ/VRQ 82 (119.41) 71 (33.591) egory ‘solid’ for coat colour pattern included animals ARQ/ARQ 636 (771.09) 352 (216.91) with light brown, dark brown and black coats. ARQ/VRQ 143 (233.36) 156 (65.645) Animals with spotted coats were excluded from coat VRQ/VRQ 18 (38.242) 31 (10.758) colour pattern classification. The category ‘non- Total 9111 2563 spotted’ included animals with grey, katmoget, gul- moget, dark brown, light brown and black coats. a Expected numbers were calculated assuming no associ- Animals with white coat colour were not scored for ation between PrP genotypes and different coat colours spotting since white spots cannot be observed in white classes. b Torddu: light colour on the dorsal and dark on the ab- animals. dominal areas; torwen: dark colour on the dorsal and light The farmers obtained the PrP genotype of the ani- on the abdominal areas. mals in the dataset through participation in the Ram Genotyping Scheme of the National Scrapie Plan for farm where an animal was kept nor the interaction Great Britain, in the Rare Breeds Survival Trust between farm and PrP genotype were statistically Genotype Survey (UK) or through private initiatives.