Our results represent the first study to systematically examine the genetic diversity and breed relationships of UK production-relevant native sheep breeds. They highlight intriguing, and previously unknown, genetic profiles. For example, the breeds associated with larger population size and production use such as the Easycare, Cheviot, Suffolk and Lleyn consistently show increased admixture and levels of genetic diversity, exhibit low degrees of genetic differentiation and have the lowest kinship co-efficients. These findings are unsurprising considering that these breeds are widely used in commercial sheep production in the UK. The strong genetic similarity among them may be attributed to shared breeding objectives that prioritise specific production relevant traits or the historical breeding relationships. Additionally, these breeds are primarily bred for economic productivity rather than for rare breed status. This means breeding practices within these breeds are likely to have a reduced emphasis on rigorous pedigree monitoring to maintain purebred animals and more crossbreeding with other commercial breeds.
In contrast, some of the less numerous native breeds demonstrated pronounced genetic differentiation, low levels of admixture, genetic diversity and higher inbreeding and within-breed relatedness. Our analysis has shown the genetics of the Wiltshire Horn to be particularly unique relative to the other breeds we investigated. The Wiltshire Horn breed is not on the UK BAR list but is considered relatively rare due to its limited population of fewer than 15,000 ewe (47). It was previously on the RBST watchlist. Our genetic diversity analysis consistently demonstrates that the breed forms a unique and isolated group, distinct from other breeds included in the study. Also, the breed exhibits no detectable admixture with other breeds across a range of estimated ancestral populations which strongly suggests that the Wiltshire Horn originated from a unique ancestral population. This is possibly attributable to the very diligent maintenance of genetic integrity in the breed by a handful of passionate breeders as well as the early implementation of thorough pedigree monitoring practices within the breed (Society). However, this breed also showed the lowest heterozygosity of all breeds in the study and high within-breed relatedness.
In both the PCA and neighbour-net graph the Border Leicester and Lincoln Longwool appeared to share a close genetic relationship. These are both ‘longwool’ breeds, which are some of the oldest documented UK breeds, with their ancestral types dating back to at least the Middle Ages (c. 500 to 1500 AD) (45). English Longwool rams were major founders of many contemporary British breeds, and both the Lincoln Longwool and the Border Leicester have the English Longwool as one of their founding varieties (45). The proximity of these breeds to the Ryeland is surprising, given that the Ryeland is an ancient short-wool breed, that has remained distinct. However, there is some suggestion that the noted 18th century breeder Robert Bakewell (48), folded the Border Leicester into the Ryeland (49), which may explain this result and also highlights the utility of genotyping to uncover poorly documented breed histories.
Interestingly the Norfolk Horn has maintained considerable genetic distinctiveness, even in the wake of historical backcrossing efforts with Suffolk sheep (50). Notably, these two breeds do not coalesce into a single group in the PCA space but the neighbour-net graph highlighted their historical relationship (Fig. 2A, 3). Throughout the 20th century, Norfolk Horns faced a decline in popularity, and by the First World War, only one flock of the breed remained (50). These surviving Norfolk Horns were characterised by extreme levels of inbreeding, rendering any attempts to expand the flock seemingly insurmountable. To tackle this, a back-crossing program using Suffolk sheep was initiated. The program spanned several decades. Today, there are over 2,500 Norfolk Horns in existence (51). This compelling evidence attests to the efficacy of the back-crossing program in rescuing the Norfolk Horn species while safeguarding the integrity of their unique genetic heritage. It serves as a resounding testament that well-planned and persistent interventions can combat the challenges posed by inbreeding.
Our examination of admixture in each of the breeds importantly showed that several of the breeds with increased admixture are the more numerous and commercially utilised breeds. For example, the Easycare, Cheviot, Lleyn and Suffolk breeds show more admixture than the Wiltshire Horn, Lincoln Longwool, Ryeland and Whiteface Woodland, all of which show no admixture. This observation aligns with the notion that these commercial breeds are likely to have been selectively bred for desirable commercial traits. The increased levels of admixture in these breeds are significant as it implies a greater genetic diversity within the breeds. This means they may have increased breed resilience and adaptability than the rarer breeds with lower levels of admixture. The low admixture in the rarer breeds underscores the importance of protecting these breeds from the negative consequences of inbreeding. Doing so is critical for preserving genetic heritage and breed purity.
The mean heterozygosity values recorded in this study (0.3 in the Wiltshire Horn to 0.44 in the Easycare) were similar to those observed for UK and European breeds in other studies e.g., Kijas et al. (2012)(29) who reported a range of 0.29–0.32. However, for some of the native UK breeds studied, including those listed on the UK BAR list, there are indications of potential inbreeding occurring, which could pose a significant threat to the long-term survival of these breeds. The Wiltshire Horn has the lowest value of heterozygosity of the sheep studied and highest average percentage of the genome in ROH (but with high within-breed variability). This is possibly due the small number of ewes that are registered annually for the breed (47) which can result in a smaller gene pool. Given the unique sustainable traits of the Wiltshire Horn, such as seasonal wool shedding, and its clear genetic distinctiveness from other breeds studied, this is particularly concerning.
The Norfolk Horn, another breed with unique traits and clear genetic distinctiveness from other breeds studied, also has particularly low values of heterozygosity. This is perhaps explainable by its historical bottle-neck in the 1970’s and subsequent rescue via crossing with the closely related Suffolk (50, 51). More generally, the trend is that the breeds on the UK BAR list, with smaller population sizes, appear to have lower levels of heterozygosity and subsequent greater degrees of inbreeding. Inbreeding elevates the risk of individuals inheriting two copies of recessive deleterious genes, which can have adverse effects, including reduced fertility(22). Considering the potential consequences, it is imperative to address the challenge of inbreeding to ensure breed preservation. Early detection of excessive inbreeding using genotyping tools can facilitate the implementation of well-designed breeding and cross-breeding programs, perhaps including importation of novel genetics from European flocks. Both the Oxford Down and the Whiteface Woodland, two BAR listed breeds, showed moderate-good levels of genetic diversity and (with the exception of a small number of outliers), low inbreeding. This demonstrates that small population size need not inevitably result in poor genetic diversity, as long as management strategies are sufficient to combat the effects of small numbers of breeding individuals. The findings of this study demonstrate that some degree of routine genotyping and comprehensive recording of easy to measure traits would be warranted particularly for the UK breeds on the BAR list.
This study represents an essential first step in the ongoing pursuit for more comprehensive genetic characterisation of native UK sheep breeds. Further research should obtain larger sample sizes for each breed and include several different flocks and geographical locations within the UK. Whole-genome sequencing, using short read Illumina data, would provide many million more SNPs for analysis and more accurate quantification of genetic diversity in UK native sheep breeds as well as identification of genetic markers driving traits of interest for breed improvement. From the whole genome sequencing data examination of runs of homozygosity and structural variants could also help to define the degree of inbreeding (52). WGS could also be used to validate the content on existing SNP chips or design new tools with content tailored specifically for UK sheep breeds, enhancing the precision of SNP genotyping and informing future breeding and cross-breeding programmes. Furthermore, global pangenome efforts for sheep to characterise and conserve global genomic diversity using long read genome sequencing technologies (53) should include the UK native breeds (6).