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Selection in the Finnhorse, a Native All‐Around Horse Breed

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Selection in the Finnhorse, a Native All‐Around Horse Breed Received: 24 August 2020 | Revised: 20 October 2020 | Accepted: 1 November 2020 DOI: 10.1111/jbg.12524 ORIGINAL ARTICLE Selection in the Finnhorse, a native all-around horse breed Laura Kvist1 | Johanna Honka1 | Markku Niskanen2 | Oona Liedes1 | Jouni Aspi1 1Department of Ecology and Genetics, University of Oulu, Oulu, Finland Abstract 2Research Unit of History, Culture and Selection by breeders modifies the morphology, behaviour and performance of do- Communications, University of Oulu, Oulu, mesticated species. Here, we examined signs of selection in Finnhorse, the only na- Finland tive horse breed in Finland. We first searched divergent genomic regions between Correspondence Finnhorses and other breeds, as well as between different breeding sections of the Laura Kvist, Department of Ecology and Finnhorse with data from Illumina Equine SNP70 BeadChip, and then studied sev- Genetics, University of Oulu, POB 8000, eral of the detected regions in more detail. We found altogether 35 common outlier 90014 Oulu, Finland. Email: [email protected] SNPs between Finnhorses and other breeds using two different selection tests. Many of the SNPs were located close to genes affecting coat colour, performance, size, Funding information Suomen Kulttuurirahasto sugar metabolism, immune response and olfaction. We selected genes affecting coat colour (KIT, MITF, PMEL), performance (MSTN) and locomotion (DMRT3) for a more detailed examination. In addition, we looked for, and found, associations with height at withers and SNPs located close to gene LCORL. Among the four breeding sections of Finnhorses (harness trotters, riding horses, draught horses and pony-sized horses), a single SNP located close to the DMRT3 gene was significantly differenti- ated and only between harness trotters and pony-sized horses. KEYWORDS coat colour, locomotion, outlier SNP, size at withers, whole-genome analysis 1 | INTRODUCTION due to artificial diversifying selection. Examples of large phenotypic differences between breeds and between wild and Domestication fundamentally changes the behaviour, mor- domesticated animals are the huge variations in coat colour phology, physiology and performance of animal species (Cieslak et al., 2011) or body size (e.g., in dogs, Canis lupus through selective breeding—breeders’ decisions of which familiaris; Beale & Ostrander, 2012), which are common in individuals will be allowed to reproduce. This artificial se- domesticated species, but often show limited variation within lection is often directional, decreasing the amount of genetic breeds. Thus, captive breeding may on the one hand decrease diversity within breeds. Genetic diversity can decrease also overall phenotypic and genetic variation and on the other because of fixation of breed-specific traits through inbreed- hand increase it for certain traits. ing, genetic drift and founder effect (Frantz et al., 2020; Horses (Equus caballus) have been selectively bred for Mignon-Grasteau et al., 2005). On the other hand, different centuries, especially for transportation, agriculture and breeds of a given domesticated species can vary considerably warfare, nowadays mainly for leisure and sports activities. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Journal of Animal Breeding and Genetics published by John Wiley & Sons Ltd 188 | wileyonlinelibrary.com/journal/jbg J Anim Breed Genet. 2021;138:188–203. KVIST ET AL. | 189 Schubert et al. (2014) identified altogether 125 genomic re- favouring of draft-type phenotypes since 1907 had already gions, which have potentially been affected by the domesti- largely depleted suitable breeding material for light horses cation process in the horse. They classified these regions into (Ojala et al., 2007), and in the late 1940s, it was actually two groups, of which the first consisted of genes involved noted that the overall suitability of the Finnhorse for riding in muscular and limb development, articular junctions and had deteriorated over time (Ojala, 1997, 2007). The light- the cardiac system (physiological adaptations), and the sec- type horse section that included also Finnhorses competing ond consisted of genes with cognitive functions (tameness). in harness trotting was renamed as the universal horse section Several of the genomic changes accompanying domestica- in 1935 and was replaced by a trotting horse section in 1965 tion have indeed been related to forelimb robustness, perfor- (Ojala, 1997; Ojala et al., 2007). mance, gaits, cognitive skills and behaviour, but also to coat Since 1971, Finnhorses have been bred in four breeding colour, many of which support the “neural crest hypothesis sections: harness trotters, riding horses, pony-sized horses for domestication” (Librado et al., 2017; Ludwig et al., 2009; and draught horses. Horses of each breeding section need Petersen, Mickelson, Rendahl, et al., 2013); that is, develop- to fill section-specific criteria for acceptance to a breed- ment of number of these traits is linked to neural crest cells ing section. This has brought additional selection for traits (Wilkins et al., 2014). Much research has recently focused on specific to these breeding sections (e.g., performance, gait, these traits in horses, especially on genes affecting colour, size and conformation; Ojala, 2007). Registered Finnhorses gait patterns and performance (reviewed, e.g., in Raudsepp form a common gene pool, from which new horses can be et al., 2019). Connected with the “neural crest hypothesis of accepted to a breeding section after individual evaluation. domestication,” mutations in genes affecting tissues originat- Thus, a given horse can belong to several breeding sections ing from the neural crest cells have been found also to cause and offspring do not automatically belong to the breeding several diseases. Such diseases are, for example, the lethal section(s) of their parents (The Finnish Trotting and Breeding white syndrome and stationary night blindness in horses Association, 2017). Most Finnhorses are not evaluated and do (Metallinos et al., 1998; Raudsepp et al., 2019), which af- not belong to any of the breeding sections. This likely leads to fect also coat colour. In general, genetic load in horses has a quite weak effect of selection within the breeding sections. increased and diversity decreased especially during the last The studbook has been closed for 110 years and provides couple of hundreds of years, due to modern breeding prac- pedigrees and much of other information of all Finnhorses tices (Fages et al., 2019; Raudsepp et al., 2019). (The Finnish Trotting and Breeding Association, 2017). Finnhorse as a breed was officially founded with the es- Recent analyses of genomic SNPs and mitochondrial DNA tablishment of the studbook in 1907. We refer native horses in Finnhorses showed that mitochondrial genetic diversity and of Finland predating this year as Finnish horses. These female effective populations sizes are high (Kvist et al., 2019), Finnish horses formed three main types in the early 20th which is common for all horse breeds (e.g., Jansen et al., 2002; century: (a) heavy horses used in agriculture; (b) lightly Raudsepp et al., 2019). On the other hand, effective population built and “leggy” horses used in harness racing; and (c) rela- size (Ne) from the nuclear SNP data was just about 50 for each tively light, pony-sized horses, in addition to local landraces. of the breeding sections and for the breed as a whole (Kvist The breed was strongly selected for colour and size in the et al., 2019). For comparison, Ne calculated from genome-wide early years. Only horses representing the heavy type were SNP data from close to 40 breeds varied between 143 and 751 accepted in the studbook between 1907 and 1924, because (Petersen, Mickelson, Cothran, et al., 2013), and in several agriculture and forestry required draft-type horses. However, native breeds with small populations, Ne was considerably as trotting speed was desired in addition to weight pulling, smaller (e.g., 41 in South Korean Jeju horses; Do et al., 2014, most stallions represented a light-draft phenotype. Accepted 39 in Italian Bardigiano horses; Ablondi et al., 2020, and stallions had to be at least 148 cm tall at the withers (Ojala 40–85 in several native Polish breeds; Jasielczuk et al., 2020). et al., 2007; Peltonen, 2014). There was also intense selection Based on inbreeding coefficients and number of runs of homo- for colour, with chestnuts strongly favoured, and “foreign” zygosity (ROHs), inbreeding has not been very high compared colours (white, grey, palomino and piebald) not accepted. In with other breeds, but ROHs were on average longer than in 1871, only about 23% of the Finnish horses were chestnuts, several other breeds (Kvist et al., 2019). There are not many contrary to 1920, during which over 85% of the Finnhorses studies of specific phenotypic or genotypic traits in Finnhorses. accepted to the studbook were chestnuts (Perttunen, 2007). However, a few reports based on pedigree analyses and infor- Due to the Finnish military's need for riding horses, the mation from studbook have shown that size is positively cor- Finnhorse studbook was divided into two sections in 1924, related with racing performance and has a high heritability, heavier draft-type horses and light-type riding horses. Light whereas correlation of body conformation with
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