Date Published: January 30, 2019
Publisher: Public Library of Science
Author(s): Artur Gurgul, Igor Jasielczuk, Ewelina Semik-Gurgul, Klaudia Pawlina-Tyszko, Monika Stefaniuk-Szmukier, Tomasz Szmatoła, Grażyna Polak, Iwona Tomczyk-Wrona, Monika Bugno-Poniewierska, Juan J Loor.
The genetic differentiation of the current horse population was evolutionarily created by natural or artificial selection which shaped the genomes of individual breeds in several unique ways. The availability of high throughput genotyping methods created the opportunity to study this genetic variation on a genome-wide level allowing detection of genome regions divergently selected between separate breeds as well as among different horse types sharing similar phenotypic features. In this study, we used the population differentiation index (FST) that is generally used for measuring locus-specific allele frequencies variation between populations, to detect selection signatures among six horse breeds maintained in Poland. These breeds can be classified into three major categories, including light, draft and primitive horses, selected mainly in terms of type (utility), exterior, performance, size, coat color and appearance. The analysis of the most pronounced selection signals found in this study allowed us to detect several genomic regions and genes connected with processes potentially important for breed phenotypic differentiation and associated with energy homeostasis during physical effort, heart functioning, fertility, disease resistance and motor coordination. Our results also confirmed previously described association of loci on ECA3 (spanning LCORL and NCAPG genes) and ECA11 (spanning LASP1 gene) with the regulation of body size in our draft and primitive (small size) horses. The efficiency of the applied FST-based approach was also confirmed by the identification of a robust selection signal in the blue dun colored Polish Konik horses at the locus of TBX3 gene, which was previously shown to be responsible for dun coat color dilution in other horse breeds. FST-based method showed to be efficient in detection of diversifying selection signatures in the analyzed horse breeds. Especially pronounced signals were observed at the loci responsible for fixed breed-specific features. Several candidate genes under selection were proposed in this study for traits selected in separate breeds and horse types, however, further functional and comparative studies are needed to confirm and explain their effect on the observed genetic diversity of the horse breeds.
The present horse population abounds in the variety of phenotypes resulting mainly from selective breeding directed at improvement of particular phenotypic features. Since the domestication, various selection criteria aimed towards the improvement of horse usability in transportation, agriculture or horsemanship have been applied [1–2]. This drove the specialization of particular populations in terms of utility and finally resulted in a creation of formal breeds constituting largely closed populations with high genetic uniformity of individuals within breeds . The current selection in the most of horse breeds is primarily directed at the improvement of traits connected with appearance and performance. However, apart from the highly specialized breeds, there are also horse populations which are valued for their primitive nature manifesting in their robust constitution for primitive living conditions . These horse populations were mainly shaped by natural selection, however, selective breeding for breed standard and mating in closed populations makes their genetic characteristics largely similar to that found in other horse breeds.
In this study we performed a genome-wide scan for diversifying selection signatures in horse breeds representing performance, exterior and size selected animals. As a comparative population we included primitive, extensively selected horses with well-developed primitive characteristics like: good fertility, disease resistance and adaptation to harsh environmental conditions . Many genome regions divergently selected between separate breeds were identified in this study as well as selection signatures characteristic for specific horse types (light, draft and primitive). This allowed for an identification of several candidate genes and associated metabolic pathways which may be potentially responsible for the divergent phenotypes of the studied breeds. To allow comprehensive analysis of the obtained results we focused only on the genome regions with the strongest selection signals, presumably being near fixation in separate breeds and spanning variants responsible for the well-established (fixed) breed-specific traits. To manage a variety of genes found within the selection signals we performed a pathways analysis aimed at the identification of enriched processes. Having in mind that the detected selection signatures are associated with a variety of phenotypic features differentiating the studied breeds (which are conditioned by complex molecular mechanisms), we expected only very few genes connected with separate biological processes in the enrichment analysis. Nevertheless, this analysis allowed us to reduce the complexity of the obtained data and allowed us to search for the pathways and underlying genes potentially being the targets of diversifying selection.
Summarizing, in this study we applied a population differentiation-based approach to detect genomic regions divergently selected between six breeds representing light, draft and primitive horses. The analysis of the most pronounced selection signals allowed us to detect several genes connected with processes potentially important for breeds phenotypic differentiation and associated with energy homeostasis during physical effort, heart functioning, neuron development, fertility, disease resistance and motor coordination. All these processes are potentially important for the traits selected in the analyzed breeds, especially for athletic performance, health and gait quality. Our results also confirmed the previously described association of loci on ECA3 and ECA11 with the regulation of body size in our draft and primitive (small size) horses. The efficiency of the applied statistical approach was also confirmed by the identification of a strong selection signal in the blue dun Polish Konik horse at the locus of TBX3 gene, which was previously shown to be causative for dun coat color dilution.