Genetic selection of athletic success in sport-hunting dogs

Abstract

Modern dogs are distinguished among domesticated species by the vast breadth of phenotypic variation produced by strong and consistent human-driven selective pressure. The resulting breeds reflect the development of closed populations with well-defined physical and behavioral attributes. The sport-hunting dog group has long been employed in assistance to hunters, reflecting strong behavioral pressures to locate and pursue quarry over great distances and variable terrain. Comparison of whole-genome sequence data between sport-hunting and terrier breeds, groups at the ends of a continuum in both form and function, reveals that genes underlying cardiovascular, muscular, and neuronal functions are under strong selection in sport-hunting breeds, including ADRB1, TRPM3, RYR3, UTRN, ASIC3, and ROBO1 We also identified an allele of TRPM3 that was significantly associated with increased racing speed in Whippets, accounting for 11.6% of the total variance in racing performance. Finally, we observed a significant association of ROBO1 with breed-specific accomplishments in competitive obstacle course events. These results provide strong evidence that sport-hunting breeds have been adapted to their occupations by improved endurance, cardiac function, blood flow, and cognitive performance, demonstrating how strong behavioral selection alters physiology to create breeds with distinct capabilities.

Keywords: athletic ability; positive selection; sport-hunting dogs; whole-genome sequencing.

Fig. 1.

Population structure of sport-hunting, terrier, and village dog populations. (A) Sport-hunting breeds pictured include (Left to Right) English Springer Spaniel, English Cocker Spaniel, German Wirehaired Pointer, and Irish Setter. Images, from left to right, courtesy of Katrine Bremser (photographer), Jillian Mennie (photographer), Flickr/Tommi Valtanen, and Flickr/Rongem Boyo. (B) Terrier breeds pictured include (Left to Right) Yorkshire Terrier, Kerry Blue Terrier, Airedale Terrier, and Border Terrier. Images, from left to right, courtesy of Flickr/Michelle Dudley, Gerry Yeager (photographer), Kay Nellis (photographer), and Flickr/Sophie Lowe. (C and D) Data from each individual sample are plotted along the two main principal components (PC1 and PC2) on three populations (C) and the first three principal components (PC1, PC2, and PC3) on sport-hunting and terrier populations (D). (E) Genome-wide LD was estimated in each group by calculating r² values between all pairs of SNVs with inter-SNV distances less than 10 Mb.

Fig. 2.

Evidence of positive selection in sport-hunting dogs (SH). (A) Flowchart of study design. (B) Maximum XP-EHH scores against maximum χ² of each 50-kb window. (C) The significant GO terms (P < 0.01) enriched from positively selected genes in sport-hunting dogs.

Fig. 3.

Signatures of the selective sweep at the ASIC3 gene region. (A) Structure of the ASIC3 gene with exons indicated by orange bars. A nonsynonymous SNV (C: ancestral and T: derived) is highlighted in yellow. Different colors represent distinct alleles, and the frequency of each haplotype is indicated on the right. (B) Nucleotide diversity plot of three populations around the ASIC3 gene region.

Fig. 4.

Signatures of the selective sweep at the CDH23 gene region. (A, Right) Structural and evolutionary analysis of the amino acid variant in CDH23. The orthologous protein sequences from mammals are aligned with the mutant residues shown in yellow. (Left) The neighbor-joining tree derived from the multiple sequence alignment. (B) Nucleotide diversity plot of three populations around the CDH23 gene region.

Fig. 5.

Association of ROBO1 allele frequency with the breed’s agility titles. Shown on the x axis are the eight breed groups stratified according to the total number of agility titles won by each breed, weighted by the total number of dogs registered for each breed. The allele frequency on the y axis was calculated for each group based on the allele selected in sport-hunting dogs. The number of dogs and breeds within each group are indicated below the graph.