title: Diversifying Selection Between Pure-Breed and Free-Breeding Dogs Inferred from Genome-Wide SNP Analysis.
abstract: Domesticated species are often composed of distinct populations differing in the character and strength of artificial and natural selection pressures, providing a valuable model to study adaptation. In contrast to pure-breed dogs that constitute artificially maintained inbred lines, free-ranging dogs are typically free-breeding, i.e., unrestrained in mate choice. Many traits in free-breeding dogs (FBDs) may be under similar natural and sexual selection conditions to wild canids, while relaxation of sexual selection is expected in pure-breed dogs. We used a Bayesian approach with strict false-positive control criteria to identify FST-outlier SNPs between FBDs and either European or East Asian breeds, based on 167,989 autosomal SNPs. By identifying outlier SNPs located within coding genes, we found four candidate genes under diversifying selection shared by these two comparisons. Three of them are associated with the Hedgehog (HH) signaling pathway regulating vertebrate morphogenesis. A comparison between FBDs and East Asian breeds also revealed diversifying selection on the BBS6 gene, which was earlier shown to cause snout shortening and dental crowding via disrupted HH signaling. Our results suggest that relaxation of natural and sexual selection in pure-breed dogs as opposed to FBDs could have led to mild changes in regulation of the HH signaling pathway. HH inhibits adhesion and the migration of neural crest cells from the neural tube, and minor deficits of these cells during embryonic development have been proposed as the underlying cause of "domestication syndrome." This suggests that the process of breed formation involved the same genetic and developmental pathways as the process of domestication.
authors.affiliation: School of Life Sciences, University of Lincoln, Lincolnshire, LN6 7DL, UK Museum and Institute of Zoology, Polish Academy of Sciences, 00-679 Warszawa, Poland.
authors.forename: Małgorzata
authors.identifier: 0000-0002-6057-5768
authors.initials: M
authors.lastname: Pilot
authors.affiliation: Museum and Institute of Zoology, Polish Academy of Sciences, 00-679 Warszawa, Poland.
authors.forename: Tadeusz
authors.identifier: 0000-0001-8061-435X
authors.initials: T
authors.lastname: Malewski
authors.affiliation: School of Life Sciences, University of Lincoln, Lincolnshire, LN6 7DL, UK.
authors.forename: Andre E
authors.identifier: 0000-0003-2140-0196
authors.initials: AE
authors.lastname: Moura
authors.affiliation: Division of Molecular and Forensic Genetics, Department of Forensic Medicine, Ludwik Rydygier Collegium Medicum, Nicolaus Copernicus University, 85-094 Bydgoszcz, Poland.
authors.forename: Tomasz
authors.initials: T
authors.lastname: Grzybowski
authors.affiliation: Department of Animal Genetics, University of Warmia and Mazury, 10-711 Olsztyn, Poland.
authors.forename: Kamil
authors.identifier: 0000-0002-5538-1352
authors.initials: K
authors.lastname: Oleński
authors.affiliation: Department of Animal Genetics, University of Warmia and Mazury, 10-711 Olsztyn, Poland.
authors.forename: Stanisław
authors.initials: S
authors.lastname: Kamiński
authors.affiliation: School of Life Sciences, University of Lincoln, Lincolnshire, LN6 7DL, UK.
authors.forename: Fernanda Ruiz
authors.identifier: 0000-0002-1173-1728
authors.initials: FR
authors.lastname: Fadel
authors.affiliation: Department of Zoology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia.
authors.forename: Abdulaziz N
authors.identifier: 0000-0002-9733-4220
authors.initials: AN
authors.lastname: Alagaili
authors.affiliation: Department of Zoology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia.
authors.forename: Osama B
authors.initials: OB
authors.lastname: Mohammed
authors.affiliation: Museum and Institute of Zoology, Polish Academy of Sciences, 00-679 Warszawa, Poland wieslawb@miiz.waw.pl.
authors.forename: Wiesław
authors.identifier: 0000-0003-1196-2494
authors.initials: W
authors.lastname: Bogdanowicz
mesh_terms: D000818:Animals; D001499:Bayes Theorem; D001947:Breeding; D004285:Dogs; D000071278:Domestication; D014644:Genetic Variation; D016678:Genome; D055106:Genome-Wide Association Study; D005838:Genotype; D053823:Hedgehog Proteins / Q000235:genetics*; D009432:Neural Crest / Q000254:growth & development; D010641:Phenotype; D020641:Polymorphism, Single Nucleotide / Q000235:genetics; D012641:Selection, Genetic / Q000235:genetics*; D013045:Species Specificity
chemical_list: D053823:Hedgehog Proteins
keywords: Canis lupus familiaris; Hedgehog signaling pathway; artificial selection; diversifying selection; domestication syndrome