Genotyping-By-Sequencing (GBS) Detects Genetic Structure and Confirms Behavioral QTL in Tame and Aggressive Foxes (Vulpes vulpes).

Jennifer L Johnson,Svetlana V Temnykh,Helena Wittgenstein,Sharon E Mitchell,Hiu Wa Flora Fong,Gregory M Acland,Katie E Hyma,Anastasiya V Vladimirova,Anastasiya V Kharlamova,Anna V Kukekova,Rimma G Gulevich,Lyudmila N Trut,William J Murphy

doi:10.1371/journal.pone.0127013

Abstract

The silver fox (Vulpes vulpes) offers a novel model for studying the genetics of social behavior and animal domestication. Selection of foxes, separately, for tame and for aggressive behavior has yielded two strains with markedly different, genetically determined, behavioral phenotypes. Tame strain foxes are eager to establish human contact while foxes from the aggressive strain are aggressive and difficult to handle. These strains have been maintained as separate outbred lines for over 40 generations but their genetic structure has not been previously investigated. We applied a genotyping-by-sequencing (GBS) approach to provide insights into the genetic composition of these fox populations. Sequence analysis of EcoT22I genomic libraries of tame and aggressive foxes identified 48,294 high quality SNPs. Population structure analysis revealed genetic divergence between the two strains and more diversity in the aggressive strain than in the tame one. Significant differences in allele frequency between the strains were identified for 68 SNPs. Three of these SNPs were located on fox chromosome 14 within an interval of a previously identified behavioral QTL, further supporting the importance of this region for behavior. The GBS SNP data confirmed that significant genetic diversity has been preserved in both fox populations despite many years of selective breeding. Analysis of SNP allele frequencies in the two populations identified several regions of genetic divergence between the tame and aggressive foxes, some of which may represent targets of selection for behavior. The GBS protocol used in this study significantly expanded genomic resources for the fox, and can be adapted for SNP discovery and genotyping in other canid species.

Highlights

The red fox (Vulpes vulpes) and the gray wolf (Canis lupus), both members of the Canidae family, diverged from a common ancestor approximately 10 million years ago [1, 2]
A total of 2,003,563 tags were identified and 1,530,295 (76.4%) of these aligned to single locations in the dog genome, 23,319 (1.2%) aligned to multiple positions, and 449,950 (22.5%) could not be aligned
The quantitative trait loci (QTL) analysis using this new VVU3 map did not identify any significant behavioral QTL in F2 pedigrees in the region of interest. These results suggest that the distal region on VVU3 may represent an example of random allele fixation in a closed population rather than a selective sweep associated with selection for behavior

Summary

Introduction

The red fox (Vulpes vulpes) and the gray wolf (Canis lupus), both members of the Canidae family, diverged from a common ancestor approximately 10 million years ago [1, 2]. The domestic dog (Canis lupus familiaris) is a recent descendant of the modern gray wolf ancestor and the only historically domesticated canid. A tame fox strain was produced from conventionally bred farm foxes by first eliminating fearful and aggressive animals from the breeding population and selecting for friendly behavior to humans [5, 8,9,10]. The tame strain foxes are eager to establish human contact and demonstrate friendly, playful behavior towards humans, paralleling the sociability of dog puppies. The tame population was maintained as a closed line and currently comprises approximately 300 breeding animals

Methods

Results

Conclusion