A meiotic linkage map of the silver fox, aligned and compared to the canine genome

Abstract

A meiotic linkage map is essential for mapping traits of interest and is often the first step toward understanding a cryptic genome. Specific strains of silver fox (a variant of the red fox, Vulpes vulpes), which segregate behavioral and morphological phenotypes, create a need for such a map. One such strain, selected for docility, exhibits friendly dog-like responses to humans, in contrast to another strain selected for aggression. Development of a fox map is facilitated by the known cytogenetic homologies between the dog and fox, and by the availability of high resolution canine genome maps and sequence data. Furthermore, the high genomic sequence identity between dog and fox allows adaptation of canine microsatellites for genotyping and meiotic mapping in foxes. Using 320 such markers, we have constructed the first meiotic linkage map of the fox genome. The resulting sex-averaged map covers 16 fox autosomes and the X chromosome with an average inter-marker distance of 7.5 cM. The total map length corresponds to 1480.2 cM. From comparison of sex-averaged meiotic linkage maps of the fox and dog genomes, suppression of recombination in pericentromeric regions of the metacentric fox chromosomes was apparent, relative to the corresponding segments of acrocentric dog chromosomes. Alignment of the fox meiotic map against the 7.6x canine genome sequence revealed high conservation of marker order between homologous regions of the two species. The fox meiotic map provides a critical tool for genetic studies in foxes and identification of genetic loci and genes implicated in fox domestication.

Figure 1.

Integrated meiotic linkage map of the silver fox (Vulpes vulpes). Each linkage group corresponding to a fox chromosome (VVU1 through VVU16 and VVUX) is presented on the left side of each panel and aligned with the corresponding segments of the 7.6x dog genome sequence (CanFam2.0). Lines connect markers mapped onto the fox meiotic linkage map and identified in the assembly of the dog genome. Markers in plain format map to unique locations with confidence ≥1000:1 (LOD ≥3.0). Boxed markers were placed to unique locations with confidence ≥100:1 (LOD ≥2). Markers in italics are drawn in their most likely position, determined at the latter confidence threshold. Genetic distances between markers were calculated using the Kosambi mapping function. In general, most dog chromosomes each map to a single fox chromosome. Dog chromosomes which have their homologs divided among more than one fox chromosome are marked by asterisks (*) (see VVU1, 2, 4, 5, and 13). Dog chromosomal segments for which the orientation on the fox meiotic map was reversed compared to the orientation reported in previous cytogenetic studies (Graphodatsky et al. 2002) are marked by dots (●) (see VVU3, 4, 6, 8, and 12). Centromere positions of dog chromosomes are indicated in accordance with the dog genome sequence, assuming that the centromere is located at the beginning of each chromosome. Where different fragments of a single dog chromosome correspond to different fox chromosomal segments, a tilde (∼) indicates the breakage point along the dog chromosome. Positions of markers in the dog sequence are indicated in accordance with the CanFam2.0 assembly, except for REN315H04 and AHTH91. In the present study, marker REN315H04 mapped to VVU2 in a region corresponding to CFA2, which is in agreement with the Breen et al. (2001) and Guyon et al. (2003) canine maps, and CanFam1.0 assembly of the canine genome (chr2:84,742,789–84,742,951). The CanFam2.0 assembly, however, locates REN315H04 on CFA9 (chr9:21,100,622–21,100,777). Marker AHTH91 was identified only in the CanFam1.0 assembly.

Figure 2.

Comparisons of recombination rates between fox and dog chromosomes. Each point on the graph represents the ratio (fox to dog) of the recombination distances between a pair of markers mapped in both the fox and the dog (fox and dog distances between these markers and recombination ratios are presented in Supplemental Table 2). Points connected by a line correspond to a single dog chromosome. Arrows indicate putative centromere positions of fox chromosomes. Relative recombination suppression (ratio <1.0) is evident in the pericentromeric region of several fox chromosomes.