A linkage map for brown trout (Salmo trutta): chromosome homeologies and comparative genome organization with other salmonid fish.

We report on the construction of a linkage map for brown trout (Salmo trutta) and its comparison with those of other tetraploid-derivative fish in the family Salmonidae, including Atlantic salmon (Salmo salar), rainbow trout (Oncorhynchus mykiss), and Arctic char (Salvelinus alpinus). Overall, we identified 37 linkage groups (2n = 80) from the analysis of 288 microsatellite polymorphisms, 13 allozyme markers, and phenotypic sex in four backcross families. Additionally, we used gene-centromere analysis to approximate the position of the centromere for 20 linkage groups and thus relate linkage arrangements to the physical morphology of chromosomes. Sex-specific maps derived from multiple parents were estimated to cover 346.4 and 912.5 cM of the male and female genomes, respectively. As previously observed in other salmonids, recombination rates showed large sex differences (average female-to-male ratio was 6.4), with male crossovers generally localized toward the distal end of linkage groups. Putative homeologous regions inherited from the salmonid tetraploid ancestor were identified for 10 pairs of linkage groups, including five chromosomes showing evidence of residual tetrasomy (pseudolinkage). Map alignments with orthologous regions in Atlantic salmon, rainbow trout, and Arctic char also revealed extensive conservation of syntenic blocks across species, which was generally consistent with chromosome divergence through Robertsonian translocations.

A comparative analysis of the rainbow trout genome with 2 other species of fish (Arctic charr and Atlantic salmon) within the tetraploid derivative Salmonidae family (subfamily: Salmoninae).

We updated the genetic map of rainbow trout (Oncorhynchus mykiss) for 2 outcrossed mapping panels, and used this map to assess the putative chromosome structure and recombination rate differences among linkage groups. We then used the rainbow trout sex-specific maps to make comparisons with 2 other ancestrally polyploid species of salmonid fishes, Arctic charr (Salvelinus alpinus) and Atlantic salmon (Salmo salar) to identify homeologous chromosome affinities within each species and ascertain homologous chromosome relationships among the species. Salmonid fishes exhibit a wide range of sex-specific differences in recombination rate, with some species having the largest differences for any vertebrate species studied to date. Our current estimate of female:male recombination rates in rainbow trout is 4.31:1. Chromosome structure and (or) size is associated with recombination rate differences between the sexes in rainbow trout. Linkage groups derived from presumptive acrocentric type chromosomes were observed to have much lower sex-specific differences in recombination rate than metacentric type linkage groups. Arctic charr is karyotypically the least derived species (i.e., possessing a high number of acrocentric chromosomes) and Atlantic salmon is the most derived (i.e., possessing a number of whole-arm fusions). Atlantic salmon have the largest female:male recombination ratio difference (i.e., 16.81:1) compared with rainbow trout, and Arctic charr (1.69:1). Comparisons of recombination rates between homologous segments of linkage groups among species indicated that when significant experiment-wise differences were detected (7/24 tests), recombination rates were generally higher in the species with a less-derived chromosome structure (6/7 significant comparisons). Greater similarity in linkage group syntenies were observed between Atlantic salmon and rainbow trout, suggesting their closer phylogenetic affinities, and most interspecific linkage group comparisons support a model that suggests whole chromosome arm translocations have occurred in the evolution of this group. However, some possible exceptions were detected and these findings are discussed in relation to their influence on segregation distortion patterns. We also report unusual meiotic segregation patterns in a female parent involving the duplicated (homeologous) linkage group pair 12/16 and discuss several models that may account for these patterns.

Comparative genome analysis of the primary sex-determining locus in salmonid fishes.

We compared the Y-chromosome linkage maps for four salmonid species (Arctic charr, Salvelinus alpinus; Atlantic salmon, Salmo salar; brown trout, Salmo trutta; and rainbow trout, Oncorhynchus mykiss) and a putative Y-linked marker from lake trout (Salvelinus namaycush). These species represent the three major genera within the subfamily Salmoninae of the Salmonidae. The data clearly demonstrate that different Y-chromosomes have evolved in each of the species. Arrangements of markers proximal to the sex-determining locus are preserved on homologous, but different, autosomal linkage groups across the four species studied in detail. This indicates that a small region of DNA has been involved in the rearrangement of the sex-determining region. Placement of the sex-determining region appears telomeric in brown trout, Atlantic salmon, and Arctic charr, whereas an intercalary location for SEX may exist in rainbow trout. Three hypotheses are proposed to account for the relocation: translocation of a small chromosome arm; transposition of the sex-determining gene; or differential activation of a primary sex-determining gene region among the species.