A dense linkage map for Chinook salmon (Oncorhynchus tshawytscha) reveals variable chromosomal divergence after an ancestral whole genome duplication event

Abstract

Comparisons between the genomes of salmon species reveal that they underwent extensive chromosomal rearrangements following whole genome duplication that occurred in their lineage 58-63 million years ago. Extant salmonids are diploid, but occasional pairing between homeologous chromosomes exists in males. The consequences of re-diploidization can be characterized by mapping the position of duplicated loci in such species. Linkage maps are also a valuable tool for genome-wide applications such as genome-wide association studies, quantitative trait loci mapping or genome scans. Here, we investigated chromosomal evolution in Chinook salmon (Oncorhynchus tshawytscha) after genome duplication by mapping 7146 restriction-site associated DNA loci in gynogenetic haploid, gynogenetic diploid, and diploid crosses. In the process, we developed a reference database of restriction-site associated DNA loci for Chinook salmon comprising 48528 non-duplicated loci and 6409 known duplicated loci, which will facilitate locus identification and data sharing. We created a very dense linkage map anchored to all 34 chromosomes for the species, and all arms were identified through centromere mapping. The map positions of 799 duplicated loci revealed that homeologous pairs have diverged at different rates following whole genome duplication, and that degree of differentiation along arms was variable. Many of the homeologous pairs with high numbers of duplicated markers appear conserved with other salmon species, suggesting that retention of conserved homeologous pairing in some arms preceded species divergence. As chromosome arms are highly conserved across species, the major resources developed for Chinook salmon in this study are also relevant for other related species.

Keywords: Chinook salmon; RAD sequencing; chromosome homeologies; linkage map; whole genome duplication.

Figure 1

Consensus Chinook salmon female linkage map—34 linkage groups corresponding to the 34 Chinook salmon chromosomes. Ots01 to Ots16 are metacentric; Ots17 to Ots34 are acrocentric. The size of each linkage group varies from 58 to 173.2 cM. Each line corresponds to the location of one or more markers. The centromere is represented in pink. All the chromosomes are oriented with the shorter arm (p arm) before the centromere, longer arm (q arm) after the centromere.

Figure 2

Percentage of heterozygous offspring in the gynogenetic diploid crosses along three acrocentric chromosomes where the p arm has been identified: Ots19, Ots20, and Ots33. On the x-axis, the distances are oriented from the p arm. Three gynogenetic crosses were used (F978, F981, and F984). The centromere is located where the percentage of heterozygous offspring is about zero.

Figure 3

Marker distribution across all chromosome arms, examined separately for all chromosomes, metacentric chromosomes, and acrocentric chromosomes (including the p arm or not for Ots19, Ots20, and Ots 33). Distances on the x-axis are represented as the relative distance from the center of the centromeric region.

Figure 4

Number of markers on each linkage group, designated by chromosome arm. Non-duplicated loci (RAD loci or SNP loci) are represented by the white bars; Duplicated loci are represented by the light gray bars (loci with only one paralog polymorphic) or dark gray bars (both paralogs polymorphic).

Figure 5

Proportion of duplicated and non-duplicated loci along the 16 linkage groups (denoted by chromosome number) with a high number of duplicated loci. Non-duplicated loci are represented in white; Duplicated loci are represented in gray (loci with one paralog polymorphic) or in dark gray (loci with both paralogs polymorphic). The centromere is represented by the cross-hatched area. All chromosomes are oriented with the short arm (p) on the left where relevant.

Figure 6

Linkage map for Ots16, denoting loci that are homologous with rainbow trout. Loci in common between the two species are underlined and the position on the rainbow trout map is indicated on the left of the chromosome (WS: linkage groups from Miller et al. 2012; Omy: rainbow trout chromosomes). The centromere is represented in gray. The chromosome is oriented with the p arm on top and the q arm at the bottom. Distances are in centimorgans.