Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

Abstract

Whole genome duplication has been implicated in evolutionary innovation and rapid diversification. In salmonid fishes, however, whole genome duplication significantly pre-dates major transitions across the family, and re-diploidization has been a gradual process between genomes that have remained essentially collinear. Nevertheless, pairs of duplicated chromosome arms have diverged at different rates from each other, suggesting that the retention of duplicated regions through occasional pairing between homeologous chromosomes may have played an evolutionary role across species pairs. Extensive chromosomal arm rearrangements have been a key mechanism involved in re-dipliodization of the salmonid genome; therefore, we investigated their influence on degree of differentiation between homeologs across salmon species. We derived a linkage map for coho salmon and performed comparative mapping across syntenic arms within the genus Oncorhynchus, and with the genus Salmo, to determine the phylogenetic relationship between chromosome arrangements and the retention of undifferentiated duplicated regions. A 6596.7 cM female coho salmon map, comprising 30 linkage groups with 7415 and 1266 nonduplicated and duplicated loci, respectively, revealed uneven distribution of duplicated loci along and between chromosome arms. These duplicated regions were conserved across syntenic arms across Oncorhynchus species and were identified in metacentric chromosomes likely formed ancestrally to the divergence of Oncorhynchus from Salmo. These findings support previous studies in which observed pairings involved at least one metacentric chromosome. Re-diploidization in salmon may have been prevented or retarded by the formation of metacentric chromosomes after the whole genome duplication event and may explain lineage-specific innovations in salmon species if functional genes are found in these regions.

The Atlantic salmon genome provides insights into rediploidization

“…Conservation of synteny between salmonids 22,35 suggests that information from one high-quality salmonid genome can be used to improve genome sequence assemblies of other salmonids. To test the feasibility of such a comparative genomics approach, we used the Atlantic salmon assembly to construct chromosome sequences for the non-chromosome anchored rainbow trout genome sequence 13 .…”

Genomic tools for new insights to variation, adaptation, and evolution in the salmonid fishes: a perspective for charr

“…Data can also be used to draw comparisons across species. For example, Kodama and colleagues developed a linkage map for coho salmon (O. kisutch) and compared it to previously published Chinook salmon, rainbow trout, and Atlantic salmon maps for genetic analysis of chromosomsal evolution across the groups (Kodama et al, 2014).…”

Salmonid chromosome evolution as revealed by a novel method for comparing RADseq linkage maps

“…Linkage maps can be highly useful for comparing chromosomal evolution among lineages using shared markers between maps to identify corresponding chromosomes (i.e. homologous chromosomes) between species (Naish et al 2013; Kodama et al 2014). Furthermore, high quality, dense linkage maps are valuable for validating and orienting genomic scaffolds (Mascher & Stein 2014; Fierst 2015), especially for cases of residual polyploidy, large genome size, and high repeat content (Amores et al 2014; Ming & Man Wai 2015).…”