Genome evolution in the fish family salmonidae: generation of a brook charr genetic map and comparisons among charrs (Arctic charr and brook charr) with rainbow trout

Abstract

BackgroundSalmonids are regarded as 4R derivative species, having experienced 4 whole genome duplication events in their ancestry. Many duplicated chromosome regions still share extensive homology with one another which is maintained primarily through male-based homeologous chromosome pairings during meiosis. The formation of quadrivalents during meiosis leads to pseudolinkage. This phenomenon is more prevalent within 5 of the 12 ancestral teleost linkage groups in salmonids.ResultsWe constructed a genetic linkage map for brook charr and used this in combination with the genetic map from Arctic charr, to make comparisons with the genetic map of rainbow trout. Although not all chromosome arms are currently mapped, some homologous chromosome rearrangements were evident between Arctic charr and brook charr. Notably, 10 chromosome arms in brook charr representing 5 metacentric chromosomes in Arctic charr have undergone rearrangements. Three metacentrics have one arm translocated and fused with another chromosome arm in brook charr to a make a new metacentrics while two metacentrics are represented by 4 acrocentric pairs in brook charr. In two cases (i.e., BC-4 and BC-16), an apparent polymorphism was observed with the identification of both a putative metacentric structure (similar to metacentric AC-4 = BC-4 and a joining of acrocentric AC-16 + one arm of AC-28 = BC-16), as well as two separate acrocentric linkage groups evident in the mapping parents. Forty-six of the expected 50 karyotypic arms could be inter-generically assigned. SEX in brook charr (BC-4) was localized to the same homologous linkage group region as in Arctic charr (AC-4). The homeologous affinities detected in the two charr species facilitated the identification of 20 (expected number = 25) shared syntenic regions with rainbow trout, although it is likely that some of these regions were partial or overlapping arm regions.ConclusionsInter-generic comparisons among 2 species of charr (genus Salvelinus) and a trout (genus Oncorhynchus) have identified that linkage group arm arrangements are largely retained among these species. Previous studies have revealed that up to 7 regions of high duplicate marker retention occur between Salmo species (i.e., Atlantic salmon and brown trout) and rainbow trout, with 5 of these regions exhibiting higher levels of pseudolinkage. Pseudolinkage was detected in the charr species (i.e., BC-1/21, AC-12/27, AC-6/23, = RT-2p/29q, RT-12p/16p, and RT-27p/31p, respectively) consistent with three of the five 'salmonid-specific' pseudolinkage regions. Chromosome arms with the highest number of duplicated markers in rainbow trout are the linkage group arms with the highest retention of duplicated markers in both charr species.

Transcriptomics of salinity tolerance capacity in Arctic charr (Salvelinus alpinus): a comparison of gene expression profiles between divergent QTL genotypes

“…Perhaps most intriguing is the presence of an eight gene cluster spanning 3.022 Mb along Ga-XIX. Unfortunately, due to the low resolution of the Arctic charr linkage map (9,63,69), the precise location of this cluster in Arctic charr is difficult to ascertain. Possible locations include AC-1, 4, 6, 12, and 19; however, most of these linkage groups are implicated by single marker associations (48).…”

“…On these occasions, synteny maps of stickleback with Atlantic salmon and rainbow trout (48) were used in the same manner to make predictions about gene positions in those species. Known homologous linkage group affinities among Arctic charr, Atlantic salmon, and rainbow trout (9,10,63) were then used to make predictions about the position of differentially expressed genes on the Arctic charr linkage map.…”

Evolution of the Sex Chromosomes in Salmonid Fishes

“…A genetic linkage map for Canadian brook trout [Timusk et al, 2011] mapped the SD to a linkage group corresponding to AC-4, the sex linkage group in Arctic char, so there may be more than one location of SD in this species as well. It is interesting that lake and brook trout form totally interfertile hybrids and that F1 hybrids between [Moghadam et al, 2007].…”

An integrated transcriptomic and comparative genomic analysis of differential gene expression in Arctic charr (Salvelinus alpinus) following seawater exposure

“…We found that stickleback synteny blocks on Arctic charr linkage groups AC-1, AC-11 [henceforth referred to as AC-1/11, due to the strong homeologous affinities of these linkage groups (Danzmann et al, 2005;Timusk et al, 2011;Norman et al, 2012)], and AC-28 contain a greater number of DEGs than expected by chance. These linkage groups also contain QTL for the salinity tolerance performance traits Na + /K + -ATPase activity and growth in seawater , suggesting that these QTL could be the product of multiple genes containing cisregulatory polymorphisms.…”

“…This would have to be temporary, however, perhaps until gill tissue and other ionoregulatory organs have transitioned to an optimal ion-excreting state, because the seawater phase of salmonid ontogeny is typically characterized by heightened growth rates. Repression of developmental gene expression may liberate energy for the transition of osmoregulatory tissues towards an ion-excreting state, as the metabolic demand of hypo-osmoregulation can be high, ranging from <4% in cut-throat trout (Oncorhynchus clarkii clarkii) (Timusk et al, 2011); stickleback chromosomes obtained from Ensembl (version 68) (Jones et al, 2012;Flicek et al, 2013); synteny block sizes obtained from Norman et al (Norman et al, 2012); numbers in parentheses for family 10 (F10) and family 12 (F12) differentially expressed genes (DEG) represent expected values from a 2×2 χ 2 test for independence; bold values are significant at P<0.05; *values pass FDR significance threshold (α=0.05). (Morgan and Iwama, 1999) to 30% in rainbow trout (Rao, 1968), and 20% of gill metabolism in Atlantic salmon (McCormick et al, 1989).…”