Differential Evolution of the 13 Atlantic Salmon Hox Clusters

Abstract

Hox cluster organization represents a valuable marker to study the effects of recent genome duplication in salmonid fish (25-100 Mya). Using polymerase chain reaction amplification of cDNAs, BAC library screening, and genome walking, we reconstructed 13 Hox clusters in the Atlantic salmon containing 118 Hox genes including 8 pseudogenes. Hox paralogs resulting from the genome duplication preceding the radiation of ray-finned fish have been much better preserved in salmon than in other model teleosts. The last genome duplication in the salmon lineage has been followed by the loss of 1 of the 4 HoxA clusters. Four rounds of genome duplication after the vertebrate ancestor salmon Hox clusters display the main organizational features of vertebrate Hox clusters, with Hox genes exclusively that are densely packed in the same orientation. Recently, duplicated Hox clusters have engaged a process of divergence, with several cases of pseudogenization or asymmetrical evolution of Hox gene duplicates, and a marked erosion of identity in noncoding sequences. Strikingly, the level of divergence attained strongly depends on the Hox cluster pairs rather than on the Hox genes within each cluster. It is particularly high between both HoxBb clusters and both HoxDa clusters, whereas both HoxBa clusters remained virtually identical. Positive selection on the Hox protein-coding sequences could not be detected.

Evidence for at least six Hox clusters in the Japanese lamprey ( Lethenteron japonicum )

“…To date there is no evidence for such large-scale segmental duplication of Hox loci in any other vertebrate. Additional Hox clusters have been found so far only in ray-finned fishes and they are all associated with additional genome duplication event(s) (7,8,35). To verify our inference of an additional genome duplication in the lamprey lineage, we compared the ages of lamprey and human paralogs by calculating the rate of transversion at fourfold degenerate sites (4DTv rates), which is insensitive to variation in local GC content.…”

“…Most teleost fishes contain seven or eight Hox clusters as a result of an additional "teleost-specific" genome duplication (TSGD) event in the ray-finned fish lineage (7). The Atlantic salmon, whose lineage has experienced a more recent tetraploidization event on top of the TSGD, contains 13 Hox clusters (8). A feature of Hox cluster genes is the collinearity between their positions in the cluster and their expression pattern along the anteroposterior axis of developing embryos.…”

Evolutionary history of two divergent Dmrt1 genes reveals two rounds of polyploidy origins in gibel carp

“…In comparison with the prevalent incidence in plants, polyploid species or forms are very rare in vertebrates including fishes and amphibians (Gui and Zhou, 2010;Otto, 2007), but some polyploid members have passed through a bottleneck of polyploidy instability in some teleost fish lineages including cyprinids, catostomids, salmonids, and cobitids, and formed diploid species via diploidization (Allendorf and Thorgaard, 1984;Gui and Zhou, 2010;Saitoh et al, 2010;Yang and Gui, 2004). Therefore, polyploidy has been a vital evolutionary force and plays important roles in fish evolution and speciation (Luo et al, 2007;Mungpakdee et al, 2008).…”

Elephant shark ( Callorhinchus milii ) provides insights into the evolution of Hox gene clusters in gnathostomes

“…In addition, several Hox genes have experienced lineagespecific secondary losses resulting in each of these teleosts possessing a unique set of Hox genes (5,15). In contrast to these teleosts, Atlantic salmon contains as many as 13 Hox clusters owing to an additional genome duplication in a salmonid ancestor (16). Although lampreys and hagfishes are known to contain multiple Hox clusters, the exact number of Hox clusters in these primitive jawless vertebrates is not known.…”