Open Access Open Badges Research article

Non-parsimonious evolution of hagfish Dlx genes

Satoko Fujimoto1, Yasuhiro Oisi12, Shigehiro Kuraku3, Kinya G Ota4* and Shigeru Kuratani1

Author Affiliations

1 Laboratory for Evolutionary Morphology, RIKEN Center for Developmental Biology, Kobe, 650-0047, Japan

2 Department of Biology, Graduate School of Science, Kobe University, Kobe, Japan

3 Genome Resource and Analysis Unit, RIKEN Center for Developmental Biology, Kobe, 650-0047, Japan

4 Laboratory of Aquatic Zoology, Marine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, Yilan, 26242, Taiwan

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BMC Evolutionary Biology 2013, 13:15  doi:10.1186/1471-2148-13-15

Published: 19 January 2013



The number of members of the Dlx gene family increased during the two rounds of whole-genome duplication that occurred in the common ancestor of the vertebrates. Because the Dlx genes are involved in the development of the cranial skeleton, brain, and sensory organs, their expression patterns have been analysed in various organisms in the context of evolutionary developmental biology. Six Dlx genes have been isolated in the lampreys, a group of living jawless vertebrates (cyclostomes), and their expression patterns analysed. However, little is known about the Dlx genes in the hagfish, the other cyclostome group, mainly because the embryological analysis of this animal is difficult.


To identify the hagfish Dlx genes and describe their expression patterns, we cloned the cDNA from embryos of the Japanese inshore hagfish Eptatretus burgeri. Our results show that the hagfish has at least six Dlx genes and one pseudogene. In a phylogenetic analysis, the hagfish Dlx genes and those of the lampreys tended to be excluded from the clade of the gnathostome Dlx genes. In several cases, the lamprey Dlx genes clustered with the clade consisting of two hagfish genes, suggesting that independent gene duplications have occurred in the hagfish lineage. Analysis of the expression of these genes showed distinctive overlapping expression patterns in the cranial mesenchymal cells and the inner ear.


Independent duplication, pseudogenization, and loss of the Dlx genes probably occurred in the hagfish lineage after its split from the other vertebrate lineages. This pattern is reminiscent of the non-parsimonious evolution of its morphological traits, including its inner ear and vertebrae, which indicate that this group is an early-branching lineage that diverged before those characters evolved.

Cyclostomes; Hagfish embryos; Dlx genes; Gene duplication