Genomic Novelty at the Vertebrate Ancestor


The group of vertebrates includes diverse evolutionary lineages, and typical laboratory‐model vertebrates are confined to only limited groups (tetrapods and teleost fishes) of its entire diversity. Accumulating information of the molecular sequence for the still‐missing lineages including jawless fishes can now provide deeper insights into the definition of the taxon Vertebrata at the genomic level. Above all, the so‐called two‐round whole genome duplications are described to have occurred in the early vertebrate evolution. Recent molecular phylogenetic analyses for some gene families resulted in a scenario in which the genome expansion might have been completed before the split of the lineage of cyclostomes (extant jawless fishes including hagfishes and lampreys) from the future jawed vertebrate lineage. In addition to this genome expansion, key features of genomic contents of the vertebrate ancestor are inferable, provided secondary changes introduced later in individual lineages are taken into deep consideration in ancestral phylogenetic reconstruction.

Key Concepts:

  • Large‐scale sequencing of genomes and transcriptomes of non‐model vertebrates in crucial phylogenetic positions provided valuable information about the vertebrates' entire diversity.

  • The two‐round genome duplications likely define the vertebrates genomically.

  • De novo genes should also have contributed to the vertebrate gene repertoire.

  • Lineage‐specific molecular changes should be taken into deep consideration in reconstructing the ancestral state as in morphological comparison.

  • Large‐scale sequence resources for early branching vertebrates are expected to provide clearer insights into the genomics' novelty which established the vertebrates.

Keywords: vertebrate; lamprey; hagfish; genome duplication; endothelin

Figure 1.

Alternative scenarios about the timing of the two‐round whole genome duplications. The arrows indicate the timing of the whole genome duplications.

Figure 2.

Identification of the genes involved in the endothelin system. Black vertical or diagonal lines indicate orthology between species. Identification of the genes in the lamprey and the cartilaginous fishes, as well as their nomenclature, is based on the author's previous study (Kuraku et al., ). Only the putative amphioxus ortholog of the endothelin receptors has been identified in its genome assembly and remains to be functionally characterised. Although the EdnrB2 is shown here as present in tetrapods, its ortholog was likely lost in the lineage leading to eutherian mammals (Braasch et al., ). The genes which were not identified within the taxonomic clades including species with sequenced genomes are indicated as ‘not found’. The node corresponding to the common ancestor of all extant vertebrates is shown with an open circle in the tree on the left.



Braasch I, Volff JN and Schartl M (2009) The endothelin system: evolution of vertebrate‐specific ligand‐receptor interactions by three rounds of genome duplication. Molecular Biology and Evolution 26: 783–799.

Carroll SB (2008) Evo‐devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25–36.

Carvunis AR, Rolland T, Wapinski I et al. (2012) Proto‐genes and de novo gene birth. Nature.

Delsuc F, Brinkmann H, Chourrout D and Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439: 965–968.

Duméril AMC (1806) Zoologie analytique, ou méthode naturelle de classification des animaux, rendue plus facile a l'Aide de Tableaux synoptiques par. Paris: Allais.

Endo T, Imanishi T, Gojobori T and Inoko H (1997) Evolutionary significance of intra‐genome duplications on human chromosomes. Gene 205: 19–27.

Furlong RF, Younger R, Kasahara M et al. (2007) A degenerate ParaHox gene cluster in a degenerate vertebrate. Molecular Biology and Evolution 24: 2681–2686.

Hedges SB and Kumar S (2009) The Timetree of Life. Oxford; New York: Oxford University Press.

Hoffmann FG, Opazo JC and Storz JF (2011) Differential loss and retention of cytoglobin, myoglobin, and globin‐E during the radiation of vertebrates. Genome Biology and Evolution 3: 588–600.

Holland PW, Garcia‐Fernandez J, Williams NA and Sidow A (1994) Gene duplications and the origins of vertebrate developement. Development Supplement: 125–133.

Janvier P (2007) Evolutionary biology: born‐again hagfishes. Nature 446: 622–623.

Jørgensen JM (1998) The Biology of Hagfishes, 1st edn. London; New York: Chapman & Hall.

Kasahara M, Hayashi M, Tanaka K et al. (1996) Chromosomal localization of the proteasome Z subunit gene reveals an ancient chromosomal duplication involving the major histocompatibility complex. Proceedings of the National Academy of Sciences of the USA 93: 9096–9101.

Katsanis N, Fitzgibbon J and Fisher EM (1996) Paralogy mapping: identification of a region in the human MHC triplicated onto human chromosomes 1 and 9 allows the prediction and isolation of novel PBX and NOTCH loci. Genomics 35: 101–108.

Kawashima T, Kawashima S, Tanaka C et al. (2009) Domain shuffling and the evolution of vertebrates. Genome Research 19: 1393–1403.

Kawauchi H, Suzuki K, Yamazaki T et al. (2002) Identification of growth hormone in the sea lamprey, an extant representative of a group of the most ancient vertebrates. Endocrinology 143: 4916–4921.

Kojima NF, Kojima KK, Kobayakawa S et al. (2010) Whole chromosome elimination and chromosome terminus elimination both contribute to somatic differentiation in Taiwanese hagfish Paramyxine sheni. Chromosome Research: an International Journal on the Molecular, Supramolecular and Evolutionary Aspects of Chromosome Biology 18: 383–400.

Kuraku S (2008) Insights into cyclostome phylogenomics: pre‐2R or post‐2R? Zoological Science 25: 960–968.

Kuraku S (2010) Palaeophylogenomics of the vertebrate ancestor – impact of hidden paralogy on hagfish and lamprey gene phylogeny. Integrative and Comparative Biology 50: 124–129.

Kuraku S (2011) Hox gene clusters of early vertebrates: do they serve as reliable markers for genome evolution? Genomics, Proteomics and Bioinformatics 9: 97–103.

Kuraku S and Kuratani S (2006) Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zoological Science 23: 1053–1064.

Kuraku S and Meyer A (2009) The evolution and maintenance of Hox gene clusters in vertebrates and the teleost‐specific genome duplication. International Journal of Developmental Biology 53: 765–773.

Kuraku S, Meyer A and Kuratani S (2009a) Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Molecular Biology and Evolution 26: 47–59.

Kuraku S, Ota KG and Kuratani S (2009b) Cyclostomata. In: Kumar S and Hedges B (eds) Timetree of Life, pp. 317–319. New York: Oxford University Press.

Kuraku S, Takio Y, Sugahara F, Takechi M and Kuratani S (2010) Evolution of oropharyngeal patterning mechanisms involving Dlx and endothelins in vertebrates. Developmental Biology 341: 315–323.

Lundin LG (1993) Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16: 1–19.

Moriyama S, Oda M, Takahashi A, Sower SA and Kawauchi H (2006) Genomic structure of the sea lamprey growth hormone‐encoding gene. General and Comparative Endocrinology 148: 33–40.

Ohno S (1970) Evolution by Gene Duplication. New York: Springer‐Verlag.

Ominato K and Nozaki M (2002) Distribution of growth hormone‐like cells in the pituitary of adult sea lampreys, Petromyzon marinus. Zoological Science 19: 1055–1059.

Ota KG, Fujimoto S, Oisi Y and Kuratani S (2011) Identification of vertebra‐like elements and their possible differentiation from sclerotomes in the hagfish. Nature Communications 2: 373.

Ota KG, Kuraku S and Kuratani S (2007) Hagfish embryology with reference to the evolution of the neural crest. Nature 446: 672–675.

Pebusque MJ, Coulier F, Birnbaum D and Pontarotti P (1998) Ancient large‐scale genome duplications: phylogenetic and linkage analyses shed light on chordate genome evolution. Molecular Biology and Evolution 15: 1145–1159.

Putnam NH, Butts T, Ferrier DE et al. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064–1071.

Qiu H, Hildebrand F, Kuraku S and Meyer A (2011) Unresolved orthology and peculiar coding sequence properties of lamprey genes: the KCNA gene family as test case. BMC Genomics 12: 325.

Sauka‐Spengler T and Bronner‐Fraser M (2006) Development and evolution of the migratory neural crest: a gene regulatory perspective. Current Opinion in Genetics and Development 16: 360–366.

Sidow A (1996) Gen(om)e duplications in the evolution of early vertebrates. Current Opinion in Genetics and Development 6: 715–722.

Smith JJ, Antonacci F, Eichler EE and Amemiya CT (2009) Programmed loss of millions of base pairs from a vertebrate genome. Proceedings of the National Academy of Sciences of the USA 106: 11212–11217.

Sower SA and Kawauchi H (2001) Update: brain and pituitary hormones of lampreys. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology 129: 291–302.

Spring J (1997) Vertebrate evolution by interspecific hybridisation – are we polyploid? FEBS Letters 400: 2–8.

Tautz D and Domazet‐Loso T (2011) The evolutionary origin of orphan genes. Nature Reviews Genetics 12: 692–702.

Further Reading

Dittmar K and Liberles DA (2010) Evolution After Gene Duplication. Hoboken, NJ: Wiley‐Blackwell.

Gee H (1996) Before the Backbone: Views on the Origin of the Vertebrates, 1st edn. London; New York: Chapman & Hall.

Janvier P (1996) Early Vertebrates. New York: Oxford University Press.

Lynch M (2007) The Origins of Genome Architecture. Sunderland, Mass: Sinauer Associates.

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How to Cite close
Kuraku, Shigehiro(Dec 2012) Genomic Novelty at the Vertebrate Ancestor. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0024137]