Basal jawed vertebrate phylogeny inferred from multiple nuclear DNA-coded genes

Abstract

Background: Phylogenetic analyses of jawed vertebrates based on mitochondrial sequences often result in confusing inferences which are obviously inconsistent with generally accepted trees. In particular, in a hypothesis by Rasmussen and Arnason based on mitochondrial trees, cartilaginous fishes have a terminal position in a paraphyletic cluster of bony fishes. No previous analysis based on nuclear DNA-coded genes could significantly reject the mitochondrial trees of jawed vertebrates.

Results: We have cloned and sequenced seven nuclear DNA-coded genes from 13 vertebrate species. These sequences, together with sequences available from databases including 13 jawed vertebrates from eight major groups (cartilaginous fishes, bichir, chondrosteans, gar, bowfin, teleost fishes, lungfishes and tetrapods) and an outgroup (a cyclostome and a lancelet), have been subjected to phylogenetic analyses based on the maximum likelihood method.

Conclusion: Cartilaginous fishes have been inferred to be basal to other jawed vertebrates, which is consistent with the generally accepted view. The minimum log-likelihood difference between the maximum likelihood tree and trees not supporting the basal position of cartilaginous fishes is 18.3 +/- 13.1. The hypothesis by Rasmussen and Arnason has been significantly rejected with the minimum log-likelihood difference of 123 +/- 23.3. Our tree has also shown that living holosteans, comprising bowfin and gar, form a monophyletic group which is the sister group to teleost fishes. This is consistent with a formerly prevalent view of vertebrate classification, although inconsistent with both of the current morphology-based and mitochondrial sequence-based trees. Furthermore, the bichir has been shown to be the basal ray-finned fish. Tetrapods and lungfish have formed a monophyletic cluster in the tree inferred from the concatenated alignment, being consistent with the currently prevalent view. It also remains possible that tetrapods are more closely related to ray-finned fishes than to lungfishes.

Figure 1

Two hypotheses on jawed vertebrates. (A) Traditional view. (B) Mitochondrial tree proposed by Arnason's group [1-3].

Figure 2

Four hypotheses of phylogenetic relationship among ray-finned fishes. (A) Formerly accepted view. (B) Currently accepted view. (C) An alternative hypothesis by Olsen [42]. (D) Mitochondrial tree by Inoue et al. [16].

Figure 3

The maximum likelihood tree inferred from the concatenated amino acid sequences (2,942 residues) of seven proteins. Reliability index [26] and the bootstrap probability for each branch are indicated before and after a slant, respectively. This tree corresponds to topology a in Tables 1 and 2. Topology b in Tables 1 and 2 is indicated by a dotted arrow. A dash-dotted line indicates the position of plownose chimaera inferred from six proteins. Branch lengths are proportional to accumulated amino acid substitutions.