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A new perspective on phylogeny and evolution of tetraodontiform fishes (Pisces: Acanthopterygii) based on whole mitochondrial genome sequences: basal ecological diversification?

Yamanoue Y, Miya M, Matsuura K, Katoh M, Sakai H, Nishida M - BMC Evol. Biol. (2008)

Bottom Line: The resultant tree topologies from the two data sets were congruent, with many internal branches showing high support values.The mitogenomic data strongly supported monophyly of all families and subfamilies (except the Tetraodontinae) and sister-group relationships of Balistidae + Monacanthidae and Tetraodontidae + Diodontidae, confirming the results of previous studies.However, we also found two unexpected basal splits into Tetraodontoidei (Triacanthidae + Balistidae + Monacanthidae + Tetraodontidae + Diodontidae + Molidae) and Triacanthodoidei (Ostraciidae + Triodontidae + Triacanthodidae).

View Article: PubMed Central - HTML - PubMed

Affiliation: Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo 164-8639, Japan. ayyamano@mail.ecc.u-tokyo.ac.jp

ABSTRACT

Background: The order Tetraodontiformes consists of approximately 429 species of fishes in nine families. Members of the order exhibit striking morphological diversity and radiated into various habitats such as freshwater, brackish and coastal waters, open seas, and deep waters along continental shelves and slopes. Despite extensive studies based on both morphology and molecules, there has been no clear resolution except for monophyly of each family and sister-group relationships of Diodontidae + Tetraodontidae and Balistidae + Monacanthidae. To address phylogenetic questions of tetraodontiform fishes, we used whole mitochondrial genome (mitogenome) sequences from 27 selected species (data for 11 species were newly determined during this study) that fully represent all families and subfamilies of Tetraodontiformes (except for Hollardinae of the Triacanthodidae). Partitioned maximum likelihood (ML) and Bayesian analyses were performed on two data sets comprising concatenated nucleotide sequences from 13 protein-coding genes (all positions included; third codon positions converted into purine [R] and pyrimidine [Y]), 22 transfer RNA and two ribosomal RNA genes (total positions = 15,084).

Results: The resultant tree topologies from the two data sets were congruent, with many internal branches showing high support values. The mitogenomic data strongly supported monophyly of all families and subfamilies (except the Tetraodontinae) and sister-group relationships of Balistidae + Monacanthidae and Tetraodontidae + Diodontidae, confirming the results of previous studies. However, we also found two unexpected basal splits into Tetraodontoidei (Triacanthidae + Balistidae + Monacanthidae + Tetraodontidae + Diodontidae + Molidae) and Triacanthodoidei (Ostraciidae + Triodontidae + Triacanthodidae).

Conclusion: This basal split into the two clades has never been reported and challenges previously proposed hypotheses based on both morphology and nuclear gene sequences. It is likely that the basal split had involved ecological diversification, because most members of Tetraodontoidei exclusively occur in shallow waters (freshwater, brackish and coastal waters, and open seas), while those of Triacanthodoidei occur mainly in relatively deep waters along continental shelves and slopes except for more derived ostraciids. This suggests that the basal split between the two clades led to subsequent radiation into the two different habitats.

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Bayesian tree using the 12n3rRTn data set. Bayesian analysis for the 123nRTn data set produced an identical topology. The numbers near internal branches indicate Bayesian posterior probabilities for the 12n3rRTn (left) and 123nRTn (right) data sets (values less than 50% not shown). Single numbers indicate that the 12n3rRTn and 123nRTn data sets resulted in identical values. Solid, open, and double circles, and triangles indicated that main habitats of a family are deep waters, coastal waters, open sea, and brackish and freshwater, respectively. Superfamilial classification follow Winterbottom [1] and Tyler and Sorbini [6].
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Figure 3: Bayesian tree using the 12n3rRTn data set. Bayesian analysis for the 123nRTn data set produced an identical topology. The numbers near internal branches indicate Bayesian posterior probabilities for the 12n3rRTn (left) and 123nRTn (right) data sets (values less than 50% not shown). Single numbers indicate that the 12n3rRTn and 123nRTn data sets resulted in identical values. Solid, open, and double circles, and triangles indicated that main habitats of a family are deep waters, coastal waters, open sea, and brackish and freshwater, respectively. Superfamilial classification follow Winterbottom [1] and Tyler and Sorbini [6].

Mentions: Although we were unable to determine a priori which data set recovered a more likely phylogeny, we considered that the 12n3rRTn data set (RY-coding) represented the best estimate of phylogenies, which effectively removes the likely noise from quickly saturated transitional changes in the third codon positions [27,33] and avoids a lack of signal by retaining all available positions in the data set [33]. Accordingly, the resultant tree from the 12n3rRTn data set derived from the partitioned ML and Bayesian analyses is shown in Figs. 3 and 4, with statistical support (bootstrap probabilities [BPs] from the partitioned ML analysis and posterior probabilities [PPs] from the partitioned Bayesian analysis) for 12n3rRTn and 123nRTn data sets indicated on each internal branch. No topological incongruities between the two data sets were found.


A new perspective on phylogeny and evolution of tetraodontiform fishes (Pisces: Acanthopterygii) based on whole mitochondrial genome sequences: basal ecological diversification?

Yamanoue Y, Miya M, Matsuura K, Katoh M, Sakai H, Nishida M - BMC Evol. Biol. (2008)

Bayesian tree using the 12n3rRTn data set. Bayesian analysis for the 123nRTn data set produced an identical topology. The numbers near internal branches indicate Bayesian posterior probabilities for the 12n3rRTn (left) and 123nRTn (right) data sets (values less than 50% not shown). Single numbers indicate that the 12n3rRTn and 123nRTn data sets resulted in identical values. Solid, open, and double circles, and triangles indicated that main habitats of a family are deep waters, coastal waters, open sea, and brackish and freshwater, respectively. Superfamilial classification follow Winterbottom [1] and Tyler and Sorbini [6].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2500030&req=5

Figure 3: Bayesian tree using the 12n3rRTn data set. Bayesian analysis for the 123nRTn data set produced an identical topology. The numbers near internal branches indicate Bayesian posterior probabilities for the 12n3rRTn (left) and 123nRTn (right) data sets (values less than 50% not shown). Single numbers indicate that the 12n3rRTn and 123nRTn data sets resulted in identical values. Solid, open, and double circles, and triangles indicated that main habitats of a family are deep waters, coastal waters, open sea, and brackish and freshwater, respectively. Superfamilial classification follow Winterbottom [1] and Tyler and Sorbini [6].
Mentions: Although we were unable to determine a priori which data set recovered a more likely phylogeny, we considered that the 12n3rRTn data set (RY-coding) represented the best estimate of phylogenies, which effectively removes the likely noise from quickly saturated transitional changes in the third codon positions [27,33] and avoids a lack of signal by retaining all available positions in the data set [33]. Accordingly, the resultant tree from the 12n3rRTn data set derived from the partitioned ML and Bayesian analyses is shown in Figs. 3 and 4, with statistical support (bootstrap probabilities [BPs] from the partitioned ML analysis and posterior probabilities [PPs] from the partitioned Bayesian analysis) for 12n3rRTn and 123nRTn data sets indicated on each internal branch. No topological incongruities between the two data sets were found.

Bottom Line: The resultant tree topologies from the two data sets were congruent, with many internal branches showing high support values.The mitogenomic data strongly supported monophyly of all families and subfamilies (except the Tetraodontinae) and sister-group relationships of Balistidae + Monacanthidae and Tetraodontidae + Diodontidae, confirming the results of previous studies.However, we also found two unexpected basal splits into Tetraodontoidei (Triacanthidae + Balistidae + Monacanthidae + Tetraodontidae + Diodontidae + Molidae) and Triacanthodoidei (Ostraciidae + Triodontidae + Triacanthodidae).

View Article: PubMed Central - HTML - PubMed

Affiliation: Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo 164-8639, Japan. ayyamano@mail.ecc.u-tokyo.ac.jp

ABSTRACT

Background: The order Tetraodontiformes consists of approximately 429 species of fishes in nine families. Members of the order exhibit striking morphological diversity and radiated into various habitats such as freshwater, brackish and coastal waters, open seas, and deep waters along continental shelves and slopes. Despite extensive studies based on both morphology and molecules, there has been no clear resolution except for monophyly of each family and sister-group relationships of Diodontidae + Tetraodontidae and Balistidae + Monacanthidae. To address phylogenetic questions of tetraodontiform fishes, we used whole mitochondrial genome (mitogenome) sequences from 27 selected species (data for 11 species were newly determined during this study) that fully represent all families and subfamilies of Tetraodontiformes (except for Hollardinae of the Triacanthodidae). Partitioned maximum likelihood (ML) and Bayesian analyses were performed on two data sets comprising concatenated nucleotide sequences from 13 protein-coding genes (all positions included; third codon positions converted into purine [R] and pyrimidine [Y]), 22 transfer RNA and two ribosomal RNA genes (total positions = 15,084).

Results: The resultant tree topologies from the two data sets were congruent, with many internal branches showing high support values. The mitogenomic data strongly supported monophyly of all families and subfamilies (except the Tetraodontinae) and sister-group relationships of Balistidae + Monacanthidae and Tetraodontidae + Diodontidae, confirming the results of previous studies. However, we also found two unexpected basal splits into Tetraodontoidei (Triacanthidae + Balistidae + Monacanthidae + Tetraodontidae + Diodontidae + Molidae) and Triacanthodoidei (Ostraciidae + Triodontidae + Triacanthodidae).

Conclusion: This basal split into the two clades has never been reported and challenges previously proposed hypotheses based on both morphology and nuclear gene sequences. It is likely that the basal split had involved ecological diversification, because most members of Tetraodontoidei exclusively occur in shallow waters (freshwater, brackish and coastal waters, and open seas), while those of Triacanthodoidei occur mainly in relatively deep waters along continental shelves and slopes except for more derived ostraciids. This suggests that the basal split between the two clades led to subsequent radiation into the two different habitats.

Show MeSH