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

Abstract

BackgroundThe 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).ResultsThe 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).ConclusionThis 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.

Teleost fish with specific genome duplication as unique models of vertebrate evolution

“…b Actinopterygian phylogeny ) and the estimated timing of the 3R-WGD (Chiu et al 2004;Hoegg et al 2004;Sato and Nishida 2007;Chambers et al 2009) proteins duplicated through WGD events, and also for addressing long-term genome evolution after WGD. In addition, comprehensive phylogenetic frameworks and estimated divergence times between lineages, which are indispensable for sound comparative evolutionary studies, are now available in teleosts Miya et al 2003Miya et al , 2005Inoue et al 2005;Lavoué et al 2005;Kawahara et al 2008;Lavoué et al 2008;Setiamarga et al 2008;Yamanoue et al 2008Yamanoue et al , 2009. Particularly, the recent divergence-time frameworks of teleosts Yamanoue et al 2006;Azuma et al 2008;Setiamarga et al 2009) would be more reliable than previous ones because the recent estimations are based on rich information of fossil records (e.g., Benton 1993;Benton and Donoghue 2007), large sequence data sets from whole mitochondrial genomes, and an method which does not depend on the assumption of constant rate of molecular evolution (Thorne et al 1998).…”

Taxonomy and systematics of tetraodontiform fishes: a review focusing primarily on progress in the period from 1980 to 2014

“…Diodontidae, as previously seen in morphological studies. On the basis of whole mitochondrial genome sequences, Yamanoue et al (2008) documented different phylogenetic relationships from those of other authors. Whereas the Triacanthidae was usually placed close to the Triacanthodidae, Balistidae, and Monacanthidae in other studies (Winterbottom 1974;Tyler 1980;Leis 1984;Santini and Tyler 2003;Holcroft 2005;Alfaro et al 2007;Santini et al 2013c), Yamanoue et al (2008) recovered a relationship of the Triacanthidae with the Tetraodontidae and Diodontidae.…”

“…Molecular studies by various authors have generally supported the monophyly of tetraodontiform families (Holcroft 2005;Alfaro et al 2007;Yamanoue et al 2007Yamanoue et al , 2008, although conflicts exist between the constructed topologies of familial relationships by morphological and molecular analyses (Figs. 7, 8).…”

“…In contrast, the Molidae was recovered as the sister group to a clade comprising the Tetraodontidae and Diodontidae by Santini et al (2013c) as previously indicated by morphological studies. The Triodontidae was considered to be close to the Tetraodontidae, Diodontidae, and Molidae by morphological studies (Winterbottom 1974;Tyler 1980;Santini and Tyler 2003), whereas molecular studies recovered close relationship of the Triodontidae with the Aracanidae and Ostraciidae (Alfaro et al 2007;Yamanoue et al 2008;Santini et al 2013c). …”

Skate-ing on thin ice: molecular ecology of longnose skates in the Southeast Pacific Ocean

“…However, by increasing the number of characters analysed in a single dataset, mitogenomes may have the potential to alleviate and resolving these intrinsic problematic issues in taxonomy (Mueller et al, 2004;Yamanoue et al, 2008;Tanaka et al, 2013;Poortvliet et al, 2015).…”