Masaya Katoh

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

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.

Mitochondrial genomes and phylogeny of the ocean sunfishes (Tetraodontiformes: Molidae)

We determined the complete nucleotide sequences of the mitochondrial genomes for the three currently recognized species of ocean sunfish: Mola mola, Masturus lanceolatus, and Ranzania laevis (Tetraodontiformes: Molidae). Each genome contained the 37 genes as found in teleosts, with the typical gene order in teleosts. Bayesian, maximum-likelihood, and maximum-parsimony analyses were conducted with the data set comprising concatenated nucleotide sequences from 36 genes (excluding the ND6 gene) of three molids and four outgroups (three tetraodontiforms plus a caproid). The resultant trees supported monophyly of the Molidae and its intrarelationships ((Mola, Masturus), Ranzania), which were congruent with previous morphology-based hypotheses.

Unique patterns of pelvic fin evolution: A case study of balistoid fishes (Pisces: Tetraodontiformes) based on whole mitochondrial genome sequences

Balistoid fishes have a unique and reduced pelvic fin structure, which does not exhibit paired structures. The pelvic complex exhibits reductive trends, but its rudimentary structure was retained among balistoids, and its unidirectional and parsimonious reduction in more derived lineages has been hypothesized based on morphology. We investigated the evolution of pelvic complex reduction in balistoids using whole mitochondrial genome (mitogenome) data from 33 species (27 newly determined during the study) that represent the entire morphological diversity of balistoids. Partitioned maximum likelihood and Bayesian analyses were conducted with two datasets that comprised concatenated nucleotide sequences from 13 protein-coding genes (all positions included; third codon positions converted into purine [R] and pyrimidine [Y] [RY-coding]) plus 22 transfer RNA and two ribosomal RNA genes. The resultant trees were well resolved and largely congruent, with most internal branches having high support values. The mitogenomic datasets strongly supported monophylies of both balistids and monacanthids, but rejected previous hypotheses on the intra-relationships in each family. The present tree topology revealed that highly reduced pelvic complexes had multiple origins, and optimization of the traits on the resultant tree strongly suggested the non-unidirectional and independent reduction of pelvic complexes in balistoids. The evolution of balistoid pelvic structure is very different among fishes that exhibit its reductive trends, and this uniqueness in pelvic evolution may be a link to their reproductive behaviors.

Intertidal burrows of the air-breathing eel goby, Odontamblyopus lacepedii (Gobiidae: Amblyopinae)

Odontamblyopus lacepedii inhabits burrows in mudflats and breathes air at the surface opening. Investigations of the intertidal burrows using resin casting demonstrated a highly branched burrow system. The burrows are composed primarily of branching patterns of interconnected tunnels and shafts that communicate into two to seven surface openings. Bulbous chambers (i.e., dilated portions of the burrow) at branching sections of the tunnels or shafts are common features of the burrow. The presence of these chambers accords the fish adequate space to maneuver inside the burrow, and thus constant access to the surface. The combination of all burrow characteristics and previously reported variability in air breathing patterns are ostensibly of selective value for aerial predator avoidance during air breathing in O. lacepedii.

Respiratory vasculatures of the intertidal air-breathing eel goby, Odontamblyopus lacepedii (Gobiidae: Amblyopinae)

Lacking a propensity to emerge over the mud surface, the eel goby, Odontamblyopus lacepedii, survives low tide periods by continuously breathing air in burrows filled with hypoxic water. As with most marine air-breathing fishes, O. lacepedii does not possess an accessory air-breathing organ, but holds air in the buccal–opercular cavity. The present study aimed to clarify how the respiratory vasculature has been modified in this facultative air-breathing fish. Results showed that the gills apparently lacked structural modifications for air breathing, whereas the inner epithelia of the opercula were richly vascularized. Comparison with two sympatric gobies revealed that the density of blood capillaries within 10μm from the inner opercular epithelial surface in O. lacepedii (14.5 ± 3.0 capillaries mm−1; mean ± s.d., n = 3) was significantly higher than in the aquatic non-air-breathing Acanthogobius hasta (0.0 ± 0.0) but significantly lower than in the amphibious air-breathing mudskipper, Periophthalmus modestus (59.1 ± 8.5). The opercular capillary bed was supplied predominantly by the 1st efferent branchial arteries (EBA1) and drained by the opercular veins, which open into the anterior cardinal vein. Deep invaginations at the distal end of the EBA1 and the junction with EBA2 are suggestive of blood flow regulatory sites during breath-holding and apnoeic periods. It remains to be investigated how blood flow through the gills is maintained during breath holding when the buccal–opercular cavity is filled with air.

Genetic and morphological identification of Sebastiscus tertius in the East China Sea (Scorpaeniformes : Scorpaenidae)

Abstract The allozymes and morphology of 110 specimens of three Sebastiscus species (S. marmoratus, S. tertius, and S. albofasciatus) in the East China Sea and near Japan were compared. Results of 20 allozyme loci studied showed that all three species were closely related (Neis unbiased genetic distances, 0.057–0.133) but could be identified on the basis of informative loci with a few exceptions. Initial identification based on color patterns agreed with allozyme identification in more than 98% of Sebastiscus specimens and agreed completely in S. albofasciatus. One specimen that was initially identified as S. marmoratus because of the dark body color was actually S. tertius according to two informative allozyme loci. Number of pectoral fin rays differed between S. marmoratus (18 or fewer, 98%) and S. tertius (19 or more, 85%) in this study. The previously mentioned dark specimen had 19 pectoral fin rays, which are characteristic in S. tertius. Using seven morphological measurements, canonical discriminant analysis between S. marmoratus and S. tertius classified less than 90% of specimens into the original groups (species). Some specimens of S. tertius resembled S. marmoratus in body shape and vice versa. A combination of genetic characterization and morphological examination is necessary to identify S. marmoratus and S. tertius accurately. Distinction based on allozymes and color patterns with numbers of pectoral fin rays should provide satisfactory identification.