Keiichi Matsuura

Explosive Speciation of Takifugu: Another Use of Fugu as a Model System for Evolutionary Biology

Although the fugu Takifugu rubripes has attracted attention as a model organism for genomic studies because of its compact genome, it is not generally appreciated that there are approximately 25 closely related species with limited distributions in the waters of East Asia. We performed molecular phylogenetic analyses and constructed a time tree using whole mitochondrial genome sequences from 15 Takifugu species together with 10 outgroups to examine patterns of diversification. The resultant time tree showed that the modern Takifugu species underwent explosive speciation during the Pliocene 1.8-5.3 Ma, which is comparable with that of the Malawi cichlids and tropheine cichlids in Lake Tanganyika. Considering their limited distributions and remarkable variations in coloration, morphology, and behavior, the results of the present study strongly suggest that Takifugu species are strong candidates as a model system for evolutionary studies of speciation mechanisms in marine environments where few such organisms are available.

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.

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

When the first Indo-Pacific Fish Conference (IPFC1) was held in Sydney in 1981, there were still many problems in the generic- and species-level taxonomy of all tetraodontiform families except for the recently reviewed Triacanthodidae and Triacanthidae. The period from IPFC1 to IPFC9 (1981−2013) was a time of great progress in the taxonomy and systematics of the Tetraodontiformes: many review and revisional papers have been published for various genera and species, with descriptions of many new taxa occurring mainly on coral reefs and in tropical freshwaters; and cladistic analyses of morphological characters have been performed to clarify phylogenetic relationships of various families and molecular analyses have greatly progressed to provide detailed phylogenetic relationships of families, genera, and even species. The purpose of this paper is to provide a review on developments in the taxonomy and systematics of the Tetraodontiformes, focusing primarily on contributions since 1980 (when James C. Tyler’s monumental work was published) through the period of IPFCs, including pertinent publications before 1980. This paper recognizes 412 extant species in the 10 families of living Tetraodontiformes, with the allocation of species and genera as follows: Triacanthodidae including 23 species in 11 genera, Triacanthidae seven species in four genera, Balistidae 37 species in 12 genera, Monacanthidae 102 species in 27 genera, Aracanidae 13 species in six genera, Ostraciidae 22 species in five genera, Triodontidae monotypic, Tetraodontidae 184 species in 27 genera, Diodontidae 18 species in seven genera, and Molidae five species in three genera. Phylogenetic relationships of the families have been clarified by morphological and molecular analyses and have provided well-supported sister relationships of the families: Triacanthodidae and Triacanthidae, Balistidae and Monacanthidae, and Tetraodontidae and Diodontidae. However, there remain problems with the phylogenetic positions of the Triodontidae and Molidae due to conflicts of differing positions in morphological and molecular studies (e.g., Molidae has been placed differently among molecular studies).

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.

Phylogeography of Blacktip Grouper, Epinephelus fasciatus (Perciformes: Serranidae), and influence of the Kuroshio Current on cryptic lineages and genetic population structure

To investigate the influence of the Kuroshio Current on the high diversity of marine fishes in Japanese waters, the intraspecific phylogeographic structure of Blacktip Grouper, Epinephelus fasciatus, was determined. The genetic analysis of E. fasciatus indicated three intraspecific mtDNA lineages representing different evolutionary histories: the first lineage differentiated in Japanese waters during a long period of fluctuations of the ancient Kuroshio Current, the second lineage, widely distributed in the tropical western Pacific, was transported to Japanese waters by the Kuroshio Current and the third lineage was distributed primarily around the Ogasawara (Bonin) Islands. Present-day sympatric distributions of the three lineages, characterized by different ratios of such individuals at each geographic site, indicated a complex genetic pattern that was classified into three demographic groups, the dispersal and gene flows of which were strongly influenced by the Kuroshio Current and factors such as countercurrent and island arc. Genetic breaks in E. fasciatus populations were congruent with other fish faunal boundaries in Japanese waters.

Redefinition and phylogenetic relationships of the family Pinguipedidae (Teleostei : Perciformes)

The phylogenetic relationships of the family Pinguipedidae plus the genus Cheimarrichthys von Haast, 1874, were studied to redefine the family. Based on a phylogenetic analysis using derived characters belonging to 21 transformation series, accepting the monophyly of Pinguipedidae plus Cheimarrichthys provisionally for the operational procedure of the analysis, it was hypothesized that Cheimarrichthys is not closely related to Parapercis Bleeker, 1863, although these genera had been considered as having a close affinity. Although the Pinguipedidae and Cheimarrichthys share nine derived characters, it was determined that these characters are also found in other trachinoid families. In addition, several families, such as the Leptoscopidae, Uranoscopidae, and Trichodontidae, have many more derived characters in common with Cheimarrichthys than the pinguipedids have with that genus. The conclusion drawn here is that it is not parsimonious to recognize the monophyly of the Pinguipedidae and Cheimarrichthys based on these nine derived characters, and that these characters are not compelling enough to link these groups. The redefined Pinguipedidae is proposed to include the following five genera: Parapercis, Prolatilus Gill, 1865, Pinguipes Cuvier, 1829, Pseudopercis de Miranda-Ribeiro, 1903, and Kochichthys Kamohara, 1960. Cheimarrichthys, excluded from the Pinguipedidae, is put into its own family, Cheimarrichthyidae.

A new species of the genus Acropoma (Perciformes: Acropomatidae) from the Philippines

Acropoma boholensis sp. nov. is described on the basis of two specimens collected from Dumaguete city market, Negros Island, Philippines. It is distinguished from other species of Acropoma by the following combination of characters: anus situated closer to the origin of pelvic fin than to that of anal fin; luminous gland extending from isthmus to anal fin base; scales cycloid except weakly ctenoid scales around anterior part of lateral line and on ventral side of body; proximal radial of first anal fin pterygiophore lacking trough or hollow; body depth 31%–33% SL; head length 40%–42% SL; length of orbit 13%–14% SL.

Redescription of Neoscombrops cynodon (Regan, 1921), a senior synonym of Neoscombrops annectens Gilchrist, 1922 (Perciformes: Acropomatidae)

Neoscombrops annectens Gilchrist, 1922, described from off Natal, South Africa, has long been regarded as a valid species. Although Acropoma cynodon Regan, 1921, also described from off Natal, was found to be Neoscombrops, they were regarded as distinct species, distinguishable by body depth and body color. Examination of many specimens, including the holotype of A. cynodon and neotype of N. annectens, revealed that the differences are within the range of intraspecific variation. N. cynodon is redescribed as a senior synonym of N. annectens.

A new pufferfish of the genus Torquigener that builds “mystery circles” on sandy bottoms in the Ryukyu Islands, Japan (Actinopterygii: Tetraodontiformes: Tetraodontidae)

Torquigener albomaculosus sp. nov. is described based on two specimens collected from sandy bottoms at depths of 15 and 18 m along the south coast of Amami-oshima Island in the Ryukyu Islands. This new species is distinguished from all other species of Torquigener by the following unique combination of characters: dorsal-fin rays 9 (10); anal-fin rays 6; pectoral-fin rays 16 (dorsalmost ray nubbin-like and rudimentary); vertebrae 8 + 11 = 19; no solid, dark, longitudinal stripe nor longitudinal rows of dark spots on the mid-side of body from behind pectoral fin to caudal-fin base; no vertical markings on cheek; dorsal half of head and body covered with fine brown reticulations and many white spots; ventral half of head and body silvery white covered by many white spots from chin to above anal-fin origin; dorsal rim of eye light yellow; and many two-rooted spinules on head and body. Males of T. albomaculosus build unique circles as spawning nests, these being 2 m in diameter on sandy bottoms at depths from 10 to 30 m at Amami-oshima Island.