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PubMed2004

A molecular test of alternative hypotheses of tetraodontiform (Acanthomorpha: Tetraodontiformes) sister group relationships using data from the RAG1 gene.

Two primary competing hypotheses regarding the identity of the sister group of the order Tetraodontiformes exist. The first hypothesis holds that some or all acanthuroid fishes represent the sister of Tetraodontiformes. The second, proposed in 1984 by Rosen, holds that the order Zeiformes is sister to Tetraodontiformes and that the family Caproidae is sister to this Zeiformes + Tetraodontiformes clade. These two hypotheses were tested using data from the single-copy nuclear gene RAG1. Representatives of most major orders of acanthomorph fishes were included to provide an appropriate context in which to place Tetraodontiformes and its hypothesized sister groups. The results of an unweighted parsimony analysis indicate that Zeiformes is not the sister group of Tetraodontiformes. In addition, Caproidae appears unrelated to Zeiformes. A monophyletic Tetraodontiformes was recovered as the sister group of the clade Ephippidae + Drepanidae and was more distantly related to the included zeiform and caproid representatives.

Animals↗
PubMed2005

A molecular analysis of the interrelationships of tetraodontiform fishes (Acanthomorpha: Tetraodontiformes).

Tetraodontiform fishes (e.g., triggerfishes, boxfishes, pufferfishes, and giant ocean sunfishes) have long been recognized as a monophyletic group. Morphological analyses have resulted in conflicting hypotheses of relationships among the tetraodontiform families. Molecular data from the single-copy nuclear gene RAG1 and from two mitochondrial ribosomal genes, 12S and 16S, were used to test these morphology-based hypotheses. Total evidence (RAG1+12S+16S), RAG1-only, and mitochondrial-only analyses were performed using both maximum parsimony and Bayesian criteria. Total evidence and RAG1-only analyses recover a monophyletic Tetraodontiformes. However, the relationships recovered within the order differ, and none completely conform to previous hypotheses. Analysis of mitochondrial data alone fails to recover a monophyletic Tetraodontiformes and therefore does not support any of the morphology-based topologies. The RAG1 data appear to give the best estimate of tetraodontiform phylogeny, resulting in many strongly supported nodes and showing a high degree of congruence between both parsimony and Bayesian analyses. All analyses recover every tetraodontiform family for which more than one representative is included as a strongly supported monophyletic group. Balistidae and Monacanthidae are recovered as sister groups with robust support in every analysis, and all analyses except the Bayesian analyses of the mitochondrial data alone recover a strongly supported sister-group relationship between Tetraodontidae and Diodontidae. Many of the intrafamilial relationships recovered from the molecular data presented here corroborate previous morphological hypotheses.

Animals↗
PubMed1986

Morphological studies of the spinal cord in tetraodontiformes fishes.

The spinal cord of two tetraodontiform fishes, the Japanese file fish (Navodon modestus) and the panther puffer (Takifugu pardalis), are unusual among vertebrates in having a markedly abbreviated spinal cord with a long and flattened filum terminale. Only the rostral short part of the cord of both species is cylindrical; the greater part of the cord is markedly flat. The majority of the spinal nerve roots leave the short cylindrical part. The flattened part of the cord contains the central canal, myelinated nerve fibers, and a few motoneurons surrounding the cauda equina, and it is histologically similar to the filum terminale of amphibians and mammals. The spinal cords of other teleosts, the sun-fish and angler, also are abbreviated and possess a filum terminale and cauda equina. These orders possess an enormous head and short trunk. However, the correlation between this body form and an abbreviated cord is not causal, since the tetraodontiform species described here show ordinary body proportions. The spinal cord may be abbreviated in tetraodontiform fishes in general.

Animals↗
PubMed1999

Evolution of complexity in motor patterns and jaw musculature of tetraodontiform fishes

The prey-processing behavior and jaw-adducting musculature of tetraodontiform fishes provide a novel system for studying the evolution of muscles and their function. The history of this clade has involved a pattern of repeated 'duplications' of jaw muscles by physical subdivision of pre-existing muscles. As a result, the number of adductor mandibulae muscles in different taxa varies from as few as two to as many as eight. We used electromyography (EMG) to quantify motor-pattern variation of adductor mandibulae muscles in four tetraodontiform species during feeding events on prey items that varied in durability and elusiveness. Statistical analyses of variation in EMG variables revealed significant differences in motor patterns between duplicated muscles derived from a common ancestral muscle in seven of nine cases examined. Overall individual EMG timing variables (e.g. relative onset or duration of bursts) were slightly less likely to diverge functionally than amplitude variables (e.g. relative intensity of bursts). Functional divergence was found in significant overall differences between muscles and twice as frequently in significant muscle-by-prey interaction terms. Such interactions represent an underappreciated way in which motor patterns can evolve and diversify. Regional variation was documented in undivided muscles in two species, indicating that it is possible for functional subdivision to precede anatomical subdivision. This study shows that phylogenetic increases in the number of tetraodontiform jaw adductor muscles have been associated with increases in the functional complexity of the jaws at the level of muscle activation patterns.

Journal Article↗
PubMed2001

Patterns of genome size evolution in tetraodontiform fishes.

We used flow cytometry to measure genome size in 15 species from seven families and subfamilies of tetraodontiform fishes. Previous studies have found that smooth pufferfishes (Tetraodontidae) have the smallest genome of any vertebrate measured to date (0.7-1.0 picograms diploid). We found that spiny pufferfishes (Diodontidae, sister group to the smooth puffers) possess a genome that is about two times larger (1.6-1.8 pg). Mola mola, a member of the sister group to Diodontidae and Tetraodontidae, also has a relatively large genome (1.7 pg). Parsimony analysis of this pattern indicates that the plesiomorphic condition for Molidae (Diodontidae, Tetraodontidae) is a genome size of 1.6-1.8 pg, and that tiny genome size is a derived character unique to smooth puffers. However, an alternative explanation is that the ancestor of Tetraodontidae acquired a heritable tendency toward decreasing genome size, such as a new or modified deletion mechanism, and genome size in all of the tetraodontid lineages has been decreasing in parallel since the split from Diodontidae. Small genome size (1.1-1.3 pg) also appears to have evolved independently in some members of Balistoidea (triggerfishes and filefishes) within Tetraodontiformes.

Animals↗
PubMed1998

Evolution of motor patterns in tetraodontiform fishes: does muscle duplication lead to functional diversification?

Several times within the teleost fish order Tetraodontiformes singular jaw adducting muscles have been effectively 'duplicated' by physical subdivision to produce new muscles. This morphological system provides an opportunity to investigate how the functional complexity of muscular systems changes with evolutionary increases in the number of component muscles. In this study we asked if muscle duplication has lead to functional diversification by comparing the motor patterns of muscles that result from subdivision events. The activity patterns of five different sets of duplicated muscles were quantified with electromyographic recordings (EMG) from four individuals in each of three species during processing of three prey types. Prey varied in durability and elusiveness (live fiddler crabs, pieces of squid tentacle and live paeneid shrimps). For each cycle of prey processing, measurements were made of the relative onset time of each adductor muscle, the duration of each burst of activity, and the relative intensity of each activity burst. Two types of functional divergence of muscles were observed in analyses of variance conducted on the EMG variables. In two of the 15 variables examined, the timing of activity of the descendant set of muscles differed. In another three of the 15 variables, there were significant interactions between muscle and prey type, indicating a prey effect which differed in the descendant muscles. Overall, evidence of motor divergence was found in three of five cases of muscle duplication. This indicates that muscle subdivision has led to increased functional complexity of the jaw-adductor muscle system in tetraodontiform fishes.

Animals↗
PubMed2005

Occipito-vertebral fusion in ocean sunfishes (Teleostei: Tetraodontiformes: Molidae) and its phylogenetic implications.

We describe the ontogeny of the occipital skull and anterior vertebrae of the molids Ranzania laevis and Masturus lanceolatus and compare it with that of the ostraciid Lactophrys sp. The first vertebra fuses to the basioccipital in early ontogeny in the two molids and previous authors thus confused that vertebra with the back of the basioccipital, so that all previous counts of their vertebral numbers are incorrect by one vertebra. As evidenced by Lactophrys sp., ostraciids are the only other tetraodontiforms with similar occipito-vertebral fusion. In contrast to the molids, additional anterior vertebrae fuse with this complex in ostraciids. We conclude that the shared occipito-vertebral fusion in molids and ostraciids and its otherwise extremely rare occurrence among teleosts provide support for a sister-group relationship of the two families.

Anatomy, Comparative↗
PubMed2006

The mitochondrial genome of spotted green pufferfish Tetraodon nigroviridis (Teleostei: Tetraodontiformes) and divergence time estimation among model organisms in fishes.

We determined the whole mitochondrial genome sequence for spotted green pufferfish, Tetraodon nigroviridis (Teleostei: Tetraodontiformes). The genome (16,488 bp) contained 37 genes (two ribosomal RNA genes, 22 transfer RNA genes, and 13 protein-coding genes) plus control region as found in other vertebrates, with the gene order identical to that of typical vertebrates. The sequence was used to estimate phylogenetic relationships and divergence times among major lineages of fishes, including representative model organisms in fishes. We employed partitioned Bayesian approaches for these two analyses using two datasets that comprised concatenated amino acid sequences from 12 protein-coding genes (excluding the ND6 gene) and concatenated nucleotide sequences from the 12 protein-coding genes (without 3rd codon positions), 22 transfer RNA genes, and two ribosomal RNA genes. The resultant trees from the two datasets were well resolved and largely congruent with those from previous studies, with spotted green pufferfish being placed in a reasonable phylogenetic position. The approximate divergence times between spotted green pufferfish and model organisms in fishes were 85 million years ago (MYA) vs. torafugu, 183 MYA vs. three-spined stickleback, 191 MYA vs. medaka, and 324 MYA vs. zebrafish, all of which were about twice as old as the divergence times estimated by their earliest occurrences in fossil records.

Animals↗
PubMed2002

Kudoa dianae sp. n. (Myxosporea: Multivalvulida), a new parasite of bullseye puffer, Sphoeroides annulatus (Tetraodontiformes: Tetraodontidae).

A new multivalvulid myxosporean species, Kudoa dianae sp. n., is described from bullseye puffer, Sphoeroides annulatus (Jenyns) (Tetraodontiformes: Tetraodontidae). Plasmodia develop in extramuscular sites, in the wall of oesophagus and less frequently on mesenteries. Mature spores can reach lumen of the digestive tract directly by disruption of plasmodial wall or via macrophage transport to the oesophageal epithelium. New species is characterised by morphology of spores and by the complete sequence of SSU rRNA gene that differs from all hitherto known sequences of Kudoa species. Spore morphology (moderate-sized, simple non-ornate spores, quadrate in apical view) clusters with that of Kudoa scienae, K. cerebralis, K. chilkaensis, K. leiostomi, K. finduli, K. cascasia and K. ovivora. Analysis of phylogenetic relationships (using SSU rRNA gene sequences) among five Kudoa species, the molecular data of which are available thus far, revealed that K. dianae is distinguishable from these five species and that its closest relation is with K. miniauiriculata.

Animals↗
PubMed2005

A revised diagnosis of Thylacicleidus (Monogenea: Dactylogyridae) with a redescription of the type species, Thylacicleidus serendipitus, and descriptions of two new species from Southeast Asian pufferfishes (Tetraodontiformes: Tetraodontidae).

Two new and 1 previously described species of Thylacicleidus Wheeler and Klassen, 1988, are reported from 2 species of brackish to freshwater puffers (Tetraodontidae) from Thailand. The generic diagnosis of Thylacicleidus is emended to incorporate the following characters: presence of a dextral muscular vagina, a vas deferens looping the left intestinal cecum, 2 prostatic reservoirs, a sclerotized tubular copulum without an accessory piece, and dorsal anchors with reduced outer root. The type species, Thylacicleidus serendipitus, is redescribed based on new information obtained from specimens found on the gills of the type host, Tetraodon nigroviridis Marion de Procé, 1822 (spotted green puffer). Two new species, Thylacicleidus latus n. sp. and Thylacicleidus brunensis n. sp., are described from the gills of T. nigroviridis and Tetraodon biocellatus Tirant, 1885 (eyespot puffer), respectively. The occurrence of common generic characters in species of Thylacicleidus and Haliotrema Johnston and Tiegs, 1922, another dactylogyrid genus recorded from tetraodontiform hosts, signifies the close relationship between the 2 genera and raises the question of synonymy. Nevertheless, because of morphological variability within Haliotrema spp., extremely wide host spectrum and the probable polyphyly of the genus, it is suggested that Thylacicleidus is a valid genus.

Animals↗
PubMed2000

Effects of prey type on motor pattern variance in tetraodontiform fishes.

It is unclear whether the high variance of electromyographic parameters measured in feeding teleost fishes reflects functionally significant motor variation that is under control of the fish, or functionally insignificant variation characteristic of EMG data. We addressed this issue by examining the effect of three prey, differing in physical characteristics, on the feeding motor pattern in three fishes of the Order Tetraodontiformes: the filefish, Monacanthus hispidus; the triggerfish, Balistes capriscus; and the puffer, Sphoeroides nephelus. EMG recordings were made from subdivisions of the mouth closing adductor mandibulae muscle and the mouth opening levator operculi muscle in four fish from each species feeding on live fiddler crabs, live shrimp, and pieces of cut squid mantle. Analysis of variance was used to test for effects of prey type on the standard deviation of muscle burst duration, burst onset time, and average burst amplitude in the adductor muscles. The filefish exhibited a doubling of standard deviation of burst duration in all muscles when feeding on fiddler crabs; triggerfish showed increased standard deviations in onset times and duration of two muscles when feeding on squid mantle; and the puffer showed no effects of prey on motor variability. The observation that prey type can elicit more than a doubling in the standard deviation of some EMG traits indicates that a large portion of the within-prey type variance is under direct control of the individual fish, suggesting an even greater level of fine motor control in teleost feeding mechanisms than previously recognized.

Animals↗
PubMed2005

Leis' conundrum: homology of the clavus of the ocean sunfishes. 2. Ontogeny of the median fins and axial skeleton of Ranzania laevis (Teleostei, Tetraodontiformes, Molidae).

One of the most conspicuous characters of the ocean sunfishes, family Molidae, is the punctuation of the body by a deep, abbreviated, caudal fin-like structure extending vertically between the posterior ends of the dorsal and anal fins, termed the clavus by Fraser Brunner. Homology of the clavus has been a matter of debate since the first studies on molid anatomy in the early 1800s. Two hypotheses have been proposed: 1) It is a highly modified caudal fin; 2) It is formed by highly modified elements of the dorsal and anal fins. To resolve this homology issue, we studied the ontogeny of the molid vertebral column and median fins and compared it to that of a less morphologically derived gymnodont (see Part 1 of this study), a member of the family Tetraodontidae. We show that in molids the chorda never flexes during development, that the claval rays form from the posterior ends of the dorsal and anal fins toward the middle, thus closing the gap inward, and that elements of the molid clavus have an identical development and composition as the proximal-middle and distal radials of the regular dorsal and anal fins. We thus conclude that the molid clavus is unequivocally formed by modified elements of the dorsal and anal fin and that the caudal fin is lost in molids.

Animals↗
PubMed2005

Leis' conundrum: homology of the clavus of the ocean sunfishes. 1. Ontogeny of the median fins and axial skeleton of Monotrete leiurus (Teleostei, Tetraodontiformes, Tetraodontidae).

We describe the ontogeny of the axial skeleton and median fins of the Southeast Asian freshwater puffer Monotrete leiurus, based on a reared developmental series. Most elements of the axial skeleton in M. leiurus arise in membrane bone. Only the base of the anterior three neural arches, the base of the hemal arches of the third preural centrum, the neural and hemal arches and spines of the second preural centrum, the parhypural, the two hypural plates, and the single epural are preformed in cartilage. In contrast to most teleosts, the proximal-middle radials of the dorsal and anal fins are upright and symmetrical and their distal tips coalesce during development to form a deep band of cartilage, from which the spherical distal radials are spatially separated.

Anatomy, Comparative↗
PubMed2006

Physical mapping of 5S and 45S rDNA loci in pufferfishes (Tetraodontiformes).

Chromosomal features, location and variation of the major and minor rDNA genes cluster were studied in three pufferfish species: Sphoeroides greeleyi and Sphoeroides testudineus (Tetraodontidae) and Cyclichthys spinosus (Diodontidae). The location of the major rDNA was revealed with an 18S probe in two loci for all species. The minor rDNA loci (5S rDNA) was found in one chromosome pair in tetraodontid fishes and four sites located on two distinct chromosomal pairs in C. spinosus. A syntenical organization was not observed among the ribosomal genes. Signal homogeneity for GC/AT-DNA specific fluorochromes was observed in diodontid fish except in the NORs regions, which were CMA3-positive. Giemsa karyotypes of tetraodontid species presents 2n=46, having the same diploid value of other Sphoeroides species that have been investigated. On the other hand, the karyotype of C. spinosus, described for the first time, shows 2n=50 chromosomes (4m+18sm+12st+16a). The foreknowledge of the karyotypic structure of this group and also the physical mapping of certain genes could be very helpful for further DNA sequence analysis.

Animals↗
PubMed1990

Structure of the corpuscles of Stannius in the euryhaline teleost Takifugu niphobles (Tetraodontiformes, Teleostei), with special regard to vascularization and extravascular channel system.

Vascularization and the extravascular channel system of the corpuscles of Stannius in a euryhaline teleost, Takifugu niphobles, were studied by scanning electron microscopy of the vascular corrosion cast, and histochemistry of exogenously injected horseradish peroxidase as a macromolecular tracer. The corpuscles were apposed to the caudal part of the ureter, away from the mesonephric kidney, and were supplied with arterioles from the genital artery running ventrally as a ramus of the dorsal aorta. Elaborate capillary networks irrigating the glandular lobules were collected by the venules to drain into the posterior cardinal veins. Electron microscopic examination of the glands demonstrated two types of secretory cells, type-1 cells with large granules, and type-2 cells with smaller granules. The type-1 cells, predominating in the gland, occasionally showed exocytosis of the secretory granules, mainly into intercellular spaces between adjoining cells. Exocytosis was also evident in the type-2 cells. The tracer molecule injected was visualized histochemically within the capillary lumina and intercellular spaces throughout the gland. The labelled spaces intercommunicated with each other to form an extensive extravascular channel system as a diffusing pathway within the gland. The possible role of this system in hormone transport and/or storage was discussed.

Animals↗
PubMed2001

Molecular phylogeny and species identification of pufferfish of the genus Takifugu (Tetraodontiformes, Tetraodontidae).

The phylogenetic relationships and species identification of pufferfishes of the genus Takifugu were examined by use of randomly amplified polymorphic DNA (RAPD) and sequencing of the amplified partial mitochondrial 16S ribosomal RNA genes. Amplifications with 200 ten-base primers under predetermined optimal reaction conditions yielded 1962 reproducible amplified fragments ranging from 200 to 3000 bp. Genetic distances between 5 species of Takifugu and Lagocephalus spadiceus as the outgroup were calculated from the presence or absence of the amplified fragments. Approximately 572 bp of the 16S ribosomal RNA gene was amplified, using universal primers, and used to determine the genetic distance values. Topological phylogenic trees for the 5 species of Takifugu and outgroup were generated from neighbor-joining analysis based on the data set of RAPD analysis and sequences of mitochondrial 16S rDNA. The genetic distance between Takifugu rubripes and Takifugu pseudommus was almost the same as that between individuals within each species, but much smaller than that between T. rubripes, T. pseudommus, and the other species. The molecular data gathered from both analysis of mitochondria and nuclear DNA strongly indicated that T. rubripes and T. pseudommus should be regarded as the same species. A fragment of approximately 900 bp was amplified from the genome of all 26 T. pseudommus individuals examined and 4 individuals of intermediate varieties between T. rubripes and T. pseudommus. Of the 32 T. rubripes individuals, only 3 had the amplified fragment. These results suggest that this fragment may be useful in distinguishing between T. rubripes and T. pseudommus.

Journal Article↗
PubMed1993

Enameloid formation in two tetraodontiform fish species with high and low fluoride contents in enameloid.

Forming teeth of parrotfish and pufferfish were viewed by transmission electron microscopy to correlate cytological features of the enameloid organ with the species' fluoride (F) content in mature enameloid. Secretory-stage inner dental epithelial cells (IDE) of parrotfish (high F) and pufferfish (low F) secreted procollagen granules into the enameloid collagen matrix. The odontoblasts of both species, less numerous than IDE cells, also contained procollagen granules at the enameloid matrix formation stage. After the full thickness of enameloid matrix collagen had been deposited, enameloid crystallites formed parallel to the long axis of the enameloid collagen fibres. Concurrently, the plasma membranes of the outer dental epithelial cells (ODE) became invaginated in both species, but to a much greater extent in parrotfish. Highly undulating parrotfish ODE cells surrounded numerous fenestrated capillaries. In contrast, pufferfish ODE cells remained straight with few adjacent capillaries. Extensive tight junctions formed between ODE and IDE cells of both species, sealing the extracellular space. With increased mineralization, enameloid collagen fibres were no longer discernible. A thin layer of amorphous material, which subsequently mineralized, was secreted on to the enameloid surface by IDE cells in both species. Pufferfish odontoblasts secreted a mineralizing amorphous layer on the pulpal aspect of the enameloid. The results suggest that at the mineralization stage, a triad of cytostructural features, highly invaginated ODE cells, highly vascularized ODE cells, and extensive tight junctions are strongly correlated with high fluoride content of mature enameloid mineral. Species without any one of these features have lower fluoride in the enameloid.

Animals↗
PubMed1993

A new species of Haliotrema (Monogenea: Ancyrocephalidae) from a Japanese puffer fish Takifugu niphobles (Tetraodontiformes: Tetraodontidae).

A new species of Haliotrema is described on the basis of material from the gills of the Japanese puffer fish Takifugu niphobles. The new species is compared to other ancyrocephalids from tetraodontid hosts and congeners with similar copulum morphology from unrelated hosts. It is distinguished from these species based on a combination of reproductive and haptoral characters. Comparison of the haptor musculature of the new species with that described for Haliotrema balisticus revealed a potential for additional taxonomic characters. Resolution of differences in the interpretation of the functional morphology of the muscle groups in the two species will require further investigation.

Animals↗