Molecular and karyological aspects of Batoidea (Chondrichthyes, Elasmobranchi) phylogeny

Although considerable progress has been made in elucidating the relationships within the Chondrichthyes, there is no agreement as it concerns the systematics of Batoidea, the most derived superorder among cartilaginous fishes, and many different interpretations exist. Our investigation provides the first assessment of relationships among the described batoid species using sequences from both mtDNA and nuclear genes as well as karyological morphology. Our work consists primarily in reconstructing the phylogenetic relationships of Batoidea by examining the mtDNA (16S) and nuclear gene (18S) sequences from 11 batoid species. The three analytical methods (NJ, MP and Bayesian analysis) grouped Rajiformes, Myliobatiformes and Rhinobatiformes. In these trees the two torpedoes diverge from the other batoid fishes. We also compare the molecular data with the available karyological evidence, which consist of the diploid number and the karyotype morphology of eight species belonging to the four orders examined. The results show that the karyological structure in the different species is generally consistent with the various phylogenetical trees, and that Torpediniformes confirm their unique genome organization.     

Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea)

Skates, rays and allies (Batoidea) comprise more than half of the species diversity and much of the morphological disparity among chondrichthyan fishes, the sister group to all other jawed vertebrates. While batoids are morphologically well characterized and have an excellent fossil record, there is currently no consensus on the interrelationships of family-level taxa. Here we construct a resolved, robust and time-calibrated batoid phylogeny using mitochondrial genomes, nuclear genes, and fossils, sampling densely across taxa. Data partitioning schemes, biases in the sequence data, and the relative informativeness of each fossil are explored. The molecular phylogeny is largely congruent with morphology crownward in the tree, but the branching orders of major batoid groups are mostly novel. Body plan convergence appears to be widespread in batoids. A depressed, rounded pectoral disk supported to the snout tip by fin radials, common to skates and stingrays, is indicated to have been derived independently by each group, while the long, spiny rostrum of sawfishes similarly appears to be convergent with that of sawsharks, which are not batoids. The major extant batoid lineages are inferred to have arisen relatively rapidly from the Late Triassic into the Jurassic, with long stems followed by subsequent radiations in each group around the Cretaceous/Tertiary boundary. The fossil record indicates that batoids were affected with disproportionate severity by the end-Cretaceous extinction event.     

The morphology and evolution of the ventral gill arch skeleton in batoid fishes (Chondrichthyes: Batoidea)

The ventral gill arch skeleton was examined in some representatives of batoid fishes. The homology of the components was elucidated by comparing similarities and differences among the components of the ventral gill arches in chondrichthyans, and attempts were made to justify the homology by giving causal mechanisms of chondrogenesis associated with the ventral gill arch skeleton. The ceratohyal is present in some batoid fishes, and its functional replacement, the pseudohyal, seems incomplete in most groups of batoid fishes, except in stingrays. The medial fusion of the pseudohyal with successive ceratobranchials occurs to varying degrees among stingray groups. The ankylosis between the last two ceratobranchials occurs uniquely in stingrays, and it serves as part of the insertion of the last pair of coracobranchialis muscles. The basihyal is possibly independently lost in electric rays, the stingray genus Urotrygon (except U. daviesi) and pelagic myiiobatoid stingrays. The first hypobranchial is oriented anteriorly or anteromedially, and it varies in shape and size among batoid fishes. It is represented by rami projecting posterolaterally from the basihyal in sawfishes, guitarfishes and skates. It consists of a small piece of cartilage which extends anteromedially from the medial end of the first ccratobranchial in electric rays. It is a large cartilaginous plate in most of stingrays. It is absent in pelagic myliobatoid stingrays. The remaining hypobranchial cartilages also vary in shape and size among batoid fishes. Torpedo and possibly the Jurassic Belemnobalis and Spathobatis possess the generalized or typical chondrichthyan ventral gill arch structure in which the hypobranchials form a Σ-shaped pattern. In the electric ray Hypnos and narkinidid and narcinidid electric rays, the hypobranchial components are oriented longitudinally along the mid-portion of the ventral gill arches. They form a single cartilaginous plate in the narkinidid electric rays, Narcine and Diplobatis. In guitarfishes and skates, the second hypobranchial is unspecialized, and in skates, it does not have a direct contact with the second ceratobranchial. In both groups, the third and fourth hypobranchials are composed of a small cartilage which forms a passage for the afferent branches of the ventral aorta and serve as part of the insertion of the coracobranchialis muscle. In sawfishes and stingrays, the hypobranchials appear to be included in the medial plate. In sawfishes, the second and third components separately chondrify in adults, but the fourth component appears to be fused with the middle medial plate. In stingrays, a large medial plate appears to include the second through to the last hypobranchial and most of the basibranchial copulae. The medial plate probably develops independently in sawfishes and stingrays. Because the last basibranchial copula appears to be a composite of one to two hypobranchials and at least two basibranchial copulae, the medial plate may be formed by several developmental processes of chondrogenesis. More detailed comparative anatomical and developmental studies are needed to unveil morphogenesis and patternings of the ventral gill arch skeleton in batoid fishes.     

Evidence of brain-warming in the mobulid rays, Mobula tarapacana and Manta birostris (Chondrichthyes: Elasmobranchii: Batoidea: Myliobatiformes)

The presence of cranial retia mirabilia in rays of the genus Mobula is well established. Although previously regarded as consisting exclusively of arteries, the presence of veins has now been established in gross dissections of the rete in the mobulid, Manta birostris. Histological examination of the retia in Manta birostris and Mobula tarapacana confirms the presence of veins. These findings suggest the presence of a counter-current heat-exchanger that warms the brain.     

Evidence of a counter-current heat exchanger in the ray, Mobula tarapacana (Chondrichthyes: Elasmobranchii: Batoidea: Myliobatiformes)

A vascular network, or rete, has been found in the pectoral fin of the mobulid ray, Mobula tarapacana. This rete appears to be a counter-current heat exchanger which, in conjunction with a high level of red muscle, indicates that this ray is warm-bodied. Preliminary results on other closely related rays indicate that retia may be more common amongst the rays than previously thought.     

Development of the Synarcual in the Elephant Sharks (Holocephali; Chondrichthyes): Implications for Vertebral Formation and Fusion

The synarcual is a structure incorporating multiple elements of two or more anterior vertebrae of the axial skeleton, forming immediately posterior to the cranium. It has been convergently acquired in the fossil group ‘Placodermi’, in Chondrichthyes (Holocephali, Batoidea), within the teleost group Syngnathiformes, and to varying degrees in a range of mammalian taxa. In addition, cervical vertebral fusion presents as an abnormal pathology in a variety of human disorders. Vertebrae develop from axially arranged somites, so that fusion could result from a failure of somite segmentation early in development, or from later heterotopic development of intervertebral bone or cartilage. Examination of early developmental stages indicates that in the Batoidea and the ‘Placodermi’, individual vertebrae developed normally and only later become incorporated into the synarcual, implying regular somite segmentation and vertebral development. Here we show that in the holocephalan Callorhinchus milii, uniform and regular vertebral segmentation also occurs, with anterior individual vertebra developing separately with subsequent fusion into a synarcual. Vertebral elements forming directly behind the synarcual continue to be incorporated into the synarcual through growth. This appears to be a common pattern through the Vertebrata. Research into human disorders, presenting as cervical fusion at birth, focuses on gene misexpression studies in humans and other mammals such as the mouse. However, in chondrichthyans, vertebral fusion represents the normal morphology, moreover, taxa such Leucoraja (Batoidea) and Callorhinchus (Holocephali) are increasingly used as laboratory animals, and the Callorhinchus genome has been sequenced and is available for study. Our observations on synarcual development in three major groups of early jawed vertebrates indicate that fusion involves heterotopic cartilage and perichondral bone/mineralised cartilage developing outside the regular skeleton. We suggest that chondrichthyans have potential as ideal extant models for identifying the genes involved in these processes, for application to human skeletal heterotopic disorders.     

Diversification and species boundaries of Rhinebothrium (Cestoda; Rhinebothriidea) in South American freshwater stingrays (Batoidea; Potamotrygonidae)

Background

Neotropical freshwater stingrays (Batoidea: Potamotrygonidae) host a diverse parasite fauna, including cestodes. Both cestodes and their stingray hosts are marine-derived, but the taxonomy of this host/parasite system is poorly understood.

Methodology

Morphological and molecular (Cytochrome oxidase I) data were used to investigate diversity in freshwater lineages of the cestode genus Rhinebothrium Linton, 1890. Results were based on a phylogenetic hypothesis for 74 COI sequences and morphological analysis of over 400 specimens. Cestodes studied were obtained from 888 individual potamotrygonids, representing 14 recognized and 18 potentially undescribed species from most river systems of South America.

Results

Morphological species boundaries were based mainly on microthrix characters observed with scanning electron microscopy, and were supported by COI data. Four species were recognized, including two redescribed (Rhinebothrium copianullum and R. paratrygoni), and two newly described (R. brooksi n. sp. and R. fulbrighti n. sp.). Rhinebothrium paranaensis Menoret & Ivanov, 2009 is considered a junior synonym of R. paratrygoni because the morphological features of the two species overlap substantially. The diagnosis of Rhinebothrium Linton, 1890 is emended to accommodate the presence of marginal longitudinal septa observed in R. copianullum and R. brooksi n. sp. Patterns of host specificity and distribution ranged from use of few host species in few river basins, to use of as many as eight host species in multiple river basins.

Significance

The level of intra-specific morphological variation observed in features such as total length and number of proglottids is unparalleled among other elasmobranch cestodes. This is attributed to the large representation of host and biogeographical samples. It is unclear whether the intra-specific morphological variation observed is unique to this freshwater system. Nonetheless, caution is urged when using morphological discontinuities to delimit elasmobranch cestode species because the amount of variation encountered is highly dependent on sample size and/or biogeographical representation.     

Interrelationships of the durophagous stingrays (Batoidea: Myliobatidae)

In the last few years, estimates of the patterns and timing of the evolution of the pelagic, durophagous stingrays (Myliobatidae) have improved through new comparative data from morphology, the fossil record, and DNA sequences. These recent studies are here reviewed and a conservative summary of myliobatid diversification and origins is presented. The interrelationships and morphological evolution of the durophagous stingrays are discussed, including the nature of devil rays as derived myliobatids. An exploration of myliobatid origins includes estimates of the timing of their diversification and an assessment of gymnurids as a possible sister group. The prevailing signal suggests that the most recent common ancestor of extant myliobatids was a Late Cretaceous oscillating swimmer with a pavement-like dentition. The devil ray lineage began the transition to planktivory by at least the Oligocene, with dentition gradually reduced from grinding plates of interlocking elements to long rows of homodont teeth. Finally, the validity of the genera Manta (Bancroft, 1829) and Pteromylaeus (Garman, 1913) are called into question.     

A review of the sensory biology of chimaeroid fishes (Chondrichthyes; Holocephali)

The chimaeroid fishes (Chondrichthyes: Holocephali) are a small, ancient and poorly studied group of cartilaginous fishes that have puzzled and intrigued taxonomists, ichthyologists and evolutionary biologists for over 100 years. Like their close relatives, the elasmobranchs (sharks, skates and rays), chimaeroids possess an extensive battery of sense organs that allow them to detect information about the external environment in order to find mates, locate food and preferred habitats and avoid predators. In recent years the sensory systems of elasmobranchs have received an up-swell of attention from biologists, which has resulted in a greater understanding of the sensory capabilities and behaviour of these fishes. However, very little recent work has been done on the chimaeroids. The aim of this review is to provide a survey of the existing literature on the major senses (vision, smell, taste, mechanoreception, hearing and electroreception) in chimaeroids, in order to stimulate and identify areas for future research. In chimaeroids information on sensory systems is largely restricted to one or two species (with the exception of some aspects of the visual system) and for some sensory systems essentially nothing is known. Most studies are anatomical in nature and so there is a demand for a greater degree of neurophysiological and behavioural assessment of sensory capability in these fishes. The majority of chimaeroids occupy deep-sea habitats and are becoming increasingly threatened by the expansion of deep-sea fisheries, so an understanding of the sensory biology and behaviour of chimaeroids may be important for the protection and management of these fascinating fishes.     

Edgeworth's legacy of cranial muscle development with an analysis of muscles in the ventral gill arch region of batoid fishes (Chondrichthyes: Batoidea).

A series of studies by Edgeworth demonstrated that cranial muscles of gnathostome fishes are embryologically of somitic origin, originating from the mandibular, hyoid, branchial, epibranchial, and hypobranchial muscle plates. Recent experimental studies using quail-chick chimeras support Edgeworth's view on the developmental origin of cranial muscles. One of his findings, the existence of the premyogenic condensation constrictor dorsalis in teleost fishes, has also been confirmed by molecular developmental studies. Therefore, developmental mechanisms for patterning of cranial muscles, as described and implicated by Edgeworth, may serve as structural entities or regulatory phenomena responsible for developmental and evolutionary changes. With Edgeworth's and other studies as background, muscles in the ventral gill arch region of batoid fishes are analyzed and compared with those of other gnathostome fishes. The spiracularis is regarded as homologous at least within batoid fishes, but its status within elasmobranchs remains unclear; developmental modifications of the spiracularis proper are evident in some batoid fishes and in several shark groups. The peculiar ventral extension of the spiracularis in electric rays and some stingrays may represent convergence, probably facilitating ventilation and/or feeding in both groups. The evolutionary origin of the "internus" and "externus" remains uncertain, despite the fact that a variety of forms of the constrictor superficiales ventrales in batoid fishes indicates an actual medio-ventral extension of the "externus." The intermandibularis is probably present only in electric rays. The "X" muscle occurs only in electric rays and is considered to be Edgeworth's intermandibularis profundus. Its association with the adductor mandibular complex in narkinidid and narcinidid electric rays may relate to its functional role in lower jaw movement. Contrary to common belief, in most batoid fishes as well as some sharks, muscles that originate from the branchial muscle plate and extend medially in the ventral gill arches do exist: the medial extension of the interbranchiales in most batoid fishes and some sharks and the "Y" muscle in the pelagic stingrays Myliobatos and Rhinoptera. The latter is another example of the medial extension of the "internus." Whether the interbranchiales and "Y" muscle are homologous within elasmobranchs and whether homologous with the obliques ventrales and/or transversi ventrales of osteichthyan fishes await further research. Four hypobranchial muscles are recognized in batoid fishes: the coracomandibularis, coracohyoideus, coracoarcualis, and coracohyomandibularis. The coracohyoideus is discrete from the coracoarcualis; its complete structural separation from the latter occurs in several groups of batoid fishes.(ABSTRACT TRUNCATED AT 400 WORDS)     

Monophyly, phylogeny and systematic position of the †Synechodontiformes (Chondrichthyes, Neoselachii)

Klug, S. (2009). Monophyly, phylogeny and systematic position of the †Synechodontiformes (Chondrichthyes, Neoselachii). — Zoologica Scripta, 39 , 37–49.
Identifying the monophyly and systematic position of extinct sharks is one of the major challenges in reconstructing the phylogeny and evolutionary history of sharks in general. Although great progress has been accomplished in the last few decades with regard to resolving the interrelationships of living sharks, a comprehensive phylogeny identifying the systematic position of problematic or exclusively fossil taxa is still lacking. Fossil taxa traditionally assigned to synechodontiform sharks are very diverse with a fossil record extending back into the Palaeozoic but with uncertain inter- and intrarelationships. Here, phylogenetic analyses using robust cladistic principles are presented for the first time to evaluate the monophyly of this group, their intrarelationships and their systematic position within Neoselachii. According to the results of this study, taxa assigned to this group form a monophyletic clade, the †Synechodontiformes. This group is sister to all living sharks and displays a suite of neoselachian characters. Consequently, the concept of neoselachian systematics needs to be enlarged to include this completely extinct group, which is considered to represent stem-group neoselachians. The origin of modern sharks can be traced back into the Late Permian (250 Mya) based on the fossil record of †Synechodontiformes. The systematic position of batoids remains contradictory, which relates to the use of different data (molecular vs. morphological) in phylogentic analyses.     

Life-history traits of batoids (Superorder Batoidea) in the Northeast Atlantic and the Mediterranean

Reviews in Fish Biology and Fisheries - Life-history traits provide a way to estimate the vulnerability of both individuals and populations of a species to disturbance (e.g., overexploitation,...     

Chemosensory cells in the oral epithelium of Raja clavata (Chondrichthyes)

Examination by scanning and transmission electron microscopy (SEM and TEM) has found no actual taste buds in the mouth of Raja clavata. Prominences of the epithelium on the roof and floor of the mouth, and on the oral valves, contain large numbers of innervated bipolar cells, not associated in the form of taste buds, with a cytology intimating that they have a chemosensory function. The apices of these sensory cells, each bearing a group of microvilli, protrude between the superficial epithelial cells. Neurite profiles are associated with the sensory cells; synaptic specializations are marked by a cluster of vesicles with inconspicuous dense cores and some densities on the cell membrane. Shrunken, electron-dense, cell profiles are interpreted as apoptotic. Shrunken sensory cell profiles are commoner than similar epithelial cells, especially in young individuals, indicating a relatively rapid turnover of sensory cells. The epithelium contains a variety of granulocytic leucocytes, some of which contain large phagosomes.     

Molecular and chromosomal analysis of ribosomal cistrons in two cartilaginous fish, <Emphasis Type="Italic">Taeniura lymma</Emphasis> and <Emphasis Type="Italic">Raja montagui</Emphasis> (Chondrichthyes,Batoidea)

We used silver nitrate staining, CMA₃ and FISH to study the chromosomal localization of both the major ribosomal genes and the nucleolar organizer regions as well as that of the minor ribosomal genes (5S rDNA) in two species of Batoidea, Taeniura lymma (Dasyatidae) and Raja montagui (Rajidae). In both species, all the metaphases examined showed the presence of multiple NOR-bearing sites, while the gene for 5S rRNA proved to be localized on two chromosome pairs. Furthermore, one of the two 5S rDNA sites in T. lymma was shown to be co-localized with the major ribosomal cluster. The presence of multiple nucleolar organizer regions in the two species might be interpreted as being the result of intraspecific polymorphisms, or as a phenomenon of the amplified transposition of mobile elements of the genome. We also determined the nucleotide sequence of the 5S rRNA gene, consisting of 564 bp in R. montagui and 612 bp in T. lymma. We also found TATA-like and (TGC)_n trinucleotides, (CA)_n dinucleotides and (GTGA)_n tetranucleotides, which probably influence gene regulation.     

Teeth of Embryos in Lamniform Sharks (Chondrichthyes: Elasmobranchii)

The dentitions of lamniform sharks possess a unique heterodonty, the lamnoid tooth pattern. However, in embryos, there are 'embryonic' and 'adult' dentitions. The teeth in the embryonic dentition are peg-like and appear to be attached to the jaw in an acrodont fashion. The adult dentition is characterized by the presence of replacement tooth series with the lamnoid tooth pattern. The embryonic–adult transition in dentitions appears at around 30–60cm TL. Tooth replacement generally begins before birth in embryos with adult dentitions. The adult dentition becomes functional just before or after parturition. An embryo of one species (Lamna nasus) shows a tooth directly on the symphysis of the upper jaws, marking the first record of a medial tooth for the order Lamniformes.     

Early scale development in Heterodontus (Heterodontiformes; Chondrichthyes): a novel chondrichthyan scale pattern

In two species of Heterodontus, H. portusjacksoni and H. galeatus, the first scales to develop form two opposing rows along the caudal fin axis on both the left and right sides of the fin. The opposing rows originate from an initial scale located on either side of the posterior tip of the caudal fin, with subsequent scales erupting in a posterior to anterior direction along the tail axis. These scale rows may strengthen tail movements, providing aeration in the egg case, but are lost later in ontogeny. Development of subsequent body scales shows a more irregular origin and arrangement, from anterior to posterior, to cover the dorsal and ventral lobes of the caudal fin. Although the early developmental pattern of the scale associated with the Heterodontus caudal fin has not been previously described, several chondrichthyan taxa, including chimeroids, likewise possess ordered rows of flank scales early in ontogeny that are subsequently lost. These ordered scales contrast with previous suggestions that chondrichthyan scale development is entirely random. Instead, regulated and sequential development of scales may be a plesiomorphic character for both chondrichthyans and osteichthyans, with the less organized arrangement in later ontogenetic stages being a derived condition within Chondrichthyes.     

Tooth replacement in the bowfin (Amia calva — Holostei)

The dissected tooth bearing bones of 20 specimens of Amia calva (Pisces:Holostei) ranging from the third to tenth season have been examined radiographically and in alizarin red S stained and cleared specimens. Although forms of alternate (1:1) tooth series replacement (sensu Edmund, '60) were frequently observed, even in the youngest, immature specimens, many examples of irregular replacement were recorded. In several bones, the maxillae in particular, series with every third (2:1) or fourth (3:1) tooth replacing were seen and possible patterns of 2:2, were recorded. It is concluded that these data are not consistent with the Zahnreihen concept but support a morphogenic field concept of tooth development.