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Relationships of the Chimaeriformes and the basal radiation of the Chondrichthyes
Abstract
The origin and early evolution of the cartilaginous fishes (Chondrichthyes) has been the subject of considerably more debate than of data. The two modern groups, Chimaeriformes and Elasmobranchii, differ so radically in morphology that in the past they have often been considered unrelated -- descended from some remote and unknown common ancestor. The current consensus promotes the Chimaeriformes and Elasmobranchii as sister taxa of the Class Chondrichthyes which are linked by an assemblage of Palaeozoic fossil taxa, but no taxonomic or phylogenetic scheme has been accepted for the Class. Of the two groups, the Chimaeriformes is the less understood. The few species of Chimaeriformes existing today are enigmatic, principally deeper-water fish that are not readily accessible for study. In the past the fossil record of both groups has been relatively scanty, primarily due to the poor potential for skeletal fossilization, and so has provided little useful input into fundamental discussions of vertebrate diversification. However, these situations are changing. Chimaerids are increasingly becoming the subject of renewed biological and limited fisheries interests. Regarding extinct chondrichthyans, the last 30 or so years have entailed discoveries of new fossils that illuminate our view of Palaeozoic life and are eliciting dramatic changes in our understanding of these early fishes, their relations, and the origins of jawed conditions.
Morphological examination of fossil chondrichthyans indicates that the plesiomorphous state of the gnathostome suspensorium is autodiastylic and that complex labial cartilages are primitive and likely to have been critical to the mechanical architecture of the first jaws. Analysis of cranial morphology, cranial proportions, the phyletic and developmental history of calcified tissues, and postcranial data including the evolution of the prepelvic tenaculum are now feasible. Cumulatively, when the results of these analyses are subject to cladistical evaluation, the result is one predominant cladogram supporting two monophyletic subclasses: the Elasmobranchii and the Euchondrocephali. The latter subclass contains a monophyletic group of holocephalans including the Cochliodontomorpha, and within this taxon, the restricted Chimaeriformes. Alternative cladograms of the non-holocephalan Euchondrocephali are dependent upon whether whole-body or cranial characters alone are employed in the analysis, or the additive or non-additive treatment of characters. Otherwise, only the discovery and description of additional members of this diverse assemblage are expected to alter these patterns of associations
... Recently the morphology of the pectoral fins of Cladoselache, a stem holocephalan, has been revised [32]; however, despite the availability of more complete pelvic material, a re-description has not taken into account features acknowledged to be misinterpreted in historical descriptions [33][34][35]. Chimaeroids are the only extant holocephalan chondrichthyans [8,36] and may serve as good models to investigate the evolution of the pelvic skeleton as they retain unfused pelvic girdles [37,38], which is considered the plesiomorphic condition of chondrichthyans [39,40]. There is only one morphological study of the chimaeroid appendicular skeleton development, that of the elephant shark (Callorhinchus milii), using wholemount clearing and alcian blue staining [41]. ...
... In contrast, in taxa from clades closer to the holocephalan and elasmobranch crown groups, such as the Chondrenchelyiformes [53,78,79], Iniopterygiformes [54,80], and Hybodontiformes [57,58,60,61,81,82], the majority of the fin radials articulate directly with a relatively larger and longer basipterygium. In extant holo-cephalans and elasmobranchs the pelvic fin radials articulate solely or almost exclusively with the basipterygium [40]. Our developmental data support the hypothesis [21,22] that the basipterygium in extant chondrichthyans develops from the fusion of fin radials during early development, prior to chondrification. ...
... This suggests that the developmental mechanism responsible for the alteration of the size and location of the basipterygium and whence the area of fin radial articulation over the course of the evolution of chondrichthyans is changes in the region and degree of radial fusion during early development. Remarkably, this developmental mechanism is likely an example of parallel evolution [83], as the fossil record of both the Elasmobranchii [58,59,61,81,82] and Holocephali [40,50,51,54,56,79,80,[84][85][86] would indicate that the resulting evolutionary transitions occurred independently (Figure 9). ...
Pelvic girdles, fins and claspers are evolutionary novelties first recorded in jawed vertebrates. Over the course of the evolution of chondrichthyans (cartilaginous fish) two trends in the morphology of the pelvic skeleton have been suggested to have occurred. These evolutionary shifts involved both an enlargement of the metapterygium (basipterygium) and a transition of fin radial articulation from the pelvic girdle to the metapterygium. To determine how these changes in morphology have occurred it is essential to understand the development of extant taxa as this can indicate potential developmental mechanisms that may have been responsible for these changes. The study of the morphology of the appendicular skeleton across development in chondrichthyans is almost entirely restricted to the historical literature with little contemporary research. Here, we have examined the morphology and development of the pelvic skeleton of a holocephalan chondrichthyan, the elephant shark (Callorhinchus milii), through a combination of dissections, histology, and nanoCT imaging and redescribed the pelvic skeleton of Cladoselache kepleri (NHMUK PV P 9269), a stem holocephalan. To put our findings in their evolutionary context we compare them with the fossil record of chondrichthyans and the literature on pelvic development in elasmobranchs from the late 19th century. Our findings demonstrate that the pelvic skeleton of C. milii initially forms as a single mesenchymal condensation, consisting of the pelvic girdle and a series of fin rays, which fuse to form the basipterygium. The girdle and fin skeleton subsequently segment into distinct components whilst chondrifying. This confirms descriptions of the early pelvic development in Scyliorhinid sharks from the historical literature and suggests that chimaeras and elasmobranchs share common developmental patterns in their pelvic anatomy. Alterations in the location and degree of radial fusion during early development may be the mechanism responsible for changes in pelvic fin morphology over the course of the evolution of both elasmobranchs and holocephalans, which appears to be an example of parallel evolution.
... Several cladograms that include both Squaloraja and crown group holocephalans (Grogan et al., 2012, fig. 1.1;Lund & Grogan, 1997;Lund et al., 2014, fig. 5(a); Stahl, 1999) differ somewhat in topology but all imply that such a divergence took place no later than the Serpukhovian (Late Mississippian), since it would have occurred prior to the appearance of Echinochimaera. ...
... One family (Squalorajidae) and one genus (Squaloraja). Squaloraja differs so much from other chimaeriforms that some place it in an order of its own (Lund & Grogan, 1997;Nelson et al., 2016). The classification used here is consistent with that used by Stahl (1999). ...
Squaloraja is a genus of chimaeriform fishes known from the Early Jurassic.
It has a dorsoventrally flattened body and a long median rostral cartilage. Males have a lance-like tenaculum that articulates with a central groove on the dorsal face of the median rostral cartilage. The genus is the only member of the family Squalorajidae, itself the only family in the suborder Squalorajoidei of the order Chimaeriformes. Phylogenetic analyses suggest a divergence of the Squalorajoidei from other Chimaeriformes in the Mississippian, implying the existence of a ghost lineage of more than 130 My. A spine that resembles a median rostral cartilage of a male Squaloraja was found in the St. Louis Formation (Visean) of Indiana, USA. As in Squaloraja, the dorsal face has a long narrow groove that would have articulated with a long narrow tenaculum. The spine is designated as the holotype of Sulcacanthus schachti, n. gen. et sp. Sulcacanthus is tentatively assigned to the
Squalorajoidei based on morphology, but the possibility of convergence cannot be eliminated.
A holocephalan tenaculum from the same locality might belong to the same taxon as
the median rostral cartilage but could also belong to the suborder Myriacanthoidei.
... Noggin4 has also disappeared in some elasmobranchs. At the same time, in Holocephali, which are considered a basally divergent group of the Chondrichthyes and sister group to elasmobranchs 35,36 , all three noggin genes characteristic of gnathostomes, including noggin1, were found. This indicates the secondary nature of the disappearance of noggin1 and noggin4 in more highly specialized representatives of elasmobranchs. ...
Secreted proteins of the Noggin family serve as pivotal regulators of early development and cell diferentiation in all multicellular animals, including vertebrates. Noggin1 was identifed frst among all Noggins. Moreover, it was described as the frst known embryonic inducer specifcally secreted by the Spemann organizer and capable of inducing a secondary body axis when expressed ectopically.
In the classical default model of neural induction, Noggin1 is presented as an antagonist of BMP signalling, playing a role as a neural inducer. Additionally, Noggin1 is involved in the dorsalization of embryonic mesoderm and later controls the diferentiation of various tissues, including muscles, bones, and neural crest derivatives. Hitherto, noggin1 was found in all studied vertebrates. Here,
we report the loss of noggin1 in elasmobranchs (sharks, rays and skates), which is a unique case among vertebrates. noggin2 and noggin4 retained in this group and studied in the embryos of the grey bamboo shark Chiloscyllium griseum revealed similarities in expression patterns and functional properties with their orthologues described in other vertebrates. The loss of noggin1 in elasmobranchs may be associated with histological features of the formation of their unique internal cartilaginous skeleton, although additional research is required to establish functional connections between these events.
... Noggin4 has also disappeared in some elasmobranchs. At the same time, in Holocephali, which are considered a basal divergent group of the Chondrichthyes and sister group to elasmobranchs 34,35 , all three noggin genes characteristic of gnathostomes, including noggin1, were found. This indicates the secondary nature of the disappearance of noggin1 and noggin4 in more highly specialized representatives of elasmobranchs. ...
Secreted proteins of the Noggin family serve as pivotal regulators of early development and cell differentiation in all multicellular animals, including vertebrates. Noggin1 was identified first among all Noggins. Moreover, it was described as the first known embryonic inducer specifically secreted by the Spemann organizer and capable of inducing a secondary body axis when expressed ectopically. In the classical default model of neural induction, Noggin1 is presented as an antagonist of BMP signalling, playing a role as a neural inducer. Additionally, Noggin1 is involved in the dorsalization of embryonic mesoderm and later controls the differentiation of various tissues, including muscles, bones, and neural crest derivatives. Hitherto, Noggin1 was found in all studied vertebrates. Here, we report the loss of noggin1 in elasmobranchs (sharks, rays and skates), which is a unique case among vertebrates. noggin2 and noggin4 retained in this group and studied in the embryos of the grey bamboo shark Chiloscyllium griseum revealed similarities in expression patterns and functional properties with their orthologues described in other vertebrates. The loss of noggin1 in elasmobranchs may be associated with histological features of the formation of their unique internal cartilaginous skeleton, although additional research is required to establish functional connections between these events.
... Subclass Euchondrocephali Lund and Grogan, 1997Order Iniopterygia Zangerl and Case, 1973Family Sibyrhynchidae Zangerl and Case, 1973 Sibyrhynchidae indet. (Fig. 7D-G) Material: One tooth whorl from sample VK3/19.83-19.95; ...
... The lateral regions of the girdle are penetrated by a variable number of obturator foramina for the passage of spinal nerves and blood vessels (Cappetta, 1987). The plesiomorphic condition of this structure is believed to consist of paired cartilages (Zangerl, 1981;Maisey, 1982;Coates and Gess, 2007) with radials articulating directly with the contralateral elements of the girdle (Lund and Grogan, 1997;Grogan et al., 2012). ...
The morphology of paired fins is commonly overlooked in morphological studies, particularly the pelvic girdle and fins. Consequently, previous phylogenetic studies incorporating morphological data used few skeletal characters from this complex. In this paper, the phylogenetic significance of pelvic articular characters for elasmobranchs is discussed in light of the morphological variation observed in 130 species, the most comprehensive study exploring the morphology of the pelvic girdle done so far. The 10 morphological characters proposed herein for the pelvic articulation were incorporated into a molecular matrix of NADH2 sequences and submitted to an analysis of maximum parsimony employing extended implied weighting. The most stable tree was selected based on the distortion coefficients, SPR distances (subtree pruning and regrafting) and fit values. Some of the striking synapomorphies recovered within elasmobranchs include the presence of an articular surface for the first enlarged pelvic radial supporting Elasmobranchii and the pelvic articular region for the basipterygium extending from the posterolatral margin of the pelvic girdle over its lateral surface in Echinorhinus + Hexanchiformes. Additionally, the proposed characters and their distributions are discussed considering the relationships recovered and also compared with previous morphological and molecular phylogenetic hypotheses.
The jaws and their supporting cartilages are tessellated in elasmobranchs and exhibit an abrupt increase in stiffness under compression. The major jaw‐supporting cartilage, the hyomandibula, varies widely by shape and size and the extent of the load‐bearing role is hypothesized to be inversely related to the number of craniopalatine articulations. Here, we test this hypothesis by evaluating the strength of the hyomandibular cartilage under compression in 13 species that represent all four jaw suspension systems in elasmobranchs (amphistyly, orbitostyly, hyostyly, and euhyostyly). The strength of the hyomandibular cartilages was measured directly using a material testing machine under compressive load, and indirectly by measuring morphological variables putatively associated with strength. The first measure of strength is force to yield ( F y ), which was the peak force (N) exerted on the hyomandibula before plastic deformation. The second measure was compressive yield strength ( σ y, also called yield stress), which is calculated as peak force (N) before plastic deformation/cross‐sectional area (mm ² ) of the specimen. Our results show that the load‐bearing role of the hyomandibular cartilage, as measured by yield strength, is inversely related to the number of craniopalatine articulations, as predicted. Force to yield was lower for euhyostylic jaw suspensions and similar for the others. We also found that mineralization is associated with greater yield strength, while the second moment of area is associated with greater force to yield.
The Paleozoic represents a key time interval in the origins and early diversification of chondrichthyans (cartilaginous fishes), but their diversity and macroevolution are largely obscured by heterogenous spatial and temporal sampling. The predominantly cartilaginous skeletons of chondrichthyans pose an additional limitation on their preservation potential and hence on the quality of their fossil record. Here, we use a newly compiled genus-level dataset and the application of sampling standardization methods to analyze global total-chondrichthyan diversity dynamics through time from their first appearance in the Ordovician through to the end of the Permian. Subsampled estimates of chondrichthyan genus richness were initially low in the Ordovician and Silurian but increased substantially in the Early Devonian. Richness reached its maximum in the middle Carboniferous before dropping across the Carboniferous/Permian boundary and gradually decreasing throughout the Permian. Sampling is higher in both the Devonian and Carboniferous compared with the Silurian and most of the Permian stages. Shark-like scales from the Ordovician are too limited to allow for some of the subsampling techniques. Our results detect two Paleozoic radiations in chondrichthyan diversity: the first in the earliest Devonian, led by acanthodians (stem-group chondrichthyans), which then decline rapidly by the Late Devonian, and the second in the earliest Carboniferous, led by holocephalans, which increase greatly in richness across the Devonian/Carboniferous boundary. Dispersal of chondrichthyans, specifically holocephalans, into deeper-water environments may reflect a niche expansion following the faunal displacement in the aftermath of the Hangenberg extinction event at the end of the Devonian.
A remarkable, complete specimen of a squalorajid holocephalian
is described for the first time from the Lower Jurassic (lower
Sinemurian) rocks of Osteno (Como, NW Italy). It is the only such
specimen known from the locality and belongs to a (possibly juvenile)
female. The Italian specimen is assigned to Squaloraja sp., and has a
large dorsoventrally flattened head, long rostrum, a single mandibular
tooth plate on each lower jaw, a well-developed synarcual, thick
notochordal sheath calcifications, and only slightly reduced squamation
comprising distinctive placoid scales with stellate bases. There
is no ethmoid canal, dorsal fin or fin spine. The Lower Jurassic succession
(‘Lower Lias’) of Lyme Regis (Dorset, UK) has yielded only
two incomplete purported female specimens of the type species of the
genus, Squaloraja polyspondyla, thus restricting potential comparison
with the Italian specimen. This new record of the genus expands the
known palaeogeographical distribution of this rare holocephalian.
Restudy of Campyloprion annectans Eastman, 1902 from North America demonstrated that neither specimen included is diagnostic at the species level; thus, the species name is a nomen dubium. Since this species was designated as the type species of the genus, this requires suppression of the generic name also. Another species earlier assigned to Campyloprion, Campyloprion ivanovi Karpinsky,
1924 is used as a type for a newly established genus Karpinskiprion Lebedev et Itano gen. nov. The composition of the family Helicoprionidae Karpinsky, 1911 is reviewed, and a new family Helicampodontidae Itano et Lebedev fam. nov. is erected.Anew specimen of Karpinskiprion ivanovi (Karpinsky, 1924) recently discovered in the Volgograd Region of Russia is the most complete Karpinskiprion specimen ever found. It unambiguously demonstrates the coiled nature of these tooth whorls and presents information on their developmental stages. During organogeny, cutting blades of the crown became reshaped, and basal spurs progressively elongated, forming a grater.Whorl growth occurred by addition of new crowns to the earlier mineralised base followed by later spur growth. In contrast to consistently uniform cutting blades, spurs are often malformed and bear traces of growth interruption. Both sides of the outer coil of the tooth whorl bear lifetime wear facets. The youngest (lingual) crowns are as yetunaffected by wear. The best-preserved facets show parallel radially directed scratch marks. The upper jaw dentition of Karpinskiprion is unknown, but we suggest that the faceted areas resulted from interaction with the antagonistic dental structures here. Three possible hypotheses for this interaction are suggested: (a) two opposing whorls acted as scissor blades, moving alternately from one side to another; (b) the lower tooth whorl fitted between paired parasymphyseal tooth whorls of the opposing jaw; or (c) the lower tooth whorl fitted into a dental pavement in the upper jaw.