Rostral and body shape analyses reveal cryptic diversity of Late Jurassic batomorphs (Chondrichthyes, Elasmobranchii) from Europe.

The fossil record of chondrichthyans (chimaeras, sharks, rays and skates) consists largely of isolated teeth, with holomorphic specimens being extraordinary exceptions. However, numerous of these more or less completely preserved specimens are known from several Upper Jurassic deposits of Europe, enabling detailed analysis of their morphology. Batomorphs (rays and skates) resembling modern guitarfishes and wedgefishes (Rhinopristiformes) are among the most common Jurassic chondrichthyans found, but they have been only sporadically studied up to now, resulting in large knowledge gaps concerning their taxonomy and phylogeny. Here, we present the most detailed revision of Late Jurassic holomorphic batomorphs to date, quantitatively analysing body proportions of specimens from Germany (Solnhofen Archipelago), France (Cerin) and the UK (Kimmeridge), using both geometric and traditional morphometrics. Furthermore, we identify qualitative morphological characters for species discrimination, to clarify the taxonomic identity and diversity of Late Jurassic batomorphs based on holomorphic specimens. Our results support the validity of Belemnobatis sismondae, Kimmerobatis etchesi and Spathobatis bugesiacus, as well as that of the previously doubtful Asterodermus platypterus. Moreover, we describe Aellopobatis bavarica, a new taxon, which has hitherto been considered to be a large-sized morphotype of Spathobatis bugesiacus. Our results highlight that the diversity of holomorphic batomorphs during the Late Jurassic was greater than previously thought, and suggest that this group was already well-established and diverse by this time. This study thus provides vital information about the evolutionary history of Late Jurassic batomorphs and has direct implications for batomorph species that are based on isolated teeth only.

Shark mandible evolution reveals patterns of trophic and habitat-mediated diversification.

Environmental controls of species diversity represent a central research focus in evolutionary biology. In the marine realm, sharks are widely distributed, occupying mainly higher trophic levels and varied dietary preferences, mirrored by several morphological traits and behaviours. Recent comparative phylogenetic studies revealed that sharks present a fairly uneven diversification across habitats, from reefs to deep-water. We show preliminary evidence that morphological diversification (disparity) in the feeding system (mandibles) follows these patterns, and we tested hypotheses linking these patterns to morphological specialisation. We conducted a 3D geometric morphometric analysis and phylogenetic comparative methods on 145 specimens representing 90 extant shark species using computed tomography models. We explored how rates of morphological evolution in the jaw correlate with habitat, size, diet, trophic level, and taxonomic order. Our findings show a relationship between disparity and environment, with higher rates of morphological evolution in reef and deep-water habitats. Deep-water species display highly divergent morphologies compared to other sharks. Strikingly, evolutionary rates of jaw disparity are associated with diversification in deep water, but not in reefs. The environmental heterogeneity of the offshore water column exposes the importance of this parameter as a driver of diversification at least in the early part of clade history.

A Synoptic Review of the Cartilaginous Fishes (Chondrichthyes: Holocephali, Elasmobranchii) from the Upper Jurassic Konservat-Lagerstätten of Southern Germany: Taxonomy, Diversity, and Faunal Relationships.

The Late Jurassic-Early Cretaceous (164-100 Ma) represents one of the main transitional periods in life history. Recent studies unveiled a complex scenario in which abiotic and biotic factors and drivers on regional and global scales due to the fragmentation of Pangaea resulted in dramatic faunal and ecological turnovers in terrestrial and marine environments. However, chondrichthyan faunas from this interval have received surprisingly little recognition. The presence of numerous entire skeletons of chondrichthyans preserved in several localities in southern Germany, often referred to as Konservat-Lagerstätten (e.g., Nusplingen and the Solnhofen Archipelago), provides a unique opportunity of to study the taxonomic composition of these assemblages, their ecological distributions and adaptations, and evolutionary histories in detail. However, even after 160 years of study, the current knowledge of southern Germany's Late Jurassic chondrichthyan diversity remains incomplete. Over the last 20 years, the systematic study and bulk sampling of southern Germany's Late Jurassic deposits significantly increased the number of known fossil chondrichthyan genera from the region (32 in the present study). In the present work, the fossil record, and the taxonomic composition of Late Jurassic chondrichthyans from southern Germany are reviewed and compared with several contemporaneous assemblages from other sites in Europe. Our results suggest, inter alia, that the Late Jurassic chondrichthyans displayed extended distributions within Europe. However, it nevertheless also is evident that the taxonomy of Late Jurassic chondrichthyans is in urgent need of revision.

Heterodonty and ontogenetic shift dynamics in the dentition of the tiger shark Galeocerdo cuvier (Chondrichthyes, Galeocerdidae).

The lifelong tooth replacement in elasmobranch fishes (sharks, rays and skates) has led to the assemblage of a great number of teeth from fossil and extant species, rendering tooth morphology an important character for taxonomic descriptions, analysing phylogenetic interrelationships and deciphering their evolutionary history (e.g. origination, divergence, extinction). Heterodonty (exhibition of different tooth morphologies) occurs in most elasmobranch species and has proven to be one of the main challenges for these analyses. Although numerous shark species are discovered and described every year, detailed descriptions of tooth morphologies and heterodonty patterns are lacking or are only insufficiently known for most species. Here, we use landmark-based 2D geometric morphometrics on teeth of the tiger shark Galeocerdo cuvier to analyse and describe dental heterodonties among four different ontogenetic stages ranging from embryo to adult. Our results reveal rather gradual and subtle ontogenetic shape changes, mostly characterized by increasing size and complexity of the teeth. We furthermore provide the first comprehensive description of embryonic dental morphologies in tiger sharks. Also, tooth shapes of tiger sharks in different ontogenetic stages are re-assessed and depicted in detail. Finally, multiple cases of tooth file reversal are described. This study, therefore, contributes to our knowledge of dental traits across ontogeny in the extant tiger shark G. cuvier and provides a baseline for further morphological and genetic studies on the dental variation in sharks. Therefore, it has the potential to assist elucidating the underlying developmental and evolutionary processes behind the vast dental diversity observed in elasmobranch fishes today and in deep time.

Early shape divergence of developmental trajectories in the jaw of galeomorph sharks.

BACKGROUND: The onset of morphological differences between related groups can be tracked at early stages during embryological development. This is expressed in functional traits that start with minor variations, but eventually diverge to defined specific morphologies. Several processes during this period, like proliferation, remodelling, and apoptosis for instance, can account for the variability observed between related groups. Morphological divergence through development is often associated with the hourglass model, in which early stages display higher variability and reach a conserved point with reduced variability from which divergence occurs again to the final phenotype. RESULTS: Here we explored the patterns of developmental shape changes in the lower jaw of two shark species, the bamboo shark (Chiloscyllium punctatum) and the catshark (Scyliorhinus canicula). These two species present marked differences in their foraging behaviour, which is reflected in their adult jaw morphology. By tracing the developmental sequence of the cartilage condensation, we identified the onset of cartilage for both species at around stage 31. Other structures that developed later without a noticeable anlage were the labial cartilages, which appear at around stage 33. We observed that the lower jaw displays striking differences in shape from the earliest moments, without any overlap in shape through the compared stages. CONCLUSIONS: The differences observed are also reflected in the functional variation in feeding mechanism between both species. Likewise, the trajectory analysis shows that the main differences are in the magnitude of the shape change through time. Both species follow a unique trajectory, which is explained by the timing between stages.

Musculotendinous system of mesopelagic fishes: Stomiiformes (Teleostei).

Every night the greatest migration on Earth starts in the deep pelagic oceans where organisms move up to the meso- and epipelagic to find food and return to the deeper zones during the day. One of the dominant fish taxa undertaking vertical migrations are the dragonfishes (Stomiiformes). However, the functional aspects of locomotion and the architecture of the musculotendinous system (MTS) in these fishes have never been examined. In general, the MTS is organized in segmented blocks of specific three-dimensional 'W-shaped' foldings, the myomeres, separated by thin sheets of connective tissue, the myosepta. Within a myoseptum characteristic intermuscular bones or tendons may be developed. Together with the fins, the MTS forms the functional unit for locomotion in fishes. For this study, microdissections of cleared and double stained specimens of seven stomiiform species (Astronesthes sp., Chauliodus sloani, Malacosteus australis, Eustomias simplex, Polymetme sp., Sigmops elongatus, Argyropelecus affinis) were conducted to investigate their MTS. Soft tissue was investigated non-invasively in E. schmidti using a micro-CT scan of one specimen stained with iodine. Additionally, classical histological serial sections were consulted. The investigated stomiiforms are characterized by the absence of anterior cones in the anteriormost myosepta. These cones are developed in myosepta at the level of the dorsal fin and elongate gradually in more posterior myosepta. In all but one investigated stomiiform taxon the horizontal septum is reduced. The amount of connective tissue in the myosepta is very low anteriorly, but increases gradually with body length. Red musculature overlies laterally the white musculature and exhibits strong tendons in each myomere within the muscle bundles dorsal and ventral to the horizontal midline. The amount of red musculature increases immensely towards the caudal fin. The elongated lateral tendons of the posterior body segments attach in a highly complex pattern on the caudal-fin rays, which indicates that the posterior most myosepta are equipped for a multisegmental force transmission towards the caudal fin. This unique anatomical condition might be essential for steady swimming during diel vertical migrations, when prey is rarely available.

Evolution, diversity, and disparity of the tiger shark lineage Galeocerdo in deep time.

Sharks have a long and rich fossil record that consists predominantly of isolated teeth due to the poorly mineralized cartilaginous skeleton. Tiger sharks (Galeocerdo), which represent apex predators in modern oceans, have a known fossil record extending back into the early Eocene (ca. 56 Ma) and comprise 22 recognized extinct and one extant species to date. However, many of the fossil species remain dubious, resulting in a still unresolved evolutionary history of the tiger shark genus. Here, we present a revision of the fossil record of Galeocerdo by examining the morphological diversity and disparity of teeth in deep time. We use landmark-based geometric morphometrics to quantify tooth shapes and qualitative morphological characters for species discrimination. Employing this combined approach on fossil and extant tiger shark teeth, our results only support six species to represent valid taxa. Furthermore, the disparity analysis revealed that diversity and disparity are not implicitly correlated and that Galeocerdo retained a relatively high dental disparity since the Miocene despite its decrease from four to one species. With this study, we demonstrate that the combined approach of quantitative geometric morphometric techniques and qualitative morphological comparisons on isolated shark teeth provides a useful tool to distinguish between species with highly similar tooth morphologies.

Rise and fall of †Pycnodontiformes: Diversity, competition and extinction of a successful fish clade.

†Pycnodontiformes was a successful lineage of primarily marine fishes that broadly diversified during the Mesozoic. They possessed a wide variety of body shapes and were adapted to a broad range of food sources. Two other neopterygian clades possessing similar ecological adaptations in both body morphology (†Dapediiformes) and dentition (Ginglymodi) also occurred in Mesozoic seas. Although these groups occupied the same marine ecosystems, the role that competitive exclusion and niche partitioning played in their ability to survive alongside each other remains unknown. Using geometric morphometrics on both the lower jaw (as constraint for feeding adaptation) and body shape (as constraint for habitat adaptation), we show that while dapediiforms and ginglymodians occupy similar lower jaw morphospace, pycnodontiforms are completely separate. Separation also occurs between the clades in body shape so that competition reduction between pycnodontiforms and the other two clades would have resulted in niche partitioning. Competition within pycnodontiforms seemingly was reduced further by evolving different feeding strategies as shown by disparate jaw shapes that also indicate high levels of plasticity. Acanthomorpha was a teleostean clade that evolved later in the Mesozoic and which has been regarded as implicated in driving the pycnodontiforms to extinction. Although they share similar body shapes, no coeval acanthomorphs had similar jaw shapes or dentitions for dealing with hard prey like pycnodontiforms do and so their success being a factor in pycnodontiform extinction is unlikely. Sea surface temperature and eustatic variations also had no impact on pycnodontiform diversity patterns according to our results. Conversely, the occurrence and number of available reefs and hardgrounds as habitats through time seems to be the main factor in pycnodontiform success. Decline in such habitats during the Late Cretaceous and Palaeogene might have had deleterious consequences for pycnodontiform diversity. Acanthomorphs occupied the niches of pycnodontiforms during the terminal phase of their existence.

Evolutionary trends of the conserved neurocranium shape in angel sharks (Squatiniformes, Elasmobranchii).

Elasmobranchii (i.e., sharks, skates, and rays) forms one of the most diverse groups of marine predators. With a fossil record extending back into the Devonian, several modifications in their body plan illustrate their body shape diversity through time. The angel sharks, whose fossil record dates back to the Late Jurassic, some 160 Ma, have a dorsoventrally flattened body, similar to skates and rays. Fossil skeletons of this group show that the overall morphology was well established earlier in its history. By examining the skull shape of well-preserved fossil material compared to extant angel sharks using geometric morphometric methods, within a phylogenetic framework, we were able to determine the conservative skull shape among angel sharks with a high degree of integration. The morphospace occupation of extant angel sharks is rather restricted, with extensive overlap. Most of the differences in skull shape are related to their geographic distribution patterns. We found higher levels of disparity in extinct forms, but lower ones in extant species. Since angel sharks display a highly specialized prey capture behaviour, we suggest that the morphological integration and biogeographic processes are the main drivers of their diversity, which might limit their capacity to display higher disparities since their origin.

Growth trajectories of prenatal embryos of the deep-sea shark Chlamydoselachus anguineus (Chondrichthyes).

Chlamydoselachus anguineus, Garman 1884, commonly called the frilled shark, is a deep-sea shark species occurring up to depths of 1300 m. It is assumed to represent an ancient morphotype of sharks (e.g., terminal mouth opening, more than five gill slits) and thus is often considered to represent plesiomorphic traits for sharks. Therefore, its early ontogenetic developmental traits are important for understanding the evolution of its particular phenotype. Here, we established six stages for prenatal embryos and used linear measurements and geometric morphometrics to analyse changes in shape and size as well as their timing during different embryonic stages. Our results show a change in head shape and a relocation of the mouth opening at a late stage of development. We also detected a negative allometric growth of the head and especially the eye compared to the rest of the body and a sexual dimorphism in total body length, which differs from the known data for adults. A multivariate analysis of covariance shows a significant interaction of shape related to the logarithm of centroid size and developmental stage. Geometric morphometrics results indicate that the head shape changes as a covariate of body size while not accounting for differences between sexes. The growth pattern of stages 32 and 33 indicates a shift in head shape, thus highlighting the moment in development when the jaws start to elongate anteriorly to finally achieve the adult condition of terminal mouth opening rather than retaining the early embryonic subterminal position as is typical for sharks. Thus, the antero-terminal mouth opening of the frilled shark has to be considered a derived feature.

Micro-computed tomography imaging reveals the development of a unique tooth mineralization pattern in mackerel sharks (Chondrichthyes; Lamniformes) in deep time.

The cartilaginous fishes (Chondrichthyes) have a rich fossil record which consists mostly of isolated teeth and, therefore, phylogenetic relationships of extinct taxa are mainly resolved based on dental characters. One character, the tooth histology, has been examined since the 19th century, but its implications on the phylogeny of Chondrichthyes is still in debate. We used high resolution micro-CT images and tooth sections of 11 recent and seven extinct lamniform sharks to examine the tooth mineralization processes in this group. Our data showed similarities between lamniform sharks and other taxa (a dentinal core of osteodentine instead of a hollow pulp cavity), but also one feature that has not been known from any other elasmobranch fish: the absence of orthodentine. Our results suggest that this character resembles a synapomorphic condition for lamniform sharks, with the basking shark, Cetorhinus maximus, representing the only exception and reverted to the plesiomorphic tooth histotype. Additionally, †Palaeocarcharias stromeri, whose affiliation still is debated, shares the same tooth histology only known from lamniform sharks. This suggests that †Palaeocarcharias stromeri is member of the order Lamniformes, contradicting recent interpretations and thus, dating the origin of this group back at least into the Middle Jurassic.

Asymmetric patterns in the cranial skeleton of zebrafish (Danio rerio) exposed to sodium pentachlorophenate at different embryonic developmental stages.

Bilaterally symmetric organisms display mirror copies of their structures on both sides of the body, and the development of both sides is regulated by the same set of genes. Environmental variations can directly affect phenotype, and exposure to chemical contaminants at certain stages may modify embryonic development. The pesticide sodium pentachlorophenate (NaPCP) was used at the no-observable-effect concentration (NOEC) to determine the degree of susceptibility of zebrafish (Danio rerio) embryos in different developmentally susceptible windows (zygote, blastula, gastrula, segmentation, pharyngula and larva). Shape variation in the zebrafish viscerocranium and fluctuating asymmetry (FA), which increases in direct proportion to environmental stress, induced by exposure to NaPCP were measured with geometric morphometrics. Procrustes ANOVA was performed to estimate the shape variation around a symmetric consensus that accounted for the following factors: shape variation in individuals (I), variation by sides (S), the Individuals×Sides interaction (I×S), and the stages of exposure to the toxicant (Stages). Factors I, S and IxS accounted for most of the morphological variation (p<0.0001). Extensive deformities throughout the viscerocranium occurred during the window of exposure from gastrula to larva. Embryonic mortality occurred and was dependent on the stage of exposure. The NOEC concentration of NaPCP affected embryonic development in D. rerio and also induced lethal effects in embryos. FA was determined in both unexposed and NaPCP-exposed embryos and was greater in the control than in some exposure windows; besides, no correlation was found between FA and developmental stages, so our results do not support FA as a bioindicator of chemical stress but confirm its value in the study of morphological effects of toxicants.