Guillaume Guinot

An Analytical Approach for Estimating Fossil Record and Diversification Events in Sharks, Skates and Rays

Background Modern selachians and their supposed sister group (hybodont sharks) have a long and successful evolutionary history. Yet, although selachian remains are considered relatively common in the fossil record in comparison with other marine vertebrates, little is known about the quality of their fossil record. Similarly, only a few works based on specific time intervals have attempted to identify major events that marked the evolutionary history of this group. Methodology/Principal Findings Phylogenetic hypotheses concerning modern selachians’ interrelationships are numerous but differ significantly and no consensus has been found. The aim of the present study is to take advantage of the range of recent phylogenetic hypotheses in order to assess the fit of the selachian fossil record to phylogenies, according to two different branching methods. Compilation of these data allowed the inference of an estimated range of diversity through time and evolutionary events that marked this group over the past 300 Ma are identified. Results indicate that with the exception of high taxonomic ranks (orders), the selachian fossil record is by far imperfect, particularly for generic and post-Triassic data. Timing and amplitude of the various identified events that marked the selachian evolutionary history are discussed. Conclusion/Significance Some identified diversity events were mentioned in previous works using alternative methods (Early Jurassic, mid-Cretaceous, K/T boundary and late Paleogene diversity drops), thus reinforcing the efficiency of the methodology presented here in inferring evolutionary events. Other events (Permian/Triassic, Early and Late Cretaceous diversifications; Triassic/Jurassic extinction) are newly identified. Relationships between these events and paleoenvironmental characteristics and other groups’ evolutionary history are proposed.

‘Fish’ (Actinopterygii and Elasmobranchii) diversification patterns through deep time

Actinopterygii (ray‐finned fishes) and Elasmobranchii (sharks, skates and rays) represent more than half of todays vertebrate taxic diversity (approximately 33000 species) and form the largest component of vertebrate diversity in extant aquatic ecosystems. Yet, patterns of ‘fish’ evolutionary history remain insufficiently understood and previous studies generally treated each group independently mainly because of their contrasting fossil record composition and corresponding sampling strategies. Because direct reading of palaeodiversity curves is affected by several biases affecting the fossil record, analytical approaches are needed to correct for these biases. In this review, we propose a comprehensive analysis based on comparison of large data sets related to competing phylogenies (including all Recent and fossil taxa) and the fossil record for both groups during the Mesozoic–Cainozoic interval. This approach provides information on the ‘fish’ fossil record quality and on the corrected ‘fish’ deep‐time phylogenetic palaeodiversity signals, with special emphasis on diversification events. Because taxonomic information is preserved after analytical treatment, identified palaeodiversity events are considered both quantitatively and qualitatively and put within corresponding palaeoenvironmental and biological settings. Results indicate a better fossil record quality for elasmobranchs due to their microfossil‐like fossil distribution and their very low diversity in freshwater systems, whereas freshwater actinopterygians are diverse in this realm with lower preservation potential. Several important diversification events are identified at familial and generic levels for elasmobranchs, and marine and freshwater actinopterygians, namely in the Early–Middle Jurassic (elasmobranchs), Late Jurassic (actinopterygians), Early Cretaceous (elasmobranchs, freshwater actinopterygians), Cenomanian (all groups) and the Paleocene–Eocene interval (all groups), the latter two representing the two most exceptional radiations among vertebrates. For each of these events along with the Cretaceous‐Paleogene extinction, we provide an in‐depth review of the taxa involved and factors that may have influenced the diversity patterns observed. Among these, palaeotemperatures, sea‐levels, ocean circulation and productivity as well as continent fragmentation and environment heterogeneity (reef environments) are parameters that largely impacted on ‘fish’ evolutionary history, along with other biotic constraints.

Sharks (Elasmobranchii: Euselachii) from the Late Cretaceous of France and the UK

Bulk-sampling of 22 phosphatic horizons from the Upper Cretaceous of northern France and the UK has yielded very rich selachian faunas dominated by shark taxa. These samples, collected from Cenomanian to Campanian Chalks and one glauconitic sediment, allow the identification of numerous new taxa, and improve our knowledge of northern European Late Cretaceous selachian assemblages, with a special focus on small to minute remains that were previously overlooked. Among the 96 taxa described here, 18 species and four genera are newly described: Protosqualus barringtonensis sp. nov., Heterodontus boussioni sp. nov., Heterodontus laevis sp. nov., Adnetoscyllium angloparisensis gen. et sp. nov., Chiloscyllium frequens sp. nov., Chiloscyllium vulloi sp. nov., Pararhincodon ornatus sp. nov., Cederstroemia siverssoni sp. nov., Pseudocorax duchaussoisi sp. nov., Squalicorax bernardezi sp. nov., Eoptolamna supracretacea sp. nov., Anomotodon genaulti sp. nov., Scyliorhinus monsaugustus sp. nov., Scyliorhinus muelleri sp. nov., Sigmoscyllium acuspidatum gen. et sp. nov., Palaeotriakis gen. nov., Paratriakis robustus sp. nov., Platyrhizodon gracilis gen. et sp. nov. and Platyrhizodon barbei gen. et sp. nov. In addition, numerous potential new taxa are left in open nomenclature pending the discovery of more material. Stratigraphical and geographical ranges of taxa are updated and observations on the dentition of a few species (Anomotodon hermani, Cederstroemia, Carcharias latus, Palaeotriakis, Paratriakis) are made. An updated Late Cretaceous selachian fossil record and global standing diversity are also presented. http://zoobank.org/urn:lsid:zoobank.org:pub:BBDF3FE8-CF78-4601-AA10-74216BE32768

Cretaceous stem chondrichthyans survived the end-Permian mass extinction

Cladodontomorph sharks are Palaeozoic stem chondrichthyans thought to go extinct at the end-Permian mass extinction. This extinction preceded the diversification of euselachians, including modern sharks. Here we describe an outer-platform cladodontomorph shark tooth assemblage from the Early Cretaceous of southern France, increasing the fossil record of this group by circa 120 million years. Identification of this material rests on new histological observations and morphological evidence. Our finding shows that this lineage survived mass extinctions most likely by habitat contraction, using deep-sea refuge environments during catastrophic events. The recorded gap in the cladodontomorph lineage represents the longest gap in the fossil record for an extinct marine vertebrate group. This discovery demonstrates that the deep-sea marine diversity, poorly known during most of the fish evolutionary history, contains essential data for a complete understanding of the long-term evolution of marine fish paleobiodiversity.

Batoids (Elasmobranchii: Batomorphii) from the British and French Late Cretaceous

Bulk sampling of phosphatic horizons from the Late Cretaceous of the Anglo-Paris Basin and Northern Ireland yielded very rich and high diversity selachian faunas. Amongst them, batoid remains (rays and skates) are commonly present and diverse although never a dominant element of these assemblages. The following new taxa are described: Cretaplatyrhinoidis ornatus gen. et sp. nov., Pseudoplatyrhina crispa gen. et sp. nov., ‘Rhinobatos’ seruensis sp. nov., Squatirhina draytoni sp. nov., Agaleorhynchus britannicus gen. et sp. nov. and Ptychotrygonoides sabatieri sp. nov. Batoids are described for the first time from post-Cenomanian Late Cretaceous deposits of England and the dentition of species of the genus Squatirhina is described and discussed. The Platyrhinidae described here represent the oldest known records for the family and the Cenomanian material identified as Dasyatoidea indet. is one of the rare remains of the order Myliobatifomes from pre-Campanian horizons. Evolutionary and palaeoecological observations are also discussed.

Development of understanding of the Mesozoic and Cenozoic chondrichthyan fossil record

Abstract Fossils of post-Palaeozoic sharks and rays are common and well known, and have been extensively studied. Early studies, especially the monographic works of Agassiz and Smith Woodward, described species based on macroscopic remains of isolated teeth, fin spines and rostral ‘teeth’ as well as rare specimens of articulated skeletons and skulls. This material was obtained from a range of sources but especially from commercial collectors in Britain and mainland Europe. Additional research over subsequent decades also concentrated on large specimens, giving a very biased perception of the chondrichthyan record. The use of large-scale bulk sampling in the latter part of the twentieth century revealed a previously unknown wealth of small fossils, especially teeth, and vastly improved knowledge of ancient sharks and rays. Widening use of these techniques to obtain small specimens has led to a dramatic increase in the fossil taxa known. In addition, reassessment of previously known taxa has allowed generic diversity of some clades to be appreciated. Detailed work on skeletal anatomy, in part aided by new non-destructive methods, continues to improve knowledge of shark and ray diversity, phylogeny and radiation.

Regional to Global Patterns in Late Cretaceous Selachian (Chondrichthyes, Euselachii) Diversity

ABSTRACT Although selachian fossil remains have been studied for nearly three centuries, little is known about their evolutionary history. Recent studies have suggested different timings of early diversification events in the Late Triassic, Jurassic, and Early Cretaceous. However, Late Cretaceous selachian diversity has remained little explored despite numerous and diversified selachian assemblages known from this time interval. Sampling standardization, origination/extinction rates, and raw ordinal diversity were examined based on taxonomic occurrences in three data sets representing distinct geographical areas (Anglo-Paris Basin, northwestern Europe, and Western Interior Seaway) spanning the Cenomanian-Campanian interval. This examination allowed the identification of regional diversity events, previously reported for some invertebrate groups, but presented for the first time for a marine vertebrate group. The local mid-Cenomanian diversity drop (Anglo-Paris Basin) is interpreted as a possible consequence of changes in bottom seawater conditions related to the rapid mid-Cenomanian transgression. The Cenomanian/Turonian faunal turnover is likely to be due to various sampling biases (Anglo-Paris Basin and northwestern Europe), but a genuine extinction in the Western Interior Seaway cannot be excluded. The Santonian diversity peak synchronous with a marked global increase in seawater temperatures contrasts with the rapid temperature decrease linked with low diversity in the early Campanian. SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP

The first articulated specimen of the Cretaceous mackerel shark Haimirichia amonensis gen. nov. (Haimirichiidae fam. nov.) reveals a novel ecomorphological adaptation within the Lamniformes (Elasmobranchii)

The first shark from the early Late Cretaceous Konservat Lagerstätte of Agoult (south-eastern Morocco) is described. The specimen consists of the anterior part of an articulated skeleton including the cephalic and branchial regions, anterior vertebrae and one pectoral fin. The well-preserved dentition of this specimen indicates that it corresponds to the fossil lamniform originally described as Odontaspis amonensis Cappetta & Case, 1975, a purported odontaspidid species of unclear affinities. The new material provides crucial anatomical data for this taxon, such as head shape, cranial structure, tooth formula, organization of the ampullary system and type of vertebra. Based on these features, this short-snouted, broad-headed shark is confirmed as a member of Lamniformes but is clearly not assignable to any of the known living and fossil genera, and is thus described as Haimirichia amonensis gen. nov. Moreover, this unique set of features, including several autapomorphies, differs sufficiently from those of odontaspidids and other lamniform families (both living and extinct) that it requires the erection of the family Haimirichiidae fam. nov. The articulated specimen of H. amonensis reveals a novel ecomorphological specialization within the Lamniformes, adding to the high disparity observed within this order. During the Cenomanian, H. amonensis was a common, widely distributed species that likely had a lifestyle similar to that of some living medium-sized coastal pelagic carcharhiniform sharks with a comparable overall morphology, such as the whitetip reef shark Triaenodon obesus. http://zoobank.org/urn:lsid:zoobank.org:pub:6B14A7F7-CBB7-4259-A339-CF2A99721FC8

Coelacanths as “almost living fossils”

Since its usage by Darwin in 1859, the concept of ‘living fossil’ has undergone multiple definitions and has been much discussed and criticized. Soon after its discovery in 1938, the coelacanth Latimeria was regarded as the iconic example of a ‘living fossil’. Several morphological studies have shown that the coelacanth lineage (Actinistia) has not displayed critical morphological transformation during its evolutionary history and molecular studies have revealed a low substitution rate for Latimeria, indicating a slow genetic evolution. This statement, however, has been recently questioned by arguing that the low substitution rate was not real, and that the slow morphological evolution of actinistians was not supported by paleontological evidence. The assessment of morphological transformation among three vertebrate lineages during a time interval of circa 400 million years shows that the morphological disparity of coelacanths is much more reduced than the morphological disparity of Actinopterygii and Tetrapoda. These results support the idea that living coelacanths are singular organisms among the living world.

On the need of providing tooth morphology in descriptions of extant elasmobranch species

Elasmobranchii is a clade of chondrichthyans (cartilaginous fishes) that comprises sharks, skates and rays represented today by approximately 1,200 species. Chondrichthyans have a long evolutionary history dating back to the Late Ordovician (ca. 450 million years ago [Mya]) based on isolated dermal denticles (Janvier 1996). Other remains such as articulated skeletons and teeth are known from the Lower Devonian (ca. 410 Mya: Mader 1986; Miller et al. 2003). The fossil record of modern elasmobranchs (Neoselachii) can be traced back to the Early Permian (ca. 290 Mya) and is represented by isolated teeth (Ivanov 2005), with fossils of crown group sharks and rays appearing in Lower Jurassic (ca. 200 Mya) rocks (e.g., Cappetta 2012). Since their appearance in the geological record, elasmobranchs are mainly represented by isolated teeth, whereas articulated skeletons are very rare and restricted to a small number of fossil localities (e.g., Cappetta 2012). The scarcity of skeletal remains in their fossil record is due to their poorly mineralized cartilaginous skeleton that requires special taphonomical conditions to be preserved. Elasmobranch teeth, in contrast, are composed of highly mineralized tissues (hydroxyapatite) that have a strong preservation potential (Shimada 2006). In addition, elasmobranchs replace their teeth continuously over the course of their life span (polyphyodonty) and therefore shed thousands of teeth in their lifetime (Reif et al. 1978; Schnetz et al. 2016) leading to large numbers of potential fossils. These morphologically highly diverse isolated teeth constitute much of the rich fossil record of elasmobranchs, and largely form the basis of our understanding of elasmobranch diversity and evolution through geological time.