The Phylogeny of Rays and Skates (Chondrichthyes: Elasmobranchii) Based on Morphological Characters Revisited

Abstract

Elasmobranchii are relatively well-studied. However, numerous phylogenetic uncertainties about their relationships remain. Here, we revisit the phylogenetic evidence based on a detailed morphological re-evaluation of all the major extant batomorph clades (skates and rays), including several holomorphic fossil taxa from the Palaeozoic, Mesozoic and Cenozoic, and an extensive outgroup sampling, which includes sharks, chimaeras and several other fossil chondrichthyans. The parsimony and maximum-likelihood analyses found more resolved but contrasting topologies, with the Bayesian inference tree neither supporting nor disfavouring any of them. Overall, the analyses result in similar clade compositions and topologies, with the Jurassic batomorphs forming the sister clade to all the other batomorphs, whilst all the Cretaceous batomorphs are nested within the remaining main clades. The disparate arrangements recovered under the different criteria suggest that a detailed study of Jurassic taxa is of utmost importance to present a more consistent topology in the deeper nodes, as issues continue to be present when analysing those clades previously recognized only by molecular analyses (e.g., Rhinopristiformes and Torpediniformes). The consistent placement of fossil taxa within specific groups by the different phylogenetic criteria is promising and indicates that the inclusion of more fossil taxa in the present matrix will likely not cause loss of resolution, therefore suggesting that a strong phylogenetic signal can be recovered from fossil taxa.

Systematics and Phylogenetic Interrelationships of the Enigmatic Late Jurassic Shark Protospinax annectans Woodward, 1918 with Comments on the Shark–Ray Sister Group Relationship

“…However, alternative hypotheses also were retrieved by molecular studies (depending on the used genes and applied evolutionary models), for example with Galeomorphii being more closely related to Batomorphii, a shark paraphyly was also retrieved by molecular data (see Li et al [ 204 ]). Although a sister-group relationship between modern sharks and rays was implied in the past [ 205 – 209 ], such a relationship only was retrieved once in phylogenies based on morphological data [ 59 ]. In the study of Villalobos-Segura et al [ 59 ], monophyly of sharks was supported by two additional characters, the presence of labial cartilages (char.…”

“…Although a sister-group relationship between modern sharks and rays was implied in the past [ 205 – 209 ], such a relationship only was retrieved once in phylogenies based on morphological data [ 59 ]. In the study of Villalobos-Segura et al [ 59 ], monophyly of sharks was supported by two additional characters, the presence of labial cartilages (char. 72) and a short clasper length (char.…”

“…Characters were mainly based on Landemaine et al [ 77 ] and Villalobos-Segura et al [ 59 ], whose matrices were largely assembled from previous phylogenetic studies on sharks [ 46 – 48 , 78 ] and rays [ 79 – 95 ], most of which were modified versions of previous studies and can be traced back to Shirai [ 45 ] for sharks and McEachran et al [ 96 ] for rays. Additionally, dental characters, which have been used for phylogenetic analyses in squalomorph sharks [ 60 , 61 , 97 ] and skeletal characters defining galeomorph sharks [ 98 – 100 ] and outgroup taxa [ 101 , 102 ] were included.…”

“…Woodward [ 53 ] suggested a close affiliation with squaliform and echinorhiniform sharks (i.e., “Spinacidae”) within a clade that also included batomorphs (“Tectospondyli”). Since that time, Protospinax has been hypothesized to represent either the ancestor of a clade comprising batomorphs, several squalomorph and galeomorph sharks [ 55 ], the base of Squalomorphii and Batomorphii [ 20 ], an intermediate group between Pristiophoriformes and batomorphs [ 56 ], a stem squalomorph [ 57 ], a sister group to squaliform sharks [ 46 ], or a squaliform shark [ 58 , 59 ]. All these hypotheses were based on the type of material (holo- and paratype).…”

“…Support for this hypothesis came from subsequent phylogenetic studies based on dental characters, which also proposed a close relationship between Protospinax , Squatiniformes, and Pristiophoriformes [ 60 , 61 ], although a closer relationship between Protospinax and Pristiophoriformes was suggested by Adnet and Cappetta [ 60 ]. Conversely, a recent morphological study based on new data proposed a closer relationship between Protospinax and Squaliformes [ 59 ]. Despite the questionable phylogenetic position of Protospinax , it has nevertheless been attributed an important place in the evolutionary history of elasmobranchs [ 54 ] and despite the uncertainty surrounding its phylogenetic relationships, it is used as an important fossil for calibrating molecular phylogenies [ 13 , 61 , 62 ].…”