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Evolutionary History of the Devilrays (Chondrichthyes: Myliobatiformes) from Fossil and Morphological Inference

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Evolutionary History of the Devilrays (Chondrichthyes: Myliobatiformes) from Fossil and Morphological Inference See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/257756584 Evolutionary history of the devilrays (Chondrichthyes: Myliobatiformes) from fossil and morphological inference Article in Zoological Journal of the Linnean Society · September 2012 DOI: 10.1111/j.1096-3642.2012.00844.x CITATIONS READS 17 631 4 authors: Sylvain Adnet Cappetta Henri Université de Montpellier Université de Montpellier 76 PUBLICATIONS 353 CITATIONS 218 PUBLICATIONS 4,073 CITATIONS SEE PROFILE SEE PROFILE Guillaume Guinot Giuseppe Notarbartolo di Sciara Université de Montpellier Tethys Research Institute 25 PUBLICATIONS 105 CITATIONS 131 PUBLICATIONS 3,350 CITATIONS SEE PROFILE SEE PROFILE All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Sylvain Adnet letting you access and read them immediately. Retrieved on: 14 September 2016 bs_bs_banner Zoological Journal of the Linnean Society, 2012, 166, 132–159. With 9 figures Evolutionary history of the devilrays (Chondrichthyes: Myliobatiformes) from fossil and morphological inference SYLVAIN ADNET1*, HENRI CAPPETTA1, GUILLAUME GUINOT1 and GIUSEPPE NOTARBARTOLO DI SCIARA2 1ISEM, UMR CNRS 5554, Université Montpellier 2, CC064, Place Eugène Bataillon, 34095 Montpellier Cedex 5, France 2Tethys Research Institute, Viale G.B. Gadio 2, 20124 Milano, Italy Received 5 October 2011; revised 4 May 2012; accepted for publication 10 May 2012 The exact affinities of the fossil teeth attributed to the devilrays (mobulids) are critical for resolving the debated origin of these giant pelagic rays amongst Myliobatiformes and the timing of their evolution toward planktivory. We performed the first detailed comparative description of teeth belonging to most of the living and fossil mobulids. Based on a survey of living devilrays, three dental morphologies are newly identified as cobblestone tooth plates, comb-like teeth, and peg-like teeth. In addition, all extinct mobulid species are reviewed with comments on their dentition, fossil record, and geographical distribution. As a result, three fossil mobulid taxa are newly described from the Late Eocene of south-west Morocco (Argoubia barbei gen. et sp. nov., Oromobula dakhlaensis gen. et sp. nov., and Eoplinthicus underwoodi sp. nov.). This has permitted the first assessment of the phylogenetic positions of extinct and extant species of mobulids, using cladistic analyses and a combined data set of nondental anatomical characters from the literature and the dental characters defined here. Our new results support the monophyly of mobulids including all living and most extinct species and indicate that mobulids are closely related to rhinopterids. They also indicate that there was a recent split within Mobulidae into the three tooth morphology groups that we describe in this paper. This work provides clues to the evolutionary history of this clade since the Early Eocene, including the gradual lack in tooth interlocking toward the filter-feeding strategy, whereas the preservation of cusped teeth without feeding function in modern filter-feeder mobulids is interpreted as a tool for precopulatory purposes. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166, 132–159. doi: 10.1111/j.1096-3642.2012.00844.x ADDITIONIAL KEYWORDS: fossil record – mobulids – phylogeny – tooth morphology. INTRODUCTION Unlike other Myliobatiformes, mobulids are filter feeders (preying on schooling fishes and planktonic Mobulids represent the largest extant rays inhabit- crustaceans); these rays direct small food into the ing subtropical and tropical waters worldwide. Like mouth through two large cephalic lobes, resembling other members of the Myliobatiformes, the 11 living horns (the origin of the name ‘devilrays’) that, when mobulid species (belonging to the genera Mobula and unfolded, create mobile peribuccal fins. The relatively Manta) have broad, well-developed pectoral fins and weak jaws and small teeth are not used for processing in certain species, a caudal spine and a whip-like tail. prey. Instead, these rays feed by filtering out small- sized prey from the water column that pass through *Corresponding author. E-mail: their large mouth and are caught on the branchial [email protected] filter plates, consisting of soft tissues and located 132 © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166, 132–159 EVOLUTIONARY HISTORY OF THE DEVILRAYS 133 within their internal gill openings (see Notarbartolo valho, Maisey & Grande, 2004; McEachran & Aschli- di Sciara, 1987 for details). Owing to their atypical man, 2004; Claeson et al., 2010). The second feeding behaviour, devilrays do not need the crushing hypothesis is less familiar and is supported by mor- or grinding dentition of the other representatives phology only (Gonzalez-Isais & Montes Dominguez, of the Myliobatiformes (i.e. dasyatids, myliobatids, 2004). The latter authors, using the first comprehen- rhinopterids). This is reflected by the numerous sive sampling of mobulids, considered the mobulids as small and often very poorly developed teeth of Recent the sister clade of a myliobatid–rhinopterid clade species. In Manta and some species of Mobula, loss (Fig. 1B; see Gonzalez-Isais & Montes Dominguez, of mastication is extreme and teeth are peg-like 2004:11 for details on synapomorphies). and/or only present in the lower jaw (as in Manta). This inconsistency in phylogenetic assumptions It remains difficult to understand the evolutionary is notable and leads us to consider the two alterna- pathway that produced planktophagous rays from tive scenarios for the evolution of cephalic lobes supposedly malacophagous ancestors, because the in myliobatids, rhinopterids, and mobulids (Fig. 1). phylogenetic relationships of the living genera These alternatives also concern the dental types (Mobula and Manta) amongst the Myliobatiformes (grinding-type in myliobatids/rhinopterids and are not fully resolved. Mobulids are sometimes con- reduced clutching-type in mobulids) corresponding to sidered a subfamily (Mobulinae) of Myliobatidae two extreme trophic adaptations. Consequently, it Bonaparte, 1838, or as a singular family (Mobulidae) remains uncertain whether the grinding tooth plate of Myliobatiformes (the taxonomic implication is of shell-predators (with cephalic lobes distally fused beyond the scope of this work and the general term together) pre-dated a reversal to the smaller teeth mobulid is preferred here rather than Mobulidae or that are typical of filter-feeders (with enlarged cepha- Mobulinae). Two alternative hypotheses are currently lic lobes) or not. presented in several phylogenetic works (Fig. 1). The Unlike the undefined taxonomic positions of taxa first hypothesis, most commonly adopted by ichthy- amongst the myliobatid–mobulid clade (corresponding ologists, considers close relationships between mobu- to the Myliobatoidea of Nishida, 1990, or aquilopelagic lids and rhinopterids (genus Rhinoptera) inside rays of Compagno, 1990), the monophyly of living a polyphyletic clade of Myliobatidae (see Fig. 1A). mobulids (species belonging to Mobula and Manta) These phylogenetic relationships are supported by is strongly supported by morphology (Gonzalez-Isais DNA sequences (Dunn, McEachran & Honeycutt, & Montes Dominguez, 2004), suggested by DNA 2003, Aschliman et al., 2012) and numerous morpho- sequences (Dunn, McEachran & Honeycutt, 2003), logical analyses (Nishida, 1990; Lovejoy, 1996; and also attested to by parasitism evolution (Benz & McEachran, Dunn & Miyake, 1996; Shirai, 1996; Car- Deets, 1988; Olson et al., 2010). The peculiar feeding Figure 1. Body shapes of pelagic Myliobatiformes are expanded to show familial differences in head shape. The two main phylogenetic hypotheses (see text for references) concerning the myliobatoids are reported on both sides: according the first one (A), more derived myliobatoids possess more enlarged cephalic lobes (shaded grey), according the second one (B), more derived myliobatoids possess a complete fusion of cephalic lobes. Line drawing inspired by Sasko et al. (2006). © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166, 132–159 134 S. ADNET ET AL. behaviour and associated morphological features (e.g. (G. Notarbartolo di Sciara and H. Cappetta). We filter plates, cephalic lobes, dysfunctional spiracle) followed the taxonomic framework proposed in Notar- of all living mobulids strongly support monophyly. bartolo di Sciara (1987), who synonymized numerous Conversely, the precise relationships amongst living invalid species. Eight out of the 11 valid species are mobulid species are still subject to debate. Some illustrated here: Mobula mobular, Mobula japanica, authors consider that the genus Mobula could be in Mobula munkiana, Mobula rochebrunei, Mobula fact paraphyletic (Herman et al., 2000) on the basis of hypostoma, Mobula thurstoni, Mobula tarapacana, closer dental morphologies between Mobula japanica/ and Manta birostris. Two additional species, Mobula Mobula mobular and Manta birostris (Herman eregoodootenke and Mobula kuhlii, were summarily et al., 2000: Group 3) than with other Mobula species illustrated by Notarbartolo di Sciara (1987: figs 12, (Herman et al., 2000: Group 4). 16C) and are not reported here in the absence of To test both interspecific and intraspecific relation- sufficient material, currently limited to juvenile speci- ships of mobulids compared to the myliobatids and mens
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