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A Microanatomical and Histological Study of the Postcranial Dermal Skeleton of the Devonian Actinopterygian Cheirolepis Canadensis

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A Microanatomical and Histological Study of the Postcranial Dermal Skeleton of the Devonian Actinopterygian Cheirolepis Canadensis A microanatomical and histological study of the postcranial dermal skeleton of the Devonian actinopterygian Cheirolepis canadensis LOUISE ZYLBERBERG, FRANÇOIS J. MEUNIER, and MICHEL LAURIN Zylberberg, L., Meunier, F.J., and Laurin, M. 2016. A microanatomical and histological study of the postcranial dermal skeleton of the Devonian actinopterygian Cheirolepis canadensis. Acta Palaeontologica Polonica 61 (2): 363–376. The Devonian stem-actinoterygian Cheirolepis canadensis is potentially important to understand the evolution of the dermal skeleton of osteichthyans, but the last detailed histological study on this taxon was published more than forty years ago. Here, we present new data about the morphology and the histological structure of scales, fulcra, and fin-rays in the Devonian actinopterygian Cheirolepis canadensis through SEM and photomicroscopy. The scales have a typical palaeoniscoid organisation, with ganoine layers overlaying dentine and a bony basal plate, but the ganoine surface lacks the characteristic microtubercles that have been described on the ganoine surface of the scales of polypterids and many other actinopterygians. Fin-rays are composed of segmented and ramified lepidotrichia that show a structure reminiscent of scales, with ganoine and dentine components lying on a thick bony base. We describe articular processes between lepidotrichia that are reminiscent of, and plausibly homologous with, the peg-and-socket articulations between the scales. The analysis of the postcranial dermal skeleton of Cheirolepis canadensis shows that structural similarities between scales and lepidotrichia of this basal actinopterygian are greater than in more recent actinopterygians. The new data on histological and microanatomical structure of the dermal skeleton lend additional support to the hypothesis that lepidoti- chia are derivatives of scales, though they are also compatible with the more general hypothesis that scales, lepidotrichia and fulcra belong to the same morphogenetic system. Key words: Actinoterygia, Cheirolepis, scales, ganoine, dentine, paleohistology, Devonian, Canada. Louise Zylberberg [[email protected]], Sorbonne Universités, ISTEP, UMR 7193 (CNRS/UPMC), Université Paris VI, 4 place Jussieu, B.C.19, F-75252 Paris cedex 05, France. François J. Meunier [[email protected]], BOREA, UMR 7208 (CNRS/IRD/MNHN/UPMC), Département des Milieux et Peuplements Aquatiques, Muséum national d’Histoire naturelle, C.P. 26, 43 rue Cuvier, F-75231 Paris cedex 05, France. Michel Laurin [[email protected]] (corresponding author), CR2P, UMR 7207 (CNRS/MNHN/UPMC/Sorbonne Univer- sités), Centre de Recherches sur la Paléobiodiversité et les Paléoenvironnements, Muséum National d’Histoire Na- turelle, Bâtiment de Géologie, C.P. 48, 43 rue Buffon, F-75231, Paris cedex 05, France. Received 16 March 2015, accepted 7 August 2015, available online 7 September 2015. Copyright © 2016 L. Zylberberg et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (for details please see http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. body, and on the other hand, the lepidotrichia, segmented Introduction bony rays that sustain paired and median fins. Lepidotrichia The post-cranial dermal skeleton of actinopterygians is have been considered as transformed scales by Goodrich composed of mineralised elements including scales, fin (1904) and by Jarvik (1959) because of the morphological rays, scutes, fulcra and spines (Schultze and Arratia 1989; continuity and because of histological similarities between Arratia 2008, 2009) that are frequently interpreted as ho- the scales and the lepidotrichia. Goodrich (1904) and Jarvik mologous structures despite their differences in morphol- (1959) supported their hypothesis for the relationships be- ogy, histological structure, and functions (e.g., Arratia tween scales and lepidotrichia by observations of these two 2008). Based on morphological observations, evolutionary dermal components in extinct Actinopterygii and in basal relationships have been established between the two main extant ones, especially the Polypteridae. However, other pa- components of the dermal skeleton in Actinopterygii: on pers have endorsed only more general suggestions about the the one hand, the scales, mineralised plates covering the link between scales and lepidotrichia (Géraudie and Landis Acta Palaeontol. Pol. 61 (2): 363–376, 2016 http://dx.doi.org/10.4202/app.00161.2015 364 ACTA PALAEONTOLOGICA POLONICA 61 (2), 2016 1982; Géraudie 1988; Johanson et al. 2005; Arratia 2008) Gross 1973; Arratia and Cloutier 2004). The anatomy of and agree with the suggestion by Schaeffer (1977) that: the former is relatively well known owing to an abundant “scales and lepidotrichia composed of enameloid, dentine material (Lehman 1947; Reed 1992; Arratia and Cloutier and bone are somewhat differently shaped manifestations of 1996). In addition to its systematic position and geological the same morphogenetic system”. Thus, Schaeffer’s (1977) age, a criterion for the choice of Cheirolepis canadensis for hypothesis is compatible with, but does not necessarily im- this study is the quality of fossil material from Miguasha, ply, the hypotheses of Goodrich (1904) and Jarvik (1959) which was recently illustrated by studies on Eusthenopteron that can be considered to be nested within Schaeffer’s (1977) foordi (Zylberberg et al. 2010; Meunier and Laurin 2012 hypothesis. Schaeffer’s (1977) hypothesis explains the pres- Sanchez et al. 2012). Even though Cheirolepis canadensis ence of the same tissues and of odontodes both on scales is represented by well-preserved material, the last detailed and on lepidotrichia (as well as in oral teeth, which are also histological descriptions of its scales were published by formed by the same morphogenetic system), but it does not Aldinger (1937) and later by Gross (1973), which followed necessarily predict that as we go back in time, scales and those of Traquair (1875) and Goodrich (1907). Then, in a lepidotrichia (or teeth, for that matter) will resemble each comparative study of fossil vertebrate scale morphology and other more closely, at the histological or anatomical levels, microanatomy, Gross (1953, 1966) reported some data on because this morphogenetic system also produces oral teeth Cheirolepis canadensis and Cheirolepis trailli. More re- that comprise the same tissues, but their anatomical orga- cently, in a comparative microscopical study of the ganoine nization differs rather drastically. Indeed, Schaeffer (1977: tissue, Richter and Smith (1995) gave more detailed data on 44) implicitly acknowledged that his hypothesis did not re- ganoine organisation in Cheirolepis’ scales and they pointed quire greater similarities in early osteichthyans than in ex- out that the term ganoine was used to describe well-miner- tant ones between scales and lepidotrichia in the following alised tissues but that the phylogenetic significance of the quote: “lepidotrichia and scales in early actinoptergians and pattern of ganoine variation remained to be resolved. The sarcoptergians frequently look alike and they may be cov- histology of fulcra and lepidotrichia was studied even less; ered with enameloid (enamel) and dentine. But this does not the most recent report (Goodrich 1904) harks back to the necessarily indicate that lepidotrichia literally evolved from early 20th century and followed those of Agassiz (1843−44) scales—there is little evidence for that. It is perhaps more and Traquair (1875). meaningful to propose that scales and lepidotrichia com- Below, we compare the cheirolepid dermal skeleton with posed of enameloid, dentine and bone are somewhat dif- that of Recent polypterids (Sewertzoff 1924, 1932; Meunier ferently shaped manifestations of the same morphogenetic 1980; Zylberberg and Meunier 2013), since the extant system”. The “But” and “necessarily” in this quote imply Cladistia are considered to occupy a basal position in the phy- partial opposition between similarity (between scales and logeny of Actinopterygii (Ørvig 1957, 1968; Patterson 1982; lepidotrichia of early osteichthyans) and Schaeffer’s hypoth- Lauder and Liem 1983; Gardiner and Schaeffer 1989; Min esis, or at least, this suggests that Schaeffer was aware that and Schultze 2001; Betancur-R. et al. 2015). Lepisosteidae, his hypothesis was not the best explanation for this fact. On which are slightly less basal than polypterids, also consti- the contrary, the hypothesis supported by Goodrich (1904) tute a good basis for comparison, given that their dermal and Jarvik (1959) does make the prediction that this simi- skeleton displays some intermediate features between that larity should decrease over time (that it should be greatest of polypterids and teleosts. in the oldest taxa); observation of a contrary pattern would falsify it, whereas it would not falsify Schaeffer’s (1977) hy- Institutional abbreviations.—MHNM, Musée d’Histoire pothesis. Note that both (histological and anatomical) levels Naturelle de Miguasha, Québec, Canada. are to some extent independent; thus, the odontodes of teeth, fulcra, scales and lepidotrichia are composed of the same Other abbreviations.—AER, apical ectodermal ridge; ECM, tissues, but their anatomical organization differs, with teeth extracellular matrix; SCPPS, secretory calcium-binding being generally composed of a single odontode, while
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