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The Origin of Orbitotemporal Diversity in Lepidosaurs: Insights from Tuatara Chondrocranial Anatomy

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The Origin of Orbitotemporal Diversity in Lepidosaurs: Insights from Tuatara Chondrocranial Anatomy 69 (2): 169 –181 © Senckenberg Gesellschaft für Naturforschung, 2019. 2019 SPECIAL ISSUE on Recent Advances in Chondrocranium Research | Guest Editor: Ingmar Werneburg The origin of orbitotemporal diversity in lepidosaurs: insights from tuatara chondrocranial anatomy Oleksandr Yaryhin 1, 3,* & Ingmar Werneburg 1, 2, * 1 Fachbereich Geowissenschaften der Eberhard-Karls-Universität Tübingen, Hölderlinstraße 12, 72074 Tübingen, Germany — 2 Senckenberg Center for Human Evolution and Palaeoenvironment (HEP) at Eberhard-Karls-Universität, Sigwartstraße 10, 72076 Tübingen, Germany — 3 Schmalhausen Institute of Zoology of NAS of Ukraine, vul. B. Khmelnytskogo, 15, Kyiv, 01030 Ukraine — * Corresponding authors — E-mails: [email protected]; [email protected] Submitted February 22, 2019. Accepted May 15, 2019. Published online at www.senckenberg.de/vertebrate-zoology on May 28, 2019. Published in print on Q2/2019. Editor in charge: Uwe Fritz Abstract Sphenodon punctatus, the tuatara, is the last survivor of the formerly widely distributed group of Rhynchocephalia, which is the sister group of Squamata. The skull anatomy of S. punctatus and its fossil relatives is comparably well known; however, embryological data of skull development are rare, incomplete, and mostly represented by dated works. Knowing the anatomy of the chondrocranium of S. punc­ tatus is crucial to an understanding of chondrocranial evolution in reptiles and particularly in lepidosaurs. Here, based on the historical histological collection of Hugo Schauinsland, we reexamined the anatomy of the fully formed chondrocranium in S. punctatus and describe a very early stage of its chondrocranium formation, which was not considered in any previous study. The architecture of the fully formed chondrocranium of S. punctatus represents one of the most complex ones among sauropsids. We observed a number of characters, that are absent in other reptiles and were never previously described in S. punctatus. We consider the robust lateral braincase wall in S. punctatus to represent an ancestral condition. In the lepidosaurian ancestor it likely had the potential for further diversifcation of the orbitotemporal region in squamates. Certainly, it provided extra mechanical strength to the chondrocranium as a whole. At the same time, the strong car- tilaginous lateral wall of the chondrocranium in S. punctatus could also be a rudimentary form of the more distant ancestor of lepidosaurs, in which the chondrocranium played a more functional role. Key words Chondrocranium; development; evolution; Lepidosauria; primary braincase, Rhynchocephalia; Sphenodon punctatus. Introduction The lizard-like reptiles of the group Rhynchocephal- 1990). However, subsequent nDNA analysis indicates ia were successful and widely distributed during the that all populations are best regarded as one species: Mesozoic, inhabited territories of Europe, Africa, and S. punctatus (HAY et al., 2010). North America and included terrestrial and marine ani- Squamata and Rhynchocephalia are sister taxa and mals (CREE, 2014, FRASER, 1988, GILMORE, 1909, JONES diverged about 250 million years ago (EVANS & JONES, & CREE, 2012, RASMUSSEN, 1981). Now, however, they 2010, JONES et al., 2013, REST et al., 2003). Therefore, are represented only by one species, Sphenodon punc­ as the only living representative of Rhynchocephalia, tatus (GRAY, 1842) (syn. “Hatteria punctata”), which is S. punctatus has been extensively studied to examine endemic to New Zealand (HAY et al., 2010). Previously, what it can tell about reptile evolution (BRENNAN, 2016, based on allozyme variation, it has been divided into two BROOM, 1906, CREE, 2014, EVANS, 2008, GISI, 1907, GOR- species, S. punctatus and S. guntheri (DAUGHERTY et al., NIAK et al., 1982, GÜNTHER, 1867, HOPPE, 1934, JONES et al., ISSN 1864-5755 | eISSN 2625-8498 | DOI: 10.26049/VZ69-2-2019-04 169 Yaryhin, O. & Werneburg, I.: The origin of orbitotemporal diversity in lepidosaurs: insights from tuatara chondrocranial anatomy 2011, JONES & CREE, 2012, JONES et al., 2012, REGNAULT different embryos sectioned in the sagittal, frontal, and et al., 2017, SANGER et al., 2015, SÄVE-SÖDERBERGH, 1946, transverse planes respectively. The second stage is older, SÄVE-SÖDERBERGH, 1947). has a fully formed chondrocranium, and it consists of 24 The skull anatomy of S. punctatus and its fossil rela- slides labeled as specimen “Hatteria d ” (original labe- tives is relatively well-known (GÜNTHER, 1867, JONES ling of Schauinsland). According to the information on et al., 2011, JONES, 2008, JONES et al., 2009, SIEBENROCK, the slides of “Hatteria d ”, the thickness of sections is 15 1894). However, embryological data of skull develop- μm. The thickness of the other sections is not recorded, ment in S. punctatus are rare and are mostly represent- but based on our own experience, we estimate that it is ed by very old studies (HOWES & SWINNERTON, 1901, not more than 10 μm. On one series of the early embryo SCHAUINSLAND, 1903, WYETH, 1924), and later studies sections, the name “F. Zinsung” is written, possibly in mostly concern dermal ossifcation (RIEPPEL, 1992, WER- reference to a technical assistant of Hugo Schauinsland. NER, 1962). Most data were summarized in the “Biology The other two series of the small embryos are labeled as of Reptilia” book series (BELLAIRS & KAMAL, 1981), in “Hatteria K ”, in which the letter “K” perhaps refers to the which the authors concluded that the fully formed chon- word “klein”, i.e. German for ‘small’. However, based on drocranium requires further, more detailed observations the progress of organ development, we conclude that the particularly in the nasal region. letters do not correspond to the letter-labeled stages of Previous descriptions of the fully formed chondro- DENDY (1899). cranium of S. punctatus differ from one another. Differ- Based on the developmental conditions, we infer that ences in overall shape are particularly surprising, this the earliest embryos of our study represent a stage that is concerns especially the orbitotemporal region (HOWES & slightly earlier than “stage P” described by Howes and SWINNERTON, 1901, SCHAUINSLAND, 1901, WERNER, 1962). Swinnerton (1901). The earliest developmental stage of Most likely, the illustrated diversity is not the result of the chondrocranium resembles that of other lepidosaurs intraspecifc variability, but an artifact of using different and sauropsids in general (BELLAIRS & KAMAL, 1981, approaches to reconstruct the primordial skull (discussed YARYHIN & WERNEBURG, 2017, YARYHIN & WERNEBURG, by YARYHIN & WERNEBURG (2017)). In general, on a cer- 2018), in which the frst mesenchymal precursors of the tain taxonomic (i.e., “family”) level, the chondrocranium chondrocranium are trabeculae, acrochordal, and para- represents a highly conserved organ (YARYHIN & WERNE- chordals. The specifc shape of the chondrocranium an- BURG, 2018). lagen closely resembles that of the crocodile Mecistops Here, we re-describe the fully formed chondrocra- cataphractus (MÜLLER, 1967). nium of S. punctatus using three dimensional computer The collection of the Übersee-Museum contains sev- imaging. We evaluate how its structure compares to that eral more slides. However, those sections provide no fur- of squamates and what this means for lepidosaurs as a ther information on development of the chondrocranium whole. In particular, we concentrate on the orbitotempo- as they are of almost the same stage as “Hatteria d ”, or ral region, which experienced the greatest diversifcation even more advanced, and/or contain postcranial mate- among lepidosaurs (DAZA & BAUER, 2010, EVANS, 2008). rial. We also describe a very early stage of chondrocranium formation, that was not considered in any study before. Image processing. The sections were photographed with an Olympus BH2 microscope equipped with a Canon EOS 650D digital camera. Where necessary, the images were stitched together using the “Photomerge” option in Materials and methods Adobe PS CC software. Background cleaning and color adjustments were also performed using Adobe PS CC software. Specimens. The original embryonic material used in our study was collected in New Zealand at the end of the 19th 3D modeling. Semiautomatic alignment of the image century by Prof. Dr. Hugo Schauinsland. He collected stack was done using Fiji software (SCHINDELIN et al., this material during his famous New Zealand expedition 2012); the 3D-reconstruction was performed in Amira either on Stephens Island from April 1896 to May 1897 5.0 software (Thermo Fisher Scientifc) using manual (SchAUINSLAND, [1899] 1996) or on the Cook Islands from seg men tation tools. December 1896 to January 1897 (SchAUINSLAND, 1898). The embryonic material was serially sectioned and, based on coloration of the sections, it was probably stained with hematoxylin. After long term storage, the sections be- Results came partially bleached and lost coloration, but they are still informative. The collection is housed at Übersee-Mu- seum (Bremen, Germany), which was founded by Hugo Early stage of chondrocranium differentiation (based Schauinsland in 1896 (SchAUINSLAND, [1899] 1996). on the three small specimens). At this stage, the embryos In the current study, we describe two stages. The frst show a weak differentiation of sensory organs. The ol- is an early stage represented by 13 slides in total of three factory organ is represented by the olfactory pits (with- 170 SPECIAL ISSUE VERTEBRATE ZOOLOGY — 69 (2) 2019 Fig. 1. 3D reconstructions
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