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Microct Survey of Larval Skeletal Mineralization in the Cuban Gar Atractosteus Tristoechus (Actinopterygii; Lepisosteiformes)

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Microct Survey of Larval Skeletal Mineralization in the Cuban Gar Atractosteus Tristoechus (Actinopterygii; Lepisosteiformes) Anatomy atlas MicroCT survey of larval skeletal mineralization in the Cuban gar Atractosteus tristoechus (Actinopterygii; Lepisosteiformes) Scherrer Raphael¨ 1, Hurtado Andres´ 2, Garcia Machado Erik3, Debiais-Thibaud Melanie´ 1* 1Institut des Sciences de l’Evolution de Montpellier, UMR5554, Universite´ Montpellier, CNRS, IRD, EPHE, c.c.064, place Eugene` Bataillon, 34095 Montpellier Cedex 05, France 2Centro Hidrobiologico,´ Parque Nacional Cienaga´ de Zapata, Matanzas, Cuba 3Centro de Investigaciones Marinas, Universidad de La Habana, Calle 16, No. 114 entre la 1ra y 3ra, Miramar, Playa, La Habana 11300, Cuba *Corresponding author: [email protected] Abstract Using X-ray microtomography, we describe the ossification events during the larval development of a non-teleost actinopterygian species: the Cuban gar Atractosteus tristoechus from the order Lepisosteiformes. We provide a detailed developmental series for each anatomical structure, covering a large sequence of mineralization events going from an early stage (13 days post-hatching, 21mm total length) to an almost fully ossified larval stage (118dph or 87mm in standard length). With this work, we expect to bring new developmental data to be used in further comparative studies with other lineages of bony vertebrates. We also hope that the online publication of these twelve successive 3D reconstructions, fully flagged, will be an educational tool for all students in comparative anatomy. Keywords: Actinopterygii, development, Lepisosteiformes, mineralization, skeleton Submitted:2016-04-04, published online:2017-05-17. https://doi.org/10.18563/m3.3.3.e3 INTRODUCTION 2013; Broughton et al., 2013; Friedman, 2015). Near et al. (2012) estimated the separation between gars and teleosts be- Gars are non-teleost ray-finned fishes (Actinopterygii) be- tween 330 and 390 million years ago (Mya), somewhere from longing to the order Lepisosteiformes, whose only extant Late Devonian to Early Carboniferous. According to the same family is Lepisosteidae. The seven extant species of gars studies, Holostei and Teleostei make up the clade Neopterygii, have been categorized in the genera Lepisosteus (4 species) sister group to Acipenseriformes with which they make up and Atractosteus (3 species). They are large (less than 1 me- the clade Actinopteri. Finally, Polypteriformes diverged from ter to more than 2 meters long) ambush predators inhabiting Actinopteri at the crown age of extant Actinopterygii, which freshwaters of North and Central America, up to Cuba (Wiley, was estimated at 380-430 Mya (Near et al., 2012), roughly 1976; Nelson et al., 2016). Lepisosteiformes belong to Ging- between the Late Silurian and the Early Devonian. lymodi, a group of actinopterygians that had its maximum Because of their phylogenetic position, gars have been a key diversity during the Late Cretaceous (Wiley, 1976; Grande, taxon to many morphological studies. Ancient literature is 2010) and included one other extinct order, †Semionotiformes, available on comparative anatomy of actinopterygians includ- according to the most recent evidence by Lopez-Arbarello´ ing gars: Gegenbauer (1887) and Sewertzoff (1895) described (2012) who placed the earliest re-assigned fossil of Lepiso- the occipital region of fishes and its development, Schreiner steiformes during the Early Jurassic (around 190-200 million (1902) compared more specifically Lepisosteiformes and Amia, years ago (Mya)). Luther (1913) described cranial musculature and nerves with Lepisosteiformes make up one of the few lineages of ray- comparison with lungfishes, and Schmalhausen (1913), Kry- finned fishes that are not teleosts, referred to by many as zanovsky (1927) and Jessen (1972) documented fins and their ’basal’, ’lower’ or ’primitive’ actinopterygians (e.g. Lauder, development. Lauder (1980) studied the biomechanics of 1980; Gardiner and Schaeffer, 1989; Gardiner et al., 1996, feeding in Polypterus, Lepisosteus oculatus and Amia. Ar- 2005). The other extant lineages of non-teleost actinoptery- ratia and Schultze (1991) published an extensive study of gians are Amiiformes (or Halecomorphi; one species, Amia the morphology and development of the palatoquadrate (the calva), Acipenseriformes (or Chondrostei; sturgeons and pad- structure in the skull responsible for articulating the lower dlefishes) and Polypteriformes (or Cladistia; bichirs). The jaw to the cranium, and that can be a significant component monophyly of Holostei (sistergroup to Teleostei) made up by of the upper jaw in non-teleost lineages) in actinopterygians Lepisosteiformes and Amiiformes, is supported by most of and some sarcopterygians. More recently, Britz and Johnson the recent molecular and anatomical/paleontological datasets (2010) documented the patterns of fusion of vertebrae to the (Normark et al., 1991; Lecointre et al., 1994; Hurley et al., occiput in actinopterygians, showing that gars have a specific 2007; Grande, 2010; Near et al., 2012; Betancur-R et al., pattern, where the two first vertebrae are fused to the occiput. Skeletal ossification during the Cuban gar larval development — 2/15 Comparative studies involving gars have also helped to doc- Inventory number Characteristics ument evolutionary convergences, such as the independent At1 13 dph larva, 21 mm TL acquisition of an elongated body shape in distantly related At2 16 dph larva, 26mm SL ambush predators such as pikes (Esox), needlefishes (Belone) At3 19 dph larva, 27mm SL and gars (Maxwell and Wilson, 2013). Another example is the At4 22 dph larva, 30mm SL ability to breathe atmospheric oxygen with their swimblad- At5 26 dph larva, 32mm SL der, analogous to the air-breathing swimbladder of Amia and At6 31 dph larva, 39mm SL some basal Teleostei as well as the lungs of Polypteriformes, At7 37 dph larva, 43mm SL lungfishes and tetrapods (Perry et al., 2001). Gars are also a At8 52 dph larva, 46mm SL key taxon to understand the evolution of scales in vertebrates. At9 74 dph larva, 61mm SL They have a peculiar type of scales, the ganoid scales, that At10 89 dph larva, 63mm SL are a synapomorphy of actinopterygians but remain only in At11 104 dph larva, 70mm SL Polypteriformes and gars (Helfman et al., 2009). Comparative At12 118 dph larva, 87mm SL studies aimed at uncovering homology relationships between Table 1. Inventory number, age and length characteristics for each ganoid scales, placoid scales of sharks, elasmoid scales of specimen. TL: total length. SL: Serial length teleosts and tooth-like structures in general (Sire et al., 1987, 2009, Sire, 1989, 1990; Huysseune and Sire, 1998; Vickary- (Slater et al., 2009), mice (Shen et al., 2013; Ho et al., 2015), ous and Sire, 2009). crocodilians (Dufeau and Witmer, 2015), turtles (Rice et al., Skeletal anatomy and development of gars have been doc- 2016) and catsharks (Enault et al., 2016). To the best of our umented by a great number of previous studies. Veit (1907) knowledge, however, a description of the development of the described the development of the skull in L. osseus. Mayhew whole skeleton in gars with precise timings of ossification is (1924) and Hammarberg (1937) described in details the skull still lacking, and 3D surfaces of the whole ossified skeleton at of L. platostomus and its development. Jollie (1984) described different stages are not available although it would be a valu- the development of the skull and the pectoral fins in L. osseus, able source of additional characters in comparative studies but L. platostomus and A. spatula, and also the patterning of the also in educational contexts. lateral line sensory system in the head of L. osseus. Long and With this aim in mind, we hereby provide a µCT develop- Ballard (2001) described the early external development of L. mental series of the mineralized skeleton in the Cuban gar, osseus from the zygote until the yolk disappearance. In 2006, Atractosteus tristoechus, a species for which development has Kammerer et al. studied the development and kinetics of the never been investigated (see Table1). Our high resolution jaws related to feeding behavior in L. osseus and A. spatula, of larval stages allows us to give details on the ossification also looking at adults of other extant and extinct species of times of most of the structures present in an adult skeleton. gars. In a recent work, Hilton et al. (2014) described the devel- Also, our hope is that our data will serve as a good support for opment of the lower jaw in L. osseus. The main reference further work focusing on more detailed aspects of gar anatomy work on the skeleton of gars and its development is, however, and development, will motivate similar exploratory studies in the published book by Grande (2010) who described fossil other species, and that the published 3D reconstructions will and extant species and reviewed former descriptions. With be used in comparative anatomy classes. similar exhaustive studies on Amia (Grande and Bemis, 1998) and Chondrostei (Grande and Bemis, 1991), this survey pro- METHODS vides a synthetic framework on the morphology of non-teleost actinopterygians. Individuals of Atractosteus tristoechus used for this study A new concern has arisen on the utility of including more were raised in the Centre for reproduction of the indigenous developmental data in comparative studies, because they add ichthyofauna, National Park Zapata swamp, Cuba. Two fe- new characters and yield deeper analyses when combined with males and four males were used for reproduction. The fer- traditional morphological data (Rucklin¨ et al.,
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