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Vertebral Development in the Devonian Sarcopterygian Fish Eusthenopteron Foordi and the Polarity of Vertebral Evolution in Non-Amniote Tetrapods

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Vertebral Development in the Devonian Sarcopterygian Fish Eusthenopteron Foordi and the Polarity of Vertebral Evolution in Non-Amniote Tetrapods Journal of Vertebrate Paleontology 22(3):487±502, September 2002 q 2002 by the Society of Vertebrate Paleontology VERTEBRAL DEVELOPMENT IN THE DEVONIAN SARCOPTERYGIAN FISH EUSTHENOPTERON FOORDI AND THE POLARITY OF VERTEBRAL EVOLUTION IN NON-AMNIOTE TETRAPODS S. COTE1*, R. CARROLL1, R. CLOUTIER2, and L. BAR-SAGI1² 1Redpath Museum, McGill University, 859 Sherbrooke St. W., Montreal, Quebec, H3A 2K6, Canada; 2DeÂpartement de Biologie, Universite de QueÂbec aÁ Rimouski, 310 alleÂe des Ursulines, Rimouski, Quebec, G5L 3A1, Canada ABSTRACTÐStudy of a growth series of twenty-seven specimens from the Upper Devonian of Escuminac Bay, QueÂbec documents a complex pattern of vertebral development in the osteolepiform ®sh Eusthenopteron foordi. Os- si®cation begins with elements associated with the caudal, anal, and second dorsal ®ns. Development of the haemal arches, caudal radials, and caudal neural arches continues anteriorly and posteriorly from near the level of the anterior margin of the caudal ®n. Trunk neural arches ossify later than the caudal neural arches and as a separate sequence. Trunk intercentra most likely begin ossi®cation posteriorly and continue forward after the ossi®cation of haemal arches is complete. Comparisons of many different patterns of vertebral development within the modern actinopterygians demonstrates that the sequence of development in Eusthenopteron foordi is unique. The diverse patterns of vertebral development observed in fossil and modern ®sh presumably result from an interplay between the inherent anterior to posterior sequence of development controlled by the Hox genes, and varying selective forces imposed by the physical and biological environment in which the ®sh develop. Initiation of vertebral development in the caudal region of Eusthenopteron foordi can be attributed to selection for early function of the tail in propulsion. In contrast, vertebral development in Carboniferous amphibians typically proceeds from anterior to posterior. This may re¯ect development in the still water of ponds and lakes in contrast with the coastal environment inhabited by the hatchlings of Eusthen- opteron foordi. The sequences of vertebral development seen in Carboniferous labyrinthodonts and lepospondyls are divergently derived from that observed in Eusthenopteron foordi. INTRODUCTION tebral development if the sequence of development seen in Car- boniferous labyrinthodonts were primitive for tetrapods. Amphibians are unique among tetrapods in commonly ex- Knowledge of the early history of Chondrichthyes, Ostei- pressing a biphasic life history with fossilizable larval stages chthyes, and Placodermi indicates that neural arches evolved that document early ontogenetic development. The sequence of long before centra (Goodrich, 1930; Remane, 1936; Carroll, development of vertebral elements differs markedly among the 1988). This suggests that the pattern of vertebral development major taxa of both Paleozoic and modern amphibians. Differ- seen in Carboniferous labyrinthodonts, in which the arches os- ences in developmental patterns provide a potential means of sify before the centra, and in an anterior to posterior direction, inferring phylogenetic relationships, but also re¯ect major dif- is probably primitive for tetrapods. However, the sequence and ference in their ways of life that are signi®cant in tracing their direction of vertebral development has never been described in evolutionary history. the closest sister-group of tetrapods, the osteolepiform sarcop- Carroll et al. (1999) attempted to establish relationships be- terygians. Large numbers of immature specimens of the best tween Paleozoic and modern amphibian orders on the basis of known of osteolepiforms, Eusthenopteron foordi Whiteaves, are different patterns of vertebral development. They documented present in numerous collections and have been used for study a consistent pattern in the timing and direction of ossi®cation of the pattern of development of both the body proportions of the arches and centra in anurans and the larvae of labyrin- (Thomson and Hahn, 1968) and the skull (Schultze, 1984). thodonts, speci®cally temnospondyl branchiosaurs, in which the However, vertebral development has been largely ignored. An- arches ossify before the multipartite centra in a clearly anterior drews and Westoll's (1970) description of the skeleton of Eusth- to posterior sequence. They contrasted this pattern with that enopteron foordi remains the most comprehensive and widely seen in lepospondyls (particularly microsaurs) and speci®c sal- accepted (Fig. 2), however it deals only with mature specimens. amanders, in which cylindrical centra ossify at a very early The current study documents the sequence and direction of ver- ontogenetic stage, prior to the neural arches (Fig. 1). tebral ossi®cation in Eusthenopteron foordi and compares this The early formation of cylindrical centra in many salaman- data with the pattern of development seen in modern ®sh, am- ders was used to suggest that they might share a common an- phibians, and Carboniferous labyrinthodonts and lepospondyls. cestry with lepospondyls (Carroll et al., 1999) since this pattern was certainly a derived character relative to the presence of VERTEBRAL DEVELOPMENT IN EUSTHENOPTERON multipartite centra in both labyrinthodonts and their putative sister-taxa, such as the osteolepiform Eusthenopteron foordi. Extensive collections of Eusthenopteron foordi from the Up- However, a sister-group relationship between frogs and labyrin- per Devonian (middle Frasnian) locality of Miguasha in QueÂbec thodonts could not be supported by the common pattern of ver- were examined from the parc de Miguasha, QueÂbec (MHNM) (approximately 800 specimens), the Natural History Museum, *Current address: Harvard University, Department of Anthropology, London (BM(NH)), and the Museum of Comparative Zoology, Peabody Museum, 11 Divinity Avenue, Cambridge, Massachusetts, Harvard (MCZ). Study was concentrated on 27 specimens rang- 02138. ing from less than 3 cm to 29.5 cm in length. The smallest ²Current address: Angell Memorial Animal Hospital, 350 S. showed no trace of ossi®ciation of the internal skeleton, but in Huntington Ave., Boston, Massachusetts, 02130. the largest, all elements of the endochondral skeleton had be- 487 488 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002 FIGURE 1. Vertebral development in Paleozoic and modern amphibians. A, dorsal view of a larva of the temnospondyl labyrinthodont Bran- chiosaurus salamandroides from the Westphalian D of NyÂrÏany, Czech Republic. Neural arches ossify from anterior to posterior; they are just beginning to form at the base of the tail. Centra ossify later, from paired, crescentic intercentra and pleurocentra. B, dorsal view of a late larval stage of the modern anuran Rana pipiens. The neural arches ossify from anterior to posterior in the trunk region, cylindrical centra form only at metamorphosis. Neither centra or arches form in the tail. C, ventral view of a juvenile specimen of the lepospondyl microsaur Hyloplesion longicostatum, from the Westphalian D of NyÂrÏany, Czech Republic. Even the smallest known specimens of this species have cylindrical centra, but loosely attached neural arches. The poor resolution of the last preserved caudal vertebrae indicate that the centra ossify in an anterior to posterior direction. D, the hynobiid salamander Salamandrella keyserlingii. Both arches and centra develop from anterior to posterior, but in contrast with the frog, the centra form ®rst, and extend to the end of the tail. The most posterior centra initially chondrify as small paired elements. Only a few paired arches can be seen just behind the skull. Reproduced from Carroll et al., 1999. Larval temnospondyl labyrinthodonts resemble anurans in that the arches form prior to the centra, and chondri®cation and ossi®cation of both arches and centra proceed from anterior to posterior. Microsaurs resemble some salamanders in having cylindrical centra that form as early or earlier than the arches. Vertebral development in all these groups is derived relative to that of Eusthenopteron foordi. come ossi®ed and resembled the shape of bones in previously an artibrary decision. Study of additional specimens by Schul- described adults (Figs. 3A±H, 4A±E). Isolated bones of Eusth- tze (1984) failed to show statistical support for changes in the enopteron suggest adults reached a size of approximately 1.5 limb positions for which Thomson and Hahn had argued. How- m (Schultze, 1984), although the largest complete specimen, on ever, Schultze did recognize that changes in skull proportions, display at parc de Miguasha, is only 1.06 m long. speci®cally the relative length of the orbit and the postorbital As others have done in the past, it was assumed that a series region of the skull, were characteristic of an early stage in of different sized specimens, belonging to a single species from growth that he also referred to as juvenile, although he did not a single locality, represent differences in age. It has previously indicate a speci®c size range for juvenile individuals. The cur- been shown that the changes accompanying size increase in rent study suggests that the time at which all elements of the Eusthenopteron foordi are similar to those seen in growth and endochondral skeleton have become ossi®ed may be a non- maturation studies in modern ®sh (Schultze, 1984). This series arbitrary means of differentiating between juvenile and adult allows comparison of juvenile to mature specimens
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