Journal of Vertebrate Paleontology 22(3):487±502, September 2002 ᭧ 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 and indi- individuals. This occurs at a total body length between 27.4 and cates the order in which different areas and elements of the 29.5 cm. vertebral column ossify. The specimens vary greatly in degree Not even the smallest specimens of Eusthenopteron, less than of completeness and quality of preservation. 3 cm in length, show any features typically associated with Thirty cm was the size limit of those specimens of this genus larvae, nor can any changes seen within the series be associated designated as ``juvenile'' by Thomson and Hahn (1968). They with a de®nable metamorphosis (Moser, 1984). On the basis of based their recognization of a juvenile stage on observations current evidence, development can be considered direct. suggesting that most pronounced modi®cations of body shape The size series (Table 1) shows a fairly even distribution had occurred before the 30 cm stage, but admitted that this was from 3 cm to 29.5 cm, with some clustering of specimens at COTE ET AL.ÐEUSTHENOPTERON VERTEBRAL DEVELOPMENT 489

FIGURE 2. Eusthenopteron foordi Whiteaves. Reconstruction of the skeleton. Reproduced from Andrews and Westoll (1970). In the specimens used for our study the intercentra appeared to be closer together than is indicated in this reconstruction. Abbreviations (used in this and all following ®gures): af, anal ®n; cf, caudal ®n.; cl, cleithrum; cna, caudal neural arch and associated spine; dd1, distal support (radial) of ®rst dorsal ®n; df1, ®rst (anterior) dorsal ®n; df2 second (posterior) dorsal ®n; f, femur; ha, haemal arch and associated spine; hu, humerus; ic, intercentrum; na, neural arch and associated spine; pc, pleurocentrum; pcf, pectoral ®n; pd1, proximal support (basal plate) of ®rst dorsal ®n; pd2, proximal support (basal plate) of second dorsal ®n; pra, proximal support (basal plate) of anal ®n; pvf, pelvic ®n; pvg, pelvic girdle; ran, radials (3) of anal ®n; rd2, radials (3) of second dorsal ®n; sa, sacral vertebra; vcr, ventral caudal radial; v1,1st vertebra (trunk vertebrae are numbered from 1 to 31 from anterior to posterior).

approximately 15 cm and 24 cm (see also Parent and Cloutier, mal arches have been added anteriorly. The large proximal sup- 1996:®g. 11). This may indicate that overall body growth is port (basal plate) for the anal ®n has begun to ossify, but that slowed at these time, or more likely, it could be an artifact of for the second dorsal ®n has not. In MHNM 06-36 (Fig. 7; 16.8 sampling. cm), almost the entire body is well preserved, but endochondral ossi®cation is limited to the posterior end of the animal. Neither Description of Specimens pectoral nor pelvic ®ns show endochondral bones. Supports for the ®rst dorsal are well formed, although the elements have The four smallest specimens (e.g., Figs. 3A, 5A), ranging been displaced and appear side by side. Anterior haemal arches from 2.9 to 4.2 cm in total length, show body scales, clearly are evident only to the level of the distal end of the proximal de®ned ®n structure, generally unjointed lepidotrichia, and the support (basal plate) for the anal ®n. The proximal support for dermal bones of the skull, but no trace of vertebral elements or the second dorsal ®n is not ossi®ed. BM(NH) P 15961 (not endochondral ®n supports. These specimens are all preserved illustrated) is only 15.5 cm in length, but has an ossi®ed prox- in dorsal or ventral view, with a broadly ¯attened head and a imal support for the second dorsal. narrow body. The beginning of internal ossi®cation can ®rst be In MHNM 06-299 (Fig. 8; estimated total length 18.2 cm), noted in the 5.0 cm specimen MHNM 06-535 (Figs. 3B, 5B), in which the endochondral skeleton is very well exposed, all which shows the entire body exposed in lateral view, with well de®ned dermal ®n elements and the initiation of ossi®cation of but the most posterior caudal neural arches and ventral radials the posterior endochondral ®n supports. These include three are ossi®ed. However, the last several posterior haemal arches neural arches with spines, extending posteriorly from the an- remain unossi®ed, showing that all of these elements ossi®ed terior margin of the epichordal lobe of the caudal ®n and four initially in association with support for the anterior margin of radials extending posteriorly from the anterior margin of the the caudal ®n, with subsequent ossi®cation extending from the hypochordal lobe, but no haemal arches. It cannot be deter- front to the back within the caudal skeleton, and slightly later mined whether or not the radials of the anal ®n were ossi®ed, from the anterior margin of the caudal ®n forward toward the but two radials were present in the second dorsal ®n. No en- trunk. In this specimen, 11 neural arches are ossi®ed, but they dochondral supports were evident in the more anterior dorsal do not extend forward of the base of the second dorsal ®n. In ®n or the paired ®ns. contrast, the haemal arches extend to a level just behind the Specimen MHNM 06-238 (Figs. 3C, 5C; 6.4 cm in length) pelvis where they continue as intercentra, the main central el- had ossi®ed all three radials of the second dorsal, as well as ements in Eusthenopteron. Eleven trunk intercentra, including two of the radials of the anal ®n. The outline of caudal neural the sacral vertebra (as identi®ed by Andrews and Westoll arches and ventral radials can be recognized through the over- (1970)), are present anterior to the pelvis, at which point the lying scales, but their speci®c number is dif®cult to establish. block ends. These would be vertebrae 22 through 32 in a fully The haemal arches were apparently not yet ossi®ed. An increas- developed adult. Traces of ribs, the bases of the trunk neural ing number of elements can be seen in the caudal region of the arches, and possibly also pleurocentra are ossi®ed in the pos- poorly preserved MHNM 06-30 (Fig. 6A), estimated to be 9.0 terior trunk. By this stage, the supports for the dorsal and anal cm in length. These include the ®rst appearance of haemal arch- ®ns have reached almost the adult form. In a marked advanced es, in addition to the neural arches and radials of the caudal ®n. over the next smaller specimens, the paired elements of the Approximately six neural arches with spines and four caudal pelvic girdle are fully formed, together with the proximal ele- radials are ossi®ed, spanning the anterior portion of the caudal ments of the pelvic ®ns. Both the proximal and distal endo- ®n, in addition to three caudal haemal arches. All three radials chondral supports for the ®rst dorsal ®n are clearly de®ned. of the anal ®n are ossi®ed. Two of the three radials in the MCZ 5810 (Fig. 9; 19.3 cm) is a critical specimen, possess- second dorsal and both bones (one radial and the basal plate) ing most of the vertebral column, although in some places the supporting the ®rst dorsal are ossi®ed, but no bones are visible vertebrae are covered by scales that could not be removed with- in the pelvic ®n. out damaging the underlying bone. The dermal bones of the In MHNM 06-59 (Fig. 6B; 12.0 cm), the caudal neural arches head are crushed and a break runs vertically through the skull and radials have ossi®ed further posteriorly and additional hae- between the parietals and postparietals. However, no bones are 490 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002

FIGURE 3. Reconstructions of a series of specimens of Eusthenopteron foordi showing changes in degree of ossi®cation of the endochondral skeleton in relation to increasing size. These changes are assumed to represent modi®cations during ontogeny. Body outline indicated in solid lines based on the fossil as preserved, with some amount of reconstruction. Dotted lines indicate missing portions of the fossil. Endochondral elements are identi®ed in subsequent illustrations. A, MHNM 06-235 A/B; B, MHNM 06-535; C, MHNM 06-238 A/B; D, MHNM 06-30 A/B; E, MHNM 06-59 A/B; F, MHNM 06-36 A/B; G, MHNM 06-299 A/B; H, MCZ 5810.

entirely missing and it is clear that the full set of dermal ele- between the most posterior intercentra and the haemal arches. ments was ossi®ed. On the other hand, it is evident that the No centra or arches are present anterior to the back of the oper- braincase and palatoquadrate were unossi®ed between the well- culum, although approximately six would be present in this area de®ned bones of both sides of the dermal skull. of an adult (Andrews and Westoll, 1970; Hitchcock, 1995). The supports for the anal and second dorsal ®n are complete Neural arches are visible above what would be the seventh, and the humerus and two other elements of the pectoral ®n are eleventh, and fourteenth intercentra in an adult. In the caudal ossi®ed. The pelvic girdle is missing, as is the distal element region, nine neural arches with spines and twelve haemal arches of the ®rst dorsal ®n support, most likely the result of local are present, as well as eight ventral radials. breakage of the specimen. Sixteen intercentra, which begin be- Although generally poorly preserved, with areas at the base hind the opercular series and proceed posteriorly along the body of the tail and in the region of the operculum obliterated by the are visible through the scales. This spans the positions of ver- formation of pyrite, MHNM 06-209 (Fig. 10; 21.0 cm) includes tebrae 7 through 22 or 23 in an adult. There is a large gap most of the skeleton. Impressions of intercentra and neural COTE ET AL.ÐEUSTHENOPTERON VERTEBRAL DEVELOPMENT 491

FIGURE 4. Continuation of Figure 3. A, MHNM 06-209; B, MHNM 06-121 A/B; C, MHNM 06-382 A; D, BM(NH) P. 6803; E, MHNM 06- 636.

arches extend anteriorly to at least the front of the shoulder As in MCZ 5810, no endochondral bone of the skull is pre- girdle, and may pass beneath the operculum. Unfortunately, the served. impressions of the vertebrae are not preserved in the matrix, Ossi®cation in the caudal region can next be seen in MHNM but against the medial surface of the dermal scales, and so show 06-121 (Fig. 11; estimated total length 24 cm), an especially almost no surface detail. Therefore, it is not possible to deter- well-preserved specimen. The caudal ®n is supported by seven mine whether or not pleurocentra were present. Endochondral to eight neural arches with spines, four to ®ve haemal arches, supports for both the pectoral and the pelvic ®ns are visible. and 11 to 12 radials. This compares, respectively, with 12, 10, 492 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002

TABLE 1. Reconstructed length of Eusthenopteron foordi specimens. In specimens BM(NH) P. 6803 (Fig. 13; 26.4 cm) and Abbreviations: MHNM, specimens from the collection of the Parc de BM(NH) P. 60341 (not illustrated; 26.7 cm), the vertebral col- Miguasha; BM(NM) P, specimens from the collection of the British Museum of Natural History; MCZ, specimens from the Museum of umn is represented primarily by impressions showing the ex- Comparative Zoology at Harvard. Total length is measured from the tip ternal surface of the scales closely overlying the arches and of the snout to the end of the medial portion of the caudal ®n in small centra. This mode of preservation shows that they were rela- specimens in which it extends beyond the dorsal and ventral lobes, and tively large and well ossi®ed, but reveals no surface detail. by the ends of the dorsal and ventral lobes of the caudal ®ns in large BM(NH) P. 6803 shows a number of clearly de®ned distal ra- specimens, where they exceed the length of the medial portion. For dials of the pectoral ®n. More proximal elements are present, incomplete specimens, total length was estimated on the basis of the proportions of the body that was preserved, accepting Schultze's (1984) but reveal little detail. Neural arches are associated with many ®nding that the position of the ®ns did not change signi®cantly during of the the intercentra. growth. In the largest specimen studied, MHNM 06-636 (Fig. 14), estimated at 29.5 cm in total length, the entire column had Specimen Approximate achieved an essentially adult condition, with probable ossi®- Rank number length (cm) cation of all elements from the skull to the end of the tail, 1 MHNM 06-234 2.9 including the ribs. Unfortunately, due to the manner of initial 2 MHNM 06-235 A/B 3.3 preparation, little surface detail remains. The elements of the 3 MHNM 06-13 3.6 pelvic ®n distal to the femur are well exposed and fully ossi®ed. 4 MHNM 06-90 4.1 5 MHNM 06-535 5.0 6 MHNM 06-238 A/B 6.4 Summary of Ossi®cation Sequences 7 MHNM 06-30 A/B 9.0 8 MHNM 06-59 A/B 12.0 Numerous, well-preserved specimens document the devel- 9 BM(NH) P. 15961 15.5 opmental sequence of endochondral bones in the posterior por- 10 BM(NH) P. 15957 16.2 tion of the vertebral column in Eusthenopteron foordi (Table 2; 11 MHNM 06-36 A/B 16.8 Figs. 3, 4, 15A). Ossi®cation of caudal neural arches, haemal 12 MHNM 06-299 A/B 18.2 13 MCZ 6518 A/B 18.9 arches, and ventral radials begins at the anterior margin of the 14 MCZ 5810 19.3 caudal ®n and proceeds both posteriorly and anteriorly. Anterior 15 MCZ 9159 19.5 to the caudal ®n, there is a gap in the ossi®cation of neural 16 BM(NH) P.7074 20.2 arches in MHNM 06-299 until roughly the level of the sacral 17 MHNM 06-209 21.0 vertebra but the haemal arches and intercentra form a contin- 18 MHNM 06-233 B 22.0 uous series, ossifying from posterior to anterior, into the pos- 19 MCZ 9265 23.0 20 BM(NH) P. 60340 23.5 terior trunk. The gap in the sequence of neural arches below 21 MHNM 06-121 A/B 24.0 and just anterior and posterior to the second dorsal ®n may be 22 MHNM 06-382 A 25.0 related to the need for ¯exion in this area for effective swim- 23 BM(NH) P. 15960 26.0 ming. The neural arches in this area are reduced in size relative 24 BM(NH) P. 6803 26.4 to those anterior and posterior to them in the adult stage as well 25 BM(NH) P. 60341 26.7 (Fig. 2). Pleurocentra are only seen with certainty in the pos- 26 BM(NH) P. 6804 27.4 27 MHNM 06-636 29.5 terior trunk region after all the other elements are formed. The distal radials of both the anal and second dorsal ®ns ossify before the large proximal supports; in contrast, the proximal and distal elements of the ®rst dorsal ®n appear to ossify si- and 14 in the restoration of an adult specimen illustrated by multaneously. Andrews and Westoll (1970). Based on the latter specimen, the Few specimens clearly show the pattern of development in longest of each element in MHNM 06-121 is identi®ed as the the anterior portion of the column. Specimens MHNM 06-59 most anterior support for the caudal ®n. The length of the neural and MHNM 06-36 show a complete covering of scales, but the arches and the radials is reduced more anteriorly. Unfortunately, endochondral elements of the caudal, dorsal, and haemal ®ns this specimen does not extend anterior to the ®n supports for protrude through them. No such protrusions are evident in the the second dorsal and anal ®ns. area of the paired ®ns or the vertebral column anterior to the MHNM 06-382 (Fig. 12; estimated total length 25 cm) is level of the base of the anal ®n. MCZ 5810 (Fig. 9) shows uniquely preserved, showing the entire vertebral column to the intercentra in the area between the pectoral and pelvic ®ns, base of the tail as well as the palatoquadrate and the braincase, corresponding with vertebrae 7 through 22 or 23. This specimen but without any dermal bones or any trace of ®ns. The cranial is most simply interpreted as indicating that ossi®ciation of the elements are preserved in dorsal view, to judge by the smooth, anterior intercentra begins just behind the operculum and pro- rather then tooth covered surface of the palatoquadrate. This is ceeds both anteriorly and posteriorly. This appears to occur as the smallest specimen in which there is de®nite evidence that a separate event from the ossi®cation of the haemal arches. the braincase and palatoquadrate are ossi®ed. The ®rst four ver- However, MHNM 06-299 (Fig. 8), which is one centimeter tebrae are disarticulated, but all 31 trunk intercentra, and a pu- shorter than MCZ 5810, shows fully developed intercentra be- tative sacral vertebra, can be accounted for. The intercentra at ginning with the sacral vertebra and extending anteriorly to the the anterior end of the column are visible in ventral view (in 22nd intercentrum, where the block ends. This specimen may be contrast with the skull). The ®rst 16 are extensive crescents, interpreted as demonstrating that the intercentra develop as a continuous at the ventral midline. The next few are either bro- continuation of the series of haemal arches, beginning at the ken ventrally or were originally paired, while those more pos- end of the trunk and proceeding anteriorly. However, we cannot terior (exposed in lateral view) were certainly paired. The last exclude the possibility that intercentra in this specimen began three elements presumably represent the most proximal portion ossi®cation near the anterior end of the trunk and continued in of the tail, but the area of the haemal arch is not preserved. a posterior direction. Small, paired, circular pleurocentra are visible in association These two specimens seem to provide contradictory infor- with intercentra 23 to 33. Pleurocentra may have been present mation regarding the sequence of development of the intercen- more anteriorly, but would not be exposed since only the ven- tra. However, further study of MCZ 5810 reveals that the gap tral surface of the intercentra can be seen. seen between the haemal arches and the last preserved inter- COTE ET AL.ÐEUSTHENOPTERON VERTEBRAL DEVELOPMENT 493

FIGURE 5. Three of the smallest, but fairly well preserved specimens of Eusthenopteron foordi. A, MHNM 06-235 A, preserved in ventral view, showing the impression of the dorsal surface of the skull. Long, essentially unjointed lepidotrichia of the pectoral and caudal ®ns are visible. No endochondral ®n supports or vertebral elements are ossi®ed at this stage; B, MHNM 06-535, complete skeleton in lateral view. Endochondral supports for the caudal, anal, and second dorsal ®n are visible through the scales. All ®ns are supported by unjointed lepidotrichia; C, MHNM 06-238 B. Ventral view of head region, showing the underside of the skull roof and cheeks. The body is twisted so that the lateral surface of the caudal region is exposed. Endochondral supports for the caudal, anal, and both dorsal ®ns can be seen through or between the scales. No endochondral elements can be seen more anteriorly. Image reversed left to right for comparison with the other two specimens. 494 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002

ance of trunk neural arches is in MHNM 06-299 (Fig. 8), how- ever they appear irregularly over a few intercentra and no pat- tern can be established. This is also the case in MCZ 5810. Therefore, ossi®cation of trunk neural arches could have oc- curred either from front to back or from back to front. Pleu- rocentra are ®rst clearly seen at the posterior end of the trunk and anterior caudal region in MHNM 06-382, but they may have been present more anteriorly in this specimen and yet not be visible. They too might have begun ossi®cation from either the anterior or posteriorly end of the body. Based on the nearly universal anterior to posterior direction of expression of the Hox genes (which control major aspects of development of the body axis; Shubin et al., 1997; Coates and Cohn, 1999), and the geologically earlier appearance of chon- dri®cation and/or ossi®cation of the neural and haemal arches relative to the centra in both Chondrichthyes and Osteichthyes, the pattern of development in Eusthenopteron foordi appears highly derived relative to more primitive aquatic vertebrates. The sequence also appears very different from that seen in both Carboniferous and modern amphibians, which is commonly an- terior to posterior. One immediate question is whether the pat- tern seen in Eusthenopteron foordi is common among modern bony ®sh or is a specialization of sarcopterygians or of the lineage leading to tetrapods. FIGURE 6. Eusthenopteron foordi. A, MHNM 06-30 A/B, showing Among sarcopterygians, neither fossil nor living coelacanths the support for the ®rst dorsal ®n and the ®rst haemal arches in addition have ossi®ed centra, and so provide only a limited basis for to the elements seen in smaller specimens; B, MHNM 06-59 A/B, also comparison (Andrews, 1977). Centra as well as neural and hae- shows the proximal ®n support for the anal ®n. mal arches are ossi®ed in Devonian lung®sh (Denison, 1968), but the relative sequence of their ossi®cation has not been es- tablished. Recent work by Arratia (2001) will provide a basis for establishing the pattern of vertebral development in the centra may be an artifact of preservation, since there is damage modern species. The primary basis for comparison thus lies to the specimen in that area. It is therefore possible that inter- with the phylogenetically divergent living actinopterygian ®sh. centra may have extended back to the haemal arches. If this were the case, it would suggest that intercentra begin ossi®ca- tion posteriorly as part of the sequence of haemal arches and ACTINOPTERYGIAN FISH proceed anteriorly. This may have occurred quite rapidly, since MHNM 06-36 (Fig. 7), which shows no intercentra and an in- Surprisingly, there is relatively little published information complete set of haemal arches, is less than two centimeters regarding vertebral development in modern actinopterygian shorter than MHNM 06-299 which possessed all the haemal ®sh, and there has been no recent synthesis of the available arches and at least the last 11 intercentra. data. Dunn (1984) listed work that had been published up to Trunk neural arches are one of the last elements to begin that date and states that the pattern of ossi®cation varies con- ossi®cation. This certainly occurred as a separate event from siderably among taxa. More recent studies further document the ossi®cation of the caudal neural arches. However, the di- this variability. In the following section, observations on ver- rection in which they ossi®ed is uncertain. The earliest appear- tebral development taken from the available literature are re-

FIGURE 7. Eusthenopteron foordi. MHNM 06-36 A. Nearly complete skeleton with continuous scale cover. Endochondral supports are clearly evident posteriorly (darkened for emphasis), and can not be seen in association with the pelvic or pectoral ®ns. COTE ET AL.ÐEUSTHENOPTERON VERTEBRAL DEVELOPMENT 495

FIGURE 8. Eusthenopteron foordi. MHNM 06-299 A/B. Caudal region and posterior trunk showing a gap in the neural arches between the caudal ®n and the area of the sacral vertebra and the ®rst evidence of the pectoral girdle and proximal support for the second dorsal ®n. Neural arches begin to appear over some intercentra.

viewed in a phylogenetic sequence beginning with the most cation begins when the ®sh is 11.0 mm long with the occipital primitive living actinopterygians. arches and the bases of the next three neural arches. By 14.5 Speci®c comparison of vertebral elements between sarcop- mm, the ®rst and second pair of neural arches and the posterior terygians and actinopterygians is complicated by the fact that ®n rays of the dorsal ®n are ossi®ed. Body scales begin to form the central elements are not homologous, and different patterns in specimens approximately 30 mm in length, in marked con- of development of both the arches and centra are indicated by trast to their much earlier appearance relative to the centra and a distinct terminology. Patterns of development among actin- ®n supports in Eusthenopteron foordi. Bartsch and Gemballa opterygians, emphasising the caudal region, are documented in (1992:519) state that the development of the vertebral column detail by Arratia and Schultze (1992) and by Schultze and Ar- in Polypterus ``is ruled by strict functional demand rather than ratia (1986). Where the terminology differs, the sarcopterygian by the `ballast' of evolutionary history.'' They interpret the ear- term is used, followed by the designation for the actinoptery- ly completion of the caudal and posterior dorsal ®n skeleton as gian analogue in parentheses. being necessary adaptations for locomotion. Polypterus (Polypteridae), considered the primitive sister-tax- Development of the primitive chondrostean Polyodon spa- on of all other living actinopterygians, provides an informative thula (Acipenseriformes: Polyodontidae), was recently de- contrast with Eusthenopteron foordi. Overall, the neural arches, scribed by Bemis and Grande (1999). The medial ®ns become vertebral centra, and ribs differentiate from anterior to posterior, distinguished from one another in an anterior to posterior se- while the lepidotrichia and endoskeletal supports of the dorsal quence- dorsal, anal, then caudal. However, as in Eusthenop- ®n form from posterior to anterior. Chondri®cation and ossi®- teron foordi, ®n supports are initially elaborated in the caudal cation of the hypaxial caudal skeleton also occur in a posterior region. The ®rst visible skeletal elements are the hypurals and to anterior direction (Bartsch and Gemballa, 1992). Chondri®- middle radials of the dorsal and anal ®n, which are initially all

FIGURE 9. Eusthenopteron foordi. MCZ 5810. Complete skeleton covered with scales. Shows the humerus and several small bones of the pectoral support. Pelvic girdle is absent, most likely due to breakage of the specimen in this area. Intercentra can be seen from the area of the pectoral girdle back to the mid-trunk region. There are no intercentra in the opercular region, or in the area of the pelvic ®n. The dermal skull is fully ossi®ed, however there is no evidence of an ossi®ed braincase or palatoquadrate. 496 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002

FIGURE 10. Eusthenopteron foordi. MHNM 06-209. Smallest specimen in which the vertebral column extends to the back of the skull, and the proximal elements of the pectoral ®n are well ossi®ed. Most of the endochondral bone is preserved as an impression on the inside surface of the scales, which shows little structural detail. Dashed outline indicates pyrite. Head omitted.

FIGURE 11. Eusthenopteron foordi. MHNM 06-121 A/B. Posterior portion of the skeleton showing the endochondral supports for the caudal, anal, and second dorsal ®n in nearly their adult con®guration. Lepidotrichia conspicuously jointed in contrast with smaller specimens. COTE ET AL.ÐEUSTHENOPTERON VERTEBRAL DEVELOPMENT 497

FIGURE 12. Eusthenopteron foordi. MHNM 06-382 A. Endochondral bones of axial skeleton, stripped of all elements of the dermal skeleton. Palatoquadrate seems to be preserved in dorsal view, anterior portion of column in ventral view, and posterior portion of column in lateral view. This is the smallest specimen to show pleurocentra unequivocally. Braincase is extensively ossi®ed.

cartilaginous. Hypurals, radials, and dermal ®n rays all begin Development of Amia calva has recently been described by development in the middle portion of the ®n and spread both Grande and Bemis (1998). As shown in their illustrations (one posteriorly and anteriorly. Polyodon does not form vertebral of which is redrawn as Figure 15B), the abdominal centra (those centra. The full adult complement of all caudal, anal, and dorsal running from the occiput to the ®rst centrum bearing a haemal ®n structures are present by the time the ®sh is 47 mm. How- canal) mineralize in an anterior to posterior sequence. Ossi®- ever, only the dermal ®n rays are ossi®ed. Bemis and Grande cation of the ural centra occurs separately and begins before believe that ®sh at this stage have completed metamorphosis, the ossi®cation of even the most anterior of the diplospondylous which indicates that ossi®cation of endochondral structures centra (part of the preural caudal region). Chondri®cation and must occur sometime in the juvenile stage. ossi®cation of the neural arches extends into the caudal region

FIGURE 13. Eusthenopteron foordi. BM(NH) P. 6803, with full pectoral ®n support and more visible neural arches over the intercentra. 498 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002

FIGURE 14. Eusthenopteron foordi. MHNM 06-636. 29.5 cm in length. Skeleton is fully ossi®ed.

prior to the centra. The supports for the caudal ®n ossify before direction of vertebral ossi®cation has been reported show an those of the paired or dorsal ®ns. More details of vertebral anterior to posterior direction of differentiation in both the arch- development are provided in Schultze and Arratia (1986). es and centra. For example, the sword®sh, Xiphidae (Potthoff Among teleost ®sh, the Catostomidae have been reported to and Kelley, 1982), the closely related Scombridae (Wollom, ossify their vertebral centra in an anterior to posterior direction, 1970), and the Anarhichadidae (Pavlov and Moksness, 1997). but in the guppy (Poeciliidae), ossi®cation begins in the middle Anisotremus virginicus (Haemulidae), known as the pork®sh, of the vertebral column and proceeds both anteriorly and pos- shows a slightly different pattern (Potthoff et al., 1984). Carti- teriorly (Weisel, 1967). Crane (1966) describes yet another pat- laginous neural arches (basidorsals) appear ®rst both just behind tern in the viper®shes (Chauliodontidae). Ossi®cation of the the skull and separately in the mid-trunk region, while cartilag- vertebrae occurs ®rst in the caudal region and proceeds ante- inous haemal arches (basiventrals) appear at the center and pos- riorly. In some specimens, the most anterior vertebrae remain terior end of the vertebral column. However, ossi®cation of both unossi®ed throughout life, which Crane suggests could be an neural and haemal arches occurs after the ossi®cation of all adaptation for increased ¯exion required for ef®cient feeding. vertebral centra in an anterior to posterior direction. The pos- Therefore, in a phylogenetically and functionally diverse group terior portion of the dorsal ®n, as well as the anal and caudal of teleost ®shes, a variety of very different patterns of vertebral ®ns are the ®rst to develop rays, while the pelvic and pectoral ossi®cation can be found. ®ns are the last to do so. The elements of the caudal ®n support, Within the order Perciformes, we see a more consistent pat- including the hypurals, normally ossify after the centra of the tern of vertebral ossi®cation. Most perciforms for which the trunk. Potthoff et al. (1984) cited several additional studies of various perciforms in which vertebral elements ossify from an- terior to posterior. TABLE 2. Sequence of ®rst appearance of endochondral bones of the The perciform Archosargus probatocephalus or sheepshead skeleton of Eusthenopteron foordi. (Sparidae), also ossi®es all its vertebral elements in an anterior to posterior direction (Mook, 1977). Here, neural and haemal Length (in cm) arches begin ossi®cation soon after the centra, so that the an- of smallest terior neural and haemal arches are ossi®ed before the posterior specimen expressing this centra. Ossi®cation of the caudal skeleton begins with the lep- Skeletal element element idotrichia in 3.5 mm larvae, followed by the urostyle, hypurals, and ®nally the epurals- all in an anterior to posterior sequence. Caudal neural arches 5.0 Ventral caudal radials 5.0 The hypurals are the last elements to complete ossi®cation, First two radials of second dorsal ®n 5.0 when the ®sh is 25 mm in length. Third radial of second dorsal ®n 6.4 In her comprehensive study of centrarchid ®shes (Centrar- First two radials of anal ®n 6.4 chidae), Mabee (1993) reported that all 30 species ossify their Third radial of anal ®n 9.0 vertebrae following the same pattern, although the number of Haemal arches of caudal ®n 9.0 Supports of ®rst dorsal ®n 9.0 elements can vary among species. Vertebral centra ossify from Proximal support for anal ®n 12.0 anterior to posterior in a continuous sequence, like other per- Proximal support of second dorsal ®n 15.5 ciforms (Fig. 15C). However, the two urostylar centra ossify Pelvic girdle and femur 18.2 earlier than the centra anterior to them, although the anterior Posterior intercentra 18.2 urostylar centrum does ossify ®rst. Another important differ- Anterior intercentra 19.3 ence from other perciforms is that ossi®cation of the haemal Pectoral support (humerus) 19.3 Endochondral skull (braincase and palatoquadrate) 25.0 arches begins in the middle of the series and then proceeds simultaneously in both anterior and posterior directions. This COTE ET AL.ÐEUSTHENOPTERON VERTEBRAL DEVELOPMENT 499

FIGURE 15. Comparison of the sequence of vertebral development in Eusthenopteron foordi with two modern ®sh. A, vertebral development in Eusthenopteron foordi with arrows indicating the direction in which elements ossify; B, larval specimen of Amia calva, which illustrates vertebral centra and neural arches ossifying in an anterior to posterior direction. Bone is shown in solid black and thick lines, thin lines and white indicate cartilage. Dermal ®n rays ossify ®rst in the caudal region; (modi®ed from Grande and Bemis, 1998:129); C, direction of ossi®cation of vertebral and ®n elements in the Centrarchidae; (reproduced from Mabee, 1993).

pattern is also shared by the ®n rays of the dorsal, anal, and tern®sh (Myctophidae) showed that there can be variability in caudal ®ns, as well as the hypurals. The ®n rays of the pectoral the sequence of ossi®cation within groups as well. Dermal ®n ®n ossify in a dorsal to ventral direction. The earliest neural rays are always the ®rst postcranial structures to ossify, but the arches to ossify are those at the very anterior part of the ver- order in which the ®ns ossify is variable. The endochondral tebral column, with ossi®cation continuing in a posterior direc- supports of the caudal ®n ossify before those of the other ®ns, tion. However, a second set of neural arches ossify in the mid- but this occurs after the complete set of caudal dermal ®n rays trunk region, from which ossi®cation proceeds in both anterior has formed. Vertebral centra, neural arches, and haemal arches and posterior directions. The sequence of development begins all ossify in an anterior to posterior direction. The timing of with the anterior neural arches and hypurals, followed by the ossi®cation can vary between species; however, in most the haemal arches and mid-trunk neural arches. Although centra are centra, neural arches, and haemal arches ossify simultaneously. the last elements to appear, they form initially as ossi®ed struc- Generally, the ossi®cation of the vertebral column occurs late tures (autocentra) and so would be visible in fossilized speci- in development relative to the ossi®cation of other structures, mens before the arches. Mabee states that this pattern of ossi- however it is usually completed before the time of metamor- ®cation has also been reported in Trachurus symmetricus (Car- phosis, which varies with species. angidae) (Ahlstrom and Ball, 1954). Although this general pattern of anterior to posterior verte- In contrast with the uniform axial development seen in all bral column development is common to most lantern®shes, two centrarchids, Moser and Ahlstrom's (1970) study of the lan- species follow the opposite sequence. The vertebral centra of 500 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002

early ossi®cation of the caudal region in Eusthenopteron foordi may be an adaptation necessary for early swimming in a fast- current marine environment.

VERTEBRAL DEVELOPMENT IN DEVONIAN AND CARBONIFEROUS TETRAPODS

No fossils are yet known of larval or juvenile individuals of either Panderichthys, which is thought to be the closest known sister-taxon to tetrapods, or of any of the Upper Devonian am- phibians. However, the high degree of development of the cau- dal ®n in these genera strongly supports its importance in swim- ming, which Clack and Coates (1995) and Clack (2000) argue FIGURE 16. Comparison between the body outlines of Eusthenopter- to be the primary, if not sole means of locomotion in Acan- on foordi and Esox lucius showing the similarity in positioning of the thostega and Ichthyostega. This suggests that the pattern of ver- dorsal and anal ®ns and overall appearance, which has been used as tebral development described in Eusthenopteron foordi, with evidence to suggest their similar behavior as adults. Both species reach the early ossi®cation of the tail region, may have been retained similar size as adults. A, Eusthenopteron foordi outline adapted from in Late Devonian amphibians. This is in strong contrast to both Schultze (1984); B, Esox lucius outline adapted from Bry (1996). the adult structure and the patterns of development seen in most members of the major groups of primitive Carboniferous am- phibians, the labyrinthodonts and lepospondyls. With the ex- ception of some embolomeres and the nectrideans, most mem- Hygophum atratum and Hygophum reinhardti ossify from pos- bers of these groups, from the Visean on, had long slender tails terior to anterior, as do their neural arches (Moser and Ahls- with little evidence of adaptation for swimming. trom, 1970). This pattern is unlike that seen in any of the other Some 20 to 30 million years separate Eusthenopteron foordi perciforms. In addition, ossi®cation begins very late in these and the Upper Devonian tetrapods from the earliest adequately two species, normally just before metamorphosis. Therefore, known members of the amphibian lineages that dominated the the lantern®sh show variation both in the sequence of ossi®- mid- to late Carboniferous and include the ancestors of the cation between elements and in the direction of ossi®cation modern orders. During this time, the reproductive environment within speci®c elements. changed from wave and current in¯uenced marginal marine From this scattered sampling of bony ®sh, it is obvious that conditions to quiet inland bodies of fresh water, including coal the sequence and direction of chondri®cation and ossi®cation swamps, oxbow lakes, and larger, semipermanent lakes. The of vertebral elements are extremely variable and are not obvi- different environments in which Eusthenopteron foordi and ously tied to the degree of taxonomic af®nity. The most com- Carboniferous amphibians reproduced may have strongly in¯u- mon pattern is for most elements to ossify in a predominantly enced their patterns of vertebral development. These quiet wa- anterior to posterior direction, but in some ®sh a posterior to ters apparently did not require the early development of the tail anterior sequence is seen. Frequently, some elements of the cau- as a major swimming structure, and their partial isolation may dal region will ossify prior to those in the posterior part of the have limited the access of large aquatic predators. Reduction in trunk. The absence of a phylogenetically consistent pattern of vertebral development among bony ®sh strongly suggests the these selective pressures may have allowed the axial skeleton importance of functional controls, such as the feeding and lo- in Carboniferous amphibians to develop in direct accordance comotive needs of hatchlings and juveniles (Crane, 1966; with the anterior to posterior direction of expression of the Hox Mook, 1977; Bartsch and Gemballa, 1992). Similarity of pat- genes. terns of development must be supplemented by other data to The relatively large adult size of most labyrinthodonts may provide a reliable means of establishing relationships. Ontogeny have required a fairly long period of aquatic development, dur- of the vertebrae does not necessarily re¯ect phylogeny. In fact, ing which ®rst the neural arches and later the multipartite centra very divergent patterns of vertebral development may give rise chondri®ed and then ossi®ed. Lepospondyls had a much differ- to very similar adult forms. ent growth strategy, with precocial ossi®cation greatly limiting The pike and muskellunge, Esox (Esocidae), have long been adult size, and resulting in formation of fully cylindrical centra recognized as similar to Eusthenopteron foordi in body form at a stage when vertebrae in labyrinthodonts had barely begun and probable behavior (Andrews and Westoll, 1970; Arsenault, to ossify (Fig. 1). 1982). This is based on their large size and the far posterior With the description of vertebral development in Eusthen- position of the dorsal and anal ®ns that give a powerful thrust opteron foordi, it is obvious that the patterns of development in lurk and lunge feeding (Fig. 16). One might expect that they in both labyrinthodonts and lepospondyls are derived relative would also share the sequence of development of the vertebrae to more primitive choanates. Hence, the pattern seen consis- and ®n supports seen in Eusthenopteron foordi. In fact, recent tently in larval temnospondyls, in which development of the X-ray studies carried out by Alison Murray show that the ver- arches long precedes that of the centra, is a putative synapo- tebral column in the four North American species of Esox de- morphy linking them with anurans, which follow a comparable velops from anterior to posterior. This marked difference in sequence in all families in which vertebral development has development suggests that factors other than adult feeding hab- been described. its may be important in the selective control of development. Comparison with salamanders is more dif®cult. It has long Reproduction in pike generally occurs in shallow, thickly veg- been assumed that the pattern of vertebral development com- etated habitats on submerged ¯ood plains (Bry, 1996). This monly seen in advanced salamanders, including plethodontids, would indicate that there would be little wave or current activity ambystomatids, and salamandrids, was typical for urodeles. in the environment in which young Esox were undergoing early This seemed to be borne out by the very early formation of development. In contrast, most specimens of Eusthenopteron cylindrical centra, and later appearance of arches in the hyno- foordi are found in tidally in¯uenced estuarine environments biid Salamandrella (Carroll et al., 1999). However, further (Chidiac, 1996; Cloutier et al., 1996). It is probable that the study of a cleared and stained specimen of another hynobiid, COTE ET AL.ÐEUSTHENOPTERON VERTEBRAL DEVELOPMENT 501

Ranodon showed very different patterns, in which the neural all ®sh. Salamanders also show a considerable variety of pat- arches in the anterior trunk form before the centra. terns of development, related to the environment in which they Most striking is the pattern of development seen in Dicamp- develop. Vertebral development in Eusthenopteron foordi is todon, generally considered a much more advanced salamander very different from the patterns seen in Carboniferous amphib- allied with the radiation leading to salamandrids and ambysto- ians. The patterns of development in lepospondyls and labyrin- matids (Milner, 2000). Wake and Shubin (1998) show that early thodonts are thought to have been derived divergently from that stages in its vertebral development closely resemble that of of Eusthenopteron foordi. frogs, with neural arches developing from anterior to posterior, well before the appearance of centra. Like bony ®sh, there is ACKNOWLEDGMENTS clearly a great variety in the patterns of vertebral development The authors wish to thank Johanne Kerr at the Parc de Mig- in salamanders that may be attributed to hatching and devel- uasha, as well as Sandra Chapman at the Natural History Mu- oping in different environments. Accepting this degree of plas- seum, London and Charles Schaff at the Museum of Compar- ticity among salamanders, and the dif®culty of establishing the ative Zoology for loan of specimens. Gloria Arratia, William polarity of character transformation within this order, it is dif- Bemis, Lance Grande, and David Johnson were helpful in sug- ®cult to use any particular mode of vertebral development for gesting references on the development of actinopterygian ®sh. establishing relationships with Paleozoic amphibians. On the Alison Murray provided X-rays and information on pike de- other hand, it opens up the possibility for their being related to velopment and Tamsin Rothery transported specimens from temnospondyls and frogs (as suggested by Trueb and Cloutier, London. This research has been supported by grants from the 1991), which seemed very unlikely if all the primitive sala- Natural Sciences and Engineering Research Council of Canada. manders had a pattern resembling that of lepospondyls, with precocial ossi®cation of cylindrical centra. Work is now under- way to examine vertebral development in a much greater range LITERATURE CITED of modern salamanders to see if a primitive salamander pattern Ahlstrom, E. H., and O. P. Ball. 1954. Description of eggs and larvae can be established (Boisvert; in press). of jack mackerel (Trachurus symmetricus) and distribution and Eusthenopteron foordi also differs signi®cantly from later abundance of larvae in 1950 and 1951. U.S. Fish and Wildlife Carboniferous tetrapods in the apparent absence of a recognized Service Fisheries Bulletin 56:209±245. larval stages and a de®nitive metamorphosis. Bemis and Grande Andrews, S. M. 1977. The axial skeleton of the coelacanth Latimeria; pp. 271±288 in S. M. Andrews, R. S. Miles, and A. D. Walker (1999:45) describe metamorphosis in the paddle ®sh Polyodon (eds.), Problems in Vertebrate Evolution. Linnean Society Sym- as occurring ``when the external shapes of the ®ns reach their posium Series, No. 4. Academic press, London. approximately adult appearance, and adult coloration and feed- ÐÐÐ, and T. S. Westoll. 1970. The postcranial skeleton of Eusthen- ing mode are achieved.'' In even the smallest known specimen opteron foordi Whiteaves. Transactions of the Royal Society of of Eusthenopteron foordi (at 29 mm), the lepidotrichia cover Edinburgh 68:207±329. all of the ®ns, which does not happen until after metamorphosis Arratia, G. 2001. Vertebral column and associated elements in dipnoans in Polyodon. This might indicate that all the specimens of and comparison with other ®shes. Journal of Morphology 250:101± Eusthenopteron foordi used in this study were post-metamor- 172. phic, or that this species developed directly, with the hatchling ÐÐÐ, and H.-P. Schultze. 1992. Reevaluation of the caudal skeleton of certain actinopterygian ®shes III. Journal of Morphology 214: alreadying attaining the general body form of the adult. 187±249. Amphibian metamorphosis may only have became evident Arsenault, M. 1982. Eusthenopteron foordi, a predator on Homalacan- with the evolutions of a clearly biphasic life history, with a thus concinnus from the Escuminac Formation, Miguasha, Quebec. long period of aquatic development, followed by emergence on Canadian Journal of Earth Sciences 19:2,214±2,217. land (Boy and Sues, 2000). This transformation is clearly evi- Bartsch, P., and S. Gemballa. 1992. On the anatomy and development dent in labyrinthodonts, whose larvae had external gills, but less of the vertebral column and pterygiophores in Polypterus senegalus well de®ned in lepospondyls, whose small, frequently elongate Cuvier, 1829 (``Pisces'', Polypteriformes). Zoologische Jahrbucher bodies would have resulted in a suf®ciently large surface to 122:497±529. volume ratio so that they may have been able to subsist on Bemis, W. E., and L. Grande. 1999. Development of the median ®ns of the North American paddle®sh (Polyodon spathula), and a reeval- cutaneous respiration both in the water and on land. uation of the lateral ®n-fold hypothesis; pp. 41±68 in G. Arratia and H.-P. Schultze (eds.), Mesozoic Fishes 2ÐSystematics and CONCLUSIONS Fossil Record. Verlag Dr. Friedrich Pfeil, MuÈnchen, Germany. Boisvert, C. In press. Vertebral development in modern salamander fam- The pattern of vertebral development seen in Eusthenopteron ilies with consideration of its evolution. Journal of Vertebrate Pa- foordi is different from that of any of the modern ®sh surveyed leontology 22(3, suppl.). and also differs from that in both the modern and fossil am- Boy, J. A., and H.-D. Sues. 2000. Branchiosaurs: larvae, metamorphosis phibians. Lepidotrichia appear in all ®ns very early in devel- and heterochrony in temnospondyls and seymouriamorphs; pp. opment. The ®rst endochondral bones to ossify are the supports 1,150±1,197 in H. Heatwole and R. L. Carroll (eds.), Amphibian Biology, Vol. 4. Palaeontology: The Evolutionary History of Am- for the caudal ®n, followed by those of the anal and dorsal ®ns. phibians. Surrey Beatty and Sons, Chipping Norton, Australia. Centra most likely ossify from the pelvic region forward. Trunk Bry, C. 1996. Role of vegetation in the life cycle of pike; pp. 45±67 in neural arches and pleurocentra are the last elements of the ver- J. F. Craig (ed.), Pike: Biology and Exploitation. Fish and Fisheries tebral column to begin ossi®cation. Dermal skull bones appear Series 19. Chapman and Hall, London. early in development, but the endochondral elements of the Carroll, R. L. 1988. Vertebrate Paleontology and Evolution. W. H. Free- braincase and palatoquadrate ossify signi®cantly later. This se- man & Co., New York, 712 pp. quence of ossi®cation suggests that effective aquatic locomo- ÐÐÐ, A. Kuntz, and K. Albright. 1999. Vertebral development and tion is critical in young Eusthenopteron foordi. Although Hox amphibian evolution. Evolution and Development 1:36±48. genes are expressed in an anterior to posterior sequence in all Chidiac, Y. 1996. Paleoenvironmental interpretation of the Escuminac Formation based on geochemical evidence; pp. 47±53 in H.-P. vertebrates, the sequence of chondri®cation and ossi®cation of Schultze and R. Cloutier (eds.), Devonian Fishes and Plants of vertebral elements is prone to modi®cation by environmental Miguasha, Quebec, Canada. Verlag Dr. Friedrich Pfeil. MuÈnchen, constraints and the functional needs of the animal. The diversity Germany. of patterns seen in modern ®sh indicates that both phylogeny Clack, J. A. 2000. The origin of tetrapods; pp. 979±1,029 in H. Hea- and adaptive factors play roles in the vertebral development of twole and R. L. Carroll (eds.), Amphibian Biology, Vol. 4. Palaeon- 502 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 22, NO. 3, 2002

tology: The Evolutionary History of Amphibians. Surrey Beatty ÐÐÐ, and E. H. Ahlstrom. 1970. Development of lantern®shes (fam- and Sons, Chipping Norton, Australia. ily Myctophidae) in the California Current. Part I, Species with ÐÐÐ, and M. I. Coates. 1995. Acanthostega gunnari, a primitive, narrow-eyed larvae. Bulletin of the Los Angeles County Museum aquatic tetrapod? Bulletin du MuseÂum National d'Histoire Natu- of Natural History, Science 7:1±145. relle, Paris 17:359±372. Parent, N., and R. Cloutier. 1996. Distribution and preservation of fos- Cloutier, R., S. Loboziak, A.-M. Candilier, and A. Blieck. 1996. Bio- sils in the Escuminac Formation; pp. 54±78 in H.-P. Schultze and stratigraphy of the Upper Devonian Escuminac Formation, eastern R. Cloutier (eds.), Devonian Fishes and Plants of Miguasha, QueÂ- QueÂbec, Canada: a comparative study based on miospores and ®sh- bec, Canada. Verlag Dr. Friedrich Pfeil. MuÈnchen, Germany. es. Review of Palaeobiology and Palynology 93:191±215. Pavlov, D. A., and E. Moksness. 1997. Development of the axial skel- Coates, M. I., and M. J. Cohn. 1999. Vertebrate axial and appendicular eton in wolf®sh, Anarhichas lupus (Pisces, Anarhichadidae), at dif- patterning: the early development of paired appendages. American ferent temperatures. Environmental Biology of Fishes 49:401±416. Zoologist 39:676±685. Potthoff, T., and S. Kelley. 1982. Development of the vertebral column, Crane, J. M., Jr. 1966. Late Tertiary radiation of viper®shes (Chaulio- ®ns, and ®n supports, branchiostegal rays, and squamation in the dontidae) based on a comparison of recent and Miocene species. sword®sh, Xiphias gladius. Fishery Bulletin 80:161±186. Los Angeles County Museum of Natural History Contributions in ÐÐÐ, S. Kelley, M. Moe, and F. Young. 1984. Description of pork®sh Science 115:1±29. larvae (Anisotremus virginicus, Haemulidae) and their osteological Dennison, R. H. 1968. The evolutionary signi®cance of the earliest development. Bulletin of Marine Science 34:21±59. known lung®sh, Uranolophus; pp. 247±258 in T. Orvig (ed.), Cur- Remane, A. 1936. Die WirbelsaÈule und ihre AbkoÈmmlinge; pp. 1±206 rent Problems of Lower Vertebrate Phylogeny. Nobel Symposium, in L. Bolk, E. GoÈppert, E. Kallius, and W. Lubsch (eds.), Handbuch No. 4. Almqvist and Wiskell, Stockholm. der vergleichenden Anatomie der Wirbeltiere, Vol. 4. Urgan and Dunn, J. R. 1984. Developmental osteology; pp. 48±50 in H. G. Moser Schwarzenberg. Berlin, Wien. (ed.), Ontogeny and Systematics of Fishes. Special publication Schultze, H.-P. 1984. Juvenile specimens of Eusthenopteron foordi Whi- Number 1, American Society of Ichthyologists and Herpetologists, teaves, 1881 (Osteolepiform Rhipidistian, Pisces) from the Late Allen Press Inc., Lawrence, Kansas. Devonian of Miguasha, QueÂbec, Canada. Journal of Vertebrate Pa- Goodrich, E. S. 1930. Studies on the Structure and Development of leontology 4:1±16. Vertebrates. London: Macmilan Co. Chicago: University of Chi- Schultze, N. C., and G. Arratia. 1986. Reevaluation of the caudal skel- cago Press, 1986, 837 pp. eton of actinoptergyian ®shes: I. Lepisosteus and Amia. Journal of Grande, L., and W. E. Bemis. 1998. A comprehensive phylogenetic Morphology 190:215±241. study of amiid ®shes (Amiidae) based on comparative skeletal anat- Shubin, N., C. Tabin, and S. Carroll. 1997. Fossils, genes, and the evo- omy. An empirical search for interconnected patterns of natural lution of animal limbs. Nature 388:639±646. history. Memoir 4 Society of Vertebrate Paleontology. Supplement Thomson, K. S., and K. V. Hahn. 1968. Growth and form in fossil to Journal of Vertebrate Paleontology 18(1), 690 pp. rhipidistian ®shes (Crossopterygii). Journal of Zoology (London) Hitchcock, E.-C. 1995. A functional interpretation of the anteriormost 156:199±223. Trueb, L., and R. Cloutier. 1991. A phylogenetic investigation of the vertebrae and skull of Eusthenopteron. Bulletin du MuseÂum Na- inter- and intrarelationships of the Lissamphibia (Amphibia: Tem- tional d'Histoire Naturelle, Paris 17:269±285. nospondylii); pp. 223±313 in H.-P. Schultze and L. Trueb (eds.), Mabee, P. M. 1993. Phylogenetic interpretation of ontogenetic change: Origins of the Higher Groups of Tetrapods. Comstock, Ithaca, New sorting out the actual and artefactual in an empirical case study of York. centrarchid ®shes. Zoological Journal of the Linnean Society 107: Wake, D. B., and N. Shubin. 1998. Limb development in the Paci®c 175±291. giant salamanders, Dicamptodon (Amphibia, Caudata, Dicampto- Milner, A. R. 2000. Mesozoic and Tertiary Caudata and Albanerpeton- dontidae). Canadian Journal of Zoology 76:2,958±2,066. tidae; pp. 1,412±1,441 in H. Heatwole and R. L. Carroll (eds.), Weisel, G. 1967. Early ossi®cation in the skeleton of the sucker (Ca- Amphibian Biology, Vol. 4. Palaeontology: The Evolutionary His- tostomus macroeheilus) and the guppy (Poecilia reticulata). Jour- tory of Amphibians. Surrey Beatty and Sons, Chipping Norton, nal of Anatomy 12:1±18. Australia. Wollom, J. 1970. Morphology and distribution of larvae and early ju- Mook, D. 1977. Larval and osteological development of the sheepshead, veniles of king mackerel, Scomberomorus cavalla, and spanish Archosargus probatocephalus (Pisces: Sparidae). Copeia 1977: mackerel, Scomberomorus maculatus; (Pisces; Scombridae); in the 126±133. western north Atlantic. M.S. thesis, University of South Florida, Moser, H. G. (ed.). 1984. Ontogeny and Systematics of Fishes. Special Tampa, 110 pp. publication Number 1, American Society of Ichthyologists and Her- petologists, Allen Press Inc., Lawrence, Kansas, 789 pp. Received 12 January 2001; accepted 25 September 2001.