The early formation of the skull in extant and Paleozoic amphibians

q 2002 The Paleontological Society. All rights reserved. 0094-8373/02/2802-0008/$1.00

Paleobiology, 28(2), 2002, pp. 278–296

The early formation of the skull in extant andPaleozoic amphibians

Rainer R. Schoch

Abstract.—Understanding of evolutionary changes in the vertebrate skull is greatly influenced bythe knowledge of ontogeny. Extant amphibians are an outstanding example in this field, becausetheir life cycles are complex and have been intensively studied. At the same time, fossil material ofPaleozoic amphibians has become available that sheds light on the ontogeny of a long-extinct clade,prompting comparison with recent forms. In this paper, the formation of the skull of a Paleozoicamphibian (the branchiosaurid temnospondyl Apateon) is analyzed in comparison with that of anextant salamander (the hynobiid Ranodon). Both temporal patterns (sequence of ossification) andspatial patterns (morphological changes) are described. The general results are that (1) the se-quence of ossification is similar in many aspects, and (2) most dermal bones share fundamentalsimilarities in morphogenesis, although sometimes the morphological result in adults may differconspicuously.

The comparison reveals that the parasphenoid, premaxillae, maxillae, frontals, parietals, squa-mosals, and prefrontals are strikingly similar in their mode of growth. In particular, the appearanceof the earliest primordia and the subsequent stages of morphological transformation are almostidentical. The development of the pterygoids and nasals is different in the earliest stages, but theontogenetic trajectories converge in later stages. In Ranodon and other transforming urodeles, thepterygoids and vomers experience extensive resorption during metamorphic climax, whereas inbranchiosaurids the morphology of this region remains stable throughout ontogeny.

In the sequence of cranial ossifications, the early appearance of the premaxilla and tooth-bearingelements of the palate characterize both genera, but the maxilla forms much later in Ranodon. Theectopterygoid, absent in all salamanders, is the last palatal element to appear in branchiosaurids.In the skull roof, the parietals, frontals, and squamosals are the first bones to form in both groups.Conversely, the circumorbital elements and tabular are among the last ossifications in branchio-saurids, and the prefrontal and lacrimal (the only circumorbital bones present in salamanders)form within the same interval in urodele ontogeny. The septomaxilla is the last dermal element toossify in both groups. Comparison with caecilians and anurans indicates that salamanders aremuch more similar to Paleozoic branchiosaurids than to other extant lissamphibians. A major dif-ference between salamanders and branchiosaurids is that the morphology of the latter is much lessaffected by developmental perturbations, such as larval specializations and metamorphosis.

Rainer R. Schoch. Humboldt Universitat zu Berlin, Museum fur Naturkunde, Institut fur Palaontologie,Invalidenstrasse 43, D-10115 Berlin, Germany. E-mail: [email protected]

Accepted: 23 January 2002

Introduction

Evolutionary developmental biology is arapidly developing field that integrates neo-and paleontological data in a fascinating way(Coates 1991, 1995; Caldwell 1994; Carroll1997; Carroll et al. 1999). Although paleontol-ogy may not be the prime source of evidencefor this field, there are cases in which well-pre-served growth series permit the comparisonof extant clades with long extinct ones. Anoutstanding, although as yet isolated, exampleof fossilized developmental stages is knownfrom a small clade of Paleozoic amphibians,the temnospondyl family Branchiosauridae. Inthis material, successive growth stages, whichare based on hundreds of specimens, allow

the study of bone formation in unparalleleddetail (Boy 1974; Schoch 1992, 1998). All larvalspecimens available for other Paleozoic andMesozoic amphibians, stem-tetrapods, andstem-amniotes are much larger and have morefully ossified skulls and postcrania (Boy 1974;Schoch in press). This paper analyzes for thefirst time the early ontogeny of the branchio-saurid Apateon caducus in comparison with sal-amanders, focusing on the supposedly ple-siomorphic hynobiid Ranodon sibiricus (Lebed-kina 1979).

The discovery of tiny amphibian skeletonsin Permo-Carboniferous sediments dates backto the middle of the nineteenth century (Mey-er 1848; Gaudry 1875; Fritsch 1876). Fossil ev-

279AMPHIBIAN SKULL FORMATION

idence of larval forms among extinct amphib-ians has accumulated subsequently (Watson1940, 1962; Romer 1947; Boy 1972, 1974, 1988,1995; Bolt 1977, 1979; Milner 1982; Werneburg1988, 1989; Klembara 1997; Dilkes 1991;Schoch 1992, 1995, 1998). Boy (1972) demon-strated that most of the larval specimens oncebelieved to represent immature eryopoid tem-nospondyls are instead mature larvae andneotenes of different groups of dissorophoids,a clade considered to be closely related to lis-samphibians by some authors (Reig 1964; Mil-ner 1988, 1993; Trueb and Cloutier 1991). Boy(1974) presented the first evidence for earlygrowth stages in branchiosaurid larvae, fromwhich crude data on the sequence of formationof bones were derived. Schoch (1992) analyzedthe ossification sequence of cranial bones intwo different species of the branchiosaurid ge-nus Apateon, based on a much larger sample.

In extant amphibians, ossification sequenc-es have been studied in salamanders, result-ing in a large body of comparative data (Wied-ersheim 1877; Parker 1879; Druner 1901; Stadt-muller 1924, 1936; Wilder 1925; Noble 1927;Aoyama 1930; Erdmann 1933; DeBeer 1937;Medvedeva 1959; Lebedkina 1964, 1968a,b,1979; Worthington and Wake 1971; Clemenand Greven 1974, 1977; Greven and Clemen1976, 1985; Wake et al. 1983; Hanken 1984,1999; Reilly 1986; Reilly and Altig 1996; Roseand Reiss 1993). The work of N. S. Lebedkina(summarized in Lebedkina 1979) has provid-ed the most detailed account of basal uro-deles, particularly hynobiids. She studied inparticular the ossification sequences in Rano-don sibiricus (Kessler 1866; Boulenger 1882;Dunn 1923; Lebedkina 1960, 1964, 1968a,b,1979) and Salamandrella keyserlingii (Strauch1870; Boulenger 1910; Dunn 1923; Lebedkina1979).

The present study compares the early larvalontogeny of two taxa representing largeclades, the Permo-Carboniferous branchio-saurid Apateon and the Recent hynobiid sala-mander Ranodon. The following traits were an-alyzed:

1. Spatial ossification patterns, assessed by(a) the morphology of bone primordia and (b)growth lines occasionally preserved in thesame specimen

2. Sequences of morphological transforma-tions studied in successively larger specimens

3. The chronological succession of first ap-pearance of bones during ontogeny

This study focuses exclusively on the cra-nium, with the goal of providing a frameworkfor the comparison of developmental events ata later stage in order to include additionaldata on the mandible, visceral skeleton, andpostcranium. The main aim of this study is tounderstand the profound morphological dif-ferences that separate Paleozoic and extantamphibians.

Materials and Methods

I studied 611 specimens of the branchio-saurid temnospondyls Apateon caducus and A.pedestris housed in the paleontological collec-tion of the Geological Institute at the Univer-sity of Mainz, Germany (GPIM 1230–1840).Developmental stages have been publishedelsewhere (Schoch 1992).

The recent material was mainly studied bymeans of thin-section series (Ranodon sibiricus,Salamandrella keyserlingii, and Ambystoma mex-icanum from the Severtsov Institute, Moscow;and Salamandrella keyserlingii from the Institutfur Systematische Zoologie, Tubingen) and invivo-stained specimens of Ranodon sibiricus,which were investigated in the collection ofDr. N. S. Lebedkina at the Severtsov Institute,Moscow.

This study deals in part with spatial ossifi-cation patterns of cranial bones, which are an-alyzed on the basis of quite different indica-tors in the fossil and Recent material. Figure 1summarizes the available body of evidence.Whereas specimens stained in vivo allow aninvestigation of actual growth increments in asingle individual, the study of fossils is main-ly confined to the analysis of previously de-termined growth series. Some of the studiedfossils, however, revealed actual growth incre-ments, present as growth lines.

The branchiosaurid material studied fallsinto numerous size classes that permit the rec-ognition of discrete growth stages, based ondifferences in morphology and the number ofbones present in the skull. The definition ofgrowth series relied on (1) consideration ofsize (measured by skull length rather than

280 RAINER R. SCHOCH


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FIGURE 1. Comparison of ossification sequences as correlated with size in Ranodon sibiricus and Apateon caducus.Abbreviations: anterior P 5 anterior anlage of parietal, ECPT 5 ectopterygoid, EO 5 exoccipital, F 5 frontal, J 5jugal, L 5 lacrimal, M 5 maxilla, N 5 nasal, P 5 parietal, PL 5 palatine, PM 5 premaxilla, posterior P 5 posterioranlage of parietal, PO 5 postorbital, PP 5 postparietal, PRO 5 prootic, PS 5 parasphenoid, PT 5 pterygoid, PTF5postfrontal, Q 5 quadrate, QJ 5 quadrojugal, SMX 5 septomaxilla, SQ 5 squamosal, ST 5 supratemporal, T 5tabular, VO 5 vomer. (Based on Lebedkina 1979, Schoch 1992, and new research.)

snout-vent length) and (2) ontogenetic ad-vancement. As size is known to be subject toextensive variation in extant amphibians, itcannot be regarded as a linear proxy of time.Therefore it could serve only as a gross guidein this study. Ontogenetic advancement wasmeasured by the number of bones present inthe skull, a method that rests on the hypoth-esis that the number of bones is more likely toincrease than decrease during ontogeny. On-togenetic advancement can be assessed onlyon the basis of articulated and well-preservedspecimens. This concept is only challenged bythe possibility that bone resorption might leadto a decrease of number of bones with onto-genetic age, but such a phenomenon has neverbeen observed in Paleozoic amphibians. Al-though resorption is common in salamandersand frogs, temnospondyls passed throughcontinuous stages of ossification with a grad-ual increase in bone thickness (Boy 1974; Boyand Sues 2000; Schoch 1998, 2001, in press).

I used numerous well-preserved specimens,all of which I collected in 1984–1986 from thesame locality at Erdesbach near Kusel, Saar-Nahe Basin, Germany, and from the same ho-rizon (Schoch 1992). These finds meet the nec-essary criteria for the interpretation of size se-ries as growth series (e.g., Schultze 1984). Twobranchiosaurid species, Apateon caducus and A.pedestris, are present in the locality, and theydiffer in the morphology of the skull roof andin absolute size. The growth series is morecomplete in the larger species, A. caducus,whose skull table is broader and is discernablefrom very small stages on (Schoch 1992). Thepresent comparative study is based exclusivelyon observations of material of Apateon caducus.

Patterns of Ossification

Spatial patterns of ossification include therelative position of bone primordia, their ini-tial morphology, and the mode of accretion

during growth (Figs. 2, 3). In Ranodon, thesedata have been gathered from specimensstained in vivo (Lebedkina 1979). The positionof cranial elements and accretion of bone werereadily traced in specimens treated with aliz-arine red S. In the branchiosaurid material,bone primordia are present as weak shadows,preserved in light brownish to red color andoften translucent with respect to the under-lying sediment (Schoch 1992). Accretion ofbone can be traced either by gradients of colorand transparency within the bone or by incre-mental growth rings; sometimes both are pre-sent.

Parasphenoid. The parasphenoid under-goes a complex development in both taxa (Fig.4). In Ranodon, primordia form first in the hy-pophyseal region. Mesenchymous tissue con-nects paired, spindle-shaped ossification cen-ters with the anterior end of the cartilaginoustrabeculae of the primordial braincase (Lebed-kina 1979). Bone formation follows thesestructures and then spreads medially fromboth sides to form the cultriform process. Thesmallest specimens of Apateon are preserved atequivalent stages, revealing almost the samemorphology and mode of growth. Paired boneprimordia, partially fused in the midline, arepreserved in several specimens of differentsizes (Schoch 1992).

In Ranodon, the hypophyseal region remainsunossified at the beginning, while the paras-phenoid expands posteriorly and laterally.Lateral to the hypophysis, and ventral to theconvergence of the trabeculae, the cultrifomprocess merges into the basal plate of the par-asphenoid. (The basal plate of the parasphen-oid is not identical with a mesodermal portionof the neurocranium also referred to as ‘‘basalplate’’.) The convergence of basal plate andcultriform process is marked by paired inden-tations, where the internal carotids penetratethe bone on their anterodorsal course toward


FIGURE 2. Growth series of skulls of Apateon caducus with poorly ossified elements stippled and fully formed bonesin black. Appearance of new bones correlates with skull size and the sequence of bone formation has been recon-structed from analysis of ;220 specimens representing the figured size range. (From Schoch 1992.)

the brain. In Apateon, the morphology is verysimilar: later growth stages suggest that theinternal carotids penetrated the element at thevery same position (Boy 1972; Schoch 1992).As ossification proceeds, the carotid groovesbecome longer and more clearly expressed. Insmall stages, the carotid foramina are markedby ascending processes, anterior and posteriorto the carotid, which merge in later stages toform a near-complete tube around the artery.

In the basal plate, early growth is subject toconsiderable variation, exemplified by thelarge number of specimens studied by Lebed-kina (1979). The parasphenoid of Apateon isalso variable, which is evident by differencesin growth lines and gradients of bone thick-ness. In both taxa, paired, laterally situatedprimordia of the cultriform process expandrapidly along their parasagittal axis. Whereasin Ranodon this has been studied on the basisof specimens stained repeatedly in vivo, in

Apateon numerous successive stages are con-served as growth lines in a single specimen,thus documenting the mode of accretion. Gen-erally, longitudinal growth of the cultrifromprocess is faster than that of the basal plate.The basal plate also remains weakly ossifiedin its central regions for a longer period. InRanodon, the region into which the basal platelater expands is marked by the notochord.There, the basal plate attains its postmeta-morphic morphology long after the comple-tion of the cultriform process and at about thesame time as the transformed vomer contactsthe parasphenoid. Larger specimens of Apa-teon have a broader, more differentiated basalplate and a narrower cultriform process. Theontogenetic trajectory of the parasphenoid isthus essentially similar in Ranodon and Apa-teon, although in the latter it seems to havebeen much more extended. A major differenceis that Apateon may have parasphenoid teeth


FIGURE 3. Skull roofs of the compared species in dorsal view, with bone primordia mapped onto fully formedbones. The size and position of each primordium, based on analysis of growth series both in the fossil and extantspecies, are precisely given. Abbreviations as in Figure 1. (Growth patterns of Apateon caducus based on Schoch 1992and that of Ranodon sibiricus on Lebedkina 1979.)


FIGURE 4. Parasphenoid of the compared species inventral view, with bone primordia mapped onto fullyformed bones. (Based on Schoch 1992 and Lebedkina1979.)

overlying the base of the cultriform process, afeature varying among different species (Boy1987; Werneburg 1989).

The three-dimensional structure of the par-asphenoid is unknown in Apateon. In Ranodon,the central region of the cultriform process isventrally concave. Apateon sometimes has anelongated ridge at the base of the cultriformprocess that may bear teeth or ill-defined ru-gosities. The basal plate may have shallow,paired impressions posterolaterally on itsventral surface (Schoch 1992). Similar impres-sions, as observed in hynobiids, are correlatedwith hypaxial musculature.

Vomer. The morphology of the larval vo-mer of urodeles is similar to that of temnos-pondyls and other Paleozoic choanates(Schoch 1998). Throughout ontogeny, the an-terior part of the palate is the main tooth-bear-ing region in Ranodon and most other uro-deles. In branchiosaurids this is only so in theearliest larval stages. The anlage and growth ofthe vomer have been thoroughly studied inRanodon and several other salamanders (Le-bedkina 1964, 1979). Tooth germs are gener-

ally found to appear before their associatedossifications and only later become attached tothem (Hertwig 1874). In the larval vomer thefirst tooth loci are arranged in a parasagittalrow. Once bones have started to form, a newtooth generation appears at the medial marginof the primordium, preceding the formationof new bone increments. The larval vomer firstexpands medially and anteriorly, and thegrowing bones rapidly contour the slit-shaped choana (Lebedkina 1979: Fig. 49), lo-cated close to the anterior end of the cultri-form process. The same patterning of ossifi-cation, and the resulting morphology, is foundin Apateon.

The first stage of metamorphosis, termed‘‘premetamorphosis’’ by Lebedkina (1979: p.87), is characterized by a resorption of the vo-mer and the sheets of connective fibers inwhich it is embedded. Major changes in tootharrangement occur before the onset of boneresorption. In Apateon neither resorption nortranslocation of tooth loci appears to have tak-en place. As Lebedkina (1979) clarified in ameticulous study, the orientation of connec-tive tissue fibers in Ranodon changes after theresorption of the posterolateral dentigerousprocess of the vomer. This process connectsthe vomer with the pterygoid in both larvalurodeles and temnospondyls, either by meansof a suture or by connective tissue. In addition,there is a vomero-pterygoid ligament presentin larval Ranodon (Lebedkina 1979: p. 91). Win-trebert (1922) reported resorption phenomenain several other urodele species, and this wascorroborated by Wilder (1920, 1925), DeBeer(1937), and Larsen (1963).

In transforming individuals of Ranodon, thechoana is shifted medially and its long axis ischanged from a parasagittal into a transversealignment. The vomer grows rapidly andforms the posterior and lateral margin of theinternal narial opening. By the end of meta-morphosis, the vomer has established contin-uous contacts with the maxilla and premaxil-la. There are no Paleozoic choanates that un-derwent similar changes. In Apateon, the po-sition and morphology of the choana isremarkably conservative in ontogeny, and invery large specimens the choana still has aslit-like outline. There are only a few disso-


rophoids that have transversely aligned cho-anae, whereas all other temnospondyls andbasal tetrapods have a parasagittally alignedchoana (Schoch 2001).

Pterygoid. This element differs in the tim-ing of its appearance in Ranodon and Apateon,but is fundamentally similar in spatial pat-terning. An anterior portion of the pterygoidhas caused some confusion because of its sep-arate anlage (Parker 1879; DeBeer 1937; Larsen1963; Lebedkina 1979; Trueb 1993). As arguedelsewhere (Schoch 1998), there is little if anyevidence that this portion represents the pal-atine, suggesting that this bone is entirely ab-sent in salamanders. Instead, this dentigerousprimordium posterior to the vomer moreplausibly constitutes the palatine ramus of thepterygoid.

The anterior portion of the pterygoid (pal-atine ramus) is the first to appear in both gen-era (Lebedkina 1979; Schoch 1992, 1998). Itforms in close proximity to the palatoquadratecartilage, which can be marked by staining inextant urodeles, and which can be deducedfrom cartilage impressions on the pterygoidin Apateon (Boy 1972). From the first stages on-wards, the palatine ramus bears numerousteeth. In urodeles, these are often located on awidened plate that extends medially to ap-proach or contact the cultriform process. InRanodon, the palatine ramus forms a thin,elongated strip that does not exactly followthe palatoquadrate cartilage (in large-larvalstages of Apateon, the pterygoid tends to en-tirely enclose the cartilage posteriorly, thusleaving characteristic impressions on the bonesurfaces that are morphologically virtuallyidentical in both species). In Apateon, the di-rection of pterygoid growth is more difficultto assess. Successively larger specimens indi-cate that it extends by prolonging both thepalatine process and the quadrate process.

The palatine process is the first portion toattain the stable, late-larval morphology inApateon. In Ranodon, however, this part is sub-ject to continued remodeling, as the interpter-ygoid vacuities successively open during lar-val development. This remodeling involvesextensive resorption.

In Ranodon, the morphological developmentof the pterygoid seems to parallel that of tem-

nospondyls, though at a much slower rate. Thesmallest specimens of Apateon possess narrowinterpterygoid vacuities, but they enlarge rap-idly during larval ontogeny. The quadrateprocess undergoes similar changes in Ranodonand Apateon. The major difference is that ingeneral the jaw articulation is much fartheranterior in salamanders than in branchiosaur-ids and most other temnospondyls. In post-metamorphic Ranodon, the quadrate process iselongate and faces posterolaterally, its poste-rior margin being at one level as the posteriorend of the basal plate. By the end of their de-velopment, the pterygoids of branchiosauridsand at least hynobiids are morphologicallysimilar, except for the remodeled palatine pro-cess in the former. The last pterygoid portionto form in both Ranodon and Apateon is the bas-ipterygoid process. In the latter, however, thisprocess expands during late ontogeny, as theposterior portion of the palate becomes slight-ly broader, a tendency not found in Ranodon.A general problem in the comparison of pter-ygoid growth patterns is the spatial arrange-ment of the bone primordia in small branchio-saurid larvae. Urodele development suggeststhat there may have been similar changes inthe 3-D patterning of the palatal elements.

Premaxilla. The premaxilla is similar inmorphogenesis in the two taxa but differs con-siderably in the elements it contacts in earlydevelopment (Fig. 3). Early stages are knownwell in Ranodon, where Lebedkina (1964) stud-ied the changes and contacts of the first pri-mordia in great detail. The alary process firstexpands ventrally to form the dental shelf,which rapidly grows in posterior and anteriordirections. Counterpart dental shelves meetearly (Lebedkina 1979), following connectivefibers in the anteriormost part of the planuminternasale. In Apateon, the premaxilla is pre-sent in the smallest specimens as a curvedbony strip forming the outline of the snout.The alary process first appears in slightlylarger specimens, and is already fully formed.Teeth are present in the smallest specimens.

The most conspicuous difference betweenRanodon and Apateon concerns the region ofthe nasal and alary process. The latter devel-ops much faster in Ranodon and normally con-tacts the frontal by an overlapping suture very


FIGURE 5. Comparison of ossification sequences of Apateon and Ranodon showing first appearances of bone primordia.The relative distance between single events is not to scale (the absolute age dates are highly variable in Ranodon,and growth stages need not correlate with absolute size in Apateon). Note the close match in the chronological se-quence of most bones; the delay in appearance of the maxilla correlates with the late onset of powerful biting inmost salamander larvae.


early in ontogeny (Lebedkina 1968b). In Apa-teon, frontal and premaxilla never meet anddo not even come close to one another (Schoch1992). In Ranodon, the frontal and premaxillaare successively separated by the nasal, andthe adult morphology does not differ substan-tially from that of Apateon as displayed fromearly stages onwards.

Frontal. In the frontal region, weakly os-sified platelets are preserved in small bran-chiosaurid larvae, permitting the study of de-tails such as the formation of sculpturing andincrease in bone thickness (Schoch 1992).Shape changes and increases in area are verypronounced in successively larger specimens(Figs. 2, 3). This forms a sound basis for com-paring bone formation in dermal elements ofApateon with in vivo-stained ossifications ofRanodon.

In Ranodon, the earliest primordia of thefrontals are very thin, parasagittally alignedbars. They form along connective fiber bun-dles located dorsal to the taeniae of the neu-rocranium (Lebedkina 1968a, 1979: Fig. 83).The primordia first grow anteriorly to contactthe premaxillae and posteriorly to meet theparietals, and only later do they start to formbroader ossified plates. In Apateon, frontalgrowth reveals the following: in the smallestspecimens in which frontals are preserved,they constitute elongated strips medial toblack stains in the eye region (Schoch 1992).The frontals commence ossifying along theirlateral border, exactly as in Ranodon. Theygrow more rapidly in the anteriomedial direc-tion than posteromedially, where a large fon-tanelle persists, the precursor of the pineal fo-ramen. In contrast to Ranodon, where frontaland parietal primordia are arranged in oneline, in Apateon the frontal primordium isfound lateral to that of the parietal. Growth in-crements are preserved only in the medialpart of the frontal, whereas the parietals evi-dently expand in all directions with growth.In most urodeles the frontal primordium alsogrows in all directions (Lebedkina 1979). Theadult morphology is quite different: Apateonhas broad frontals with pronounced postero-lateral outgrowths to which the postfrontalsattach later. In Ranodon, the parietals are muchwider than the frontals, and the latter do not

extend posterolaterally; urodeles also lack apostfrontal. However, an anterolateral broad-ening of the frontals is found in both Apateonand Ranodon, and this is associated with theappearance of a tiny prefrontal later in devel-opment.

Medial growth of the frontals varies consid-erably in both species, resulting in numerousspecimens that retain large fontanelles; somehynobiids and many plethodontids retainsuch openings even long after metamorphosis(Wilder 1925; Lebedkina 1979). Occasionally,in branchiosaurids the median margins of thefrontals are curved and consist of several pro-tuberances where the bone was growing mostrapidly. The fontanelle—except for the per-sisting pineal foramen—is closed in all spec-imens larger than 7 mm skull length, but mayoccur in individuals of only slightly morethan 4 mm length (Schoch 1992). The suturaltopography at the anterior margin of the fron-tals is almost identical in both species, where-as the suture with the parietals is different. InApateon, the posterolateral process of the fron-tal overlaps the lateral margin of the parietal,and anteromedian processes of the parietalscontact or overlap the posteromedian marginsof the frontals, a common suture topographyin basal tetrapods.

Parietal. In Apateon, the parietal appears atthe same time as the frontal but is somewhatsmaller initially and develops at a slower rate.In Ranodon, it is actually a compound element,including a posterior, transversely elongatedossification, which has been discussed else-where (Lebedkina 1979; Schoch 1998) and willbe treated below under a separate paragraph.In its earliest stages, the parietal proper ofRanodon (i.e., the anterior primordium) arisesfrom one or two parasagittally aligned ossi-fication centers (Lebedkina 1979); fusion ofthese occurs in a very early state, and so mightnot be recognized in fossil growth stages. InApateon, there is always a single ossificationcenter of the parietal (Fig. 3).

Squamosal. In Ranodon, the squamosal aris-es from two originally separate centers: a‘‘squamosal part’’ situated on top of the au-ditory capsule, and a ‘‘palatoquadrate part’’covering the palatoquadrate process. Aftertheir fusion, the ‘‘squamosal part’’ contacts


the parietal at later stages. According to Le-bedkina (1979), fusion occurs rapidly in allspecimens. In Apateon, the anlage of the squa-mosal resembles the ‘‘palatoquadrate part’’ ofRanodon, in both its position and its mode ofgrowth. In both genera, a thin transverse barappears first and broadens medially later. The‘‘squamosal part’’ is not observed in Apateon,but it is known that the supratemporal formedin a similar position. This element originatedat the medial margin of the squamosal andafterwards grew medially and anteriorly, latercontacting the parietal. From its position andmode of mineralization, the supratemporal issimilar to the ‘‘squamosal part’’ of the com-pound squamosal ossification in Ranodon.Without more precise topological and devel-opmental information, however, it is not pos-sible to determine if Ranodon possesses a su-pratemporal in early stages, let alone resolveproblems posed by conflicting evidence inphylogenetic analysis.

What can be said is that the mode of growthof the ‘‘palatoquadrate part’’ in Ranodon isvery similar to that in Apateon. First an elon-gated ossified bar forms that becomes broaderlater, particularly medially. Broadening of thedistal end—relative to the progress in the restof the skull—is much slower in Ranodon,where it occurs about at metamorphosis. Be-cause of a higher rate of ossification, Apateondevelops a much larger squamosal that partic-ipates in an entirely closed cheek region in theadult stage (Schoch 1992), which representsthe plesiomorphic condition for tetrapods.

In both genera, the squamosal is short andoriented anterolaterally in the first stages ofdevelopment. Whereas in Apateon the elementrotates into a more posterolateral alignmentby the early larval period, such a rotationtakes place much more slowly and ceases ear-lier in Ranodon. A slight posterolateral orien-tation is established only after metamorphosisin this taxon, resembling the condition insmall Apateon larvae (Fig. 3).

Posterior Parietal. The separate, posterioranlage, which later forms part of the parietal,grows along a transverse axis. It remains iso-lated from the parietal for a long but variableperiod (Schmalhausen 1968; Lebedkina 1979).In Ranodon and Salamandrella, this bone is as-

sociated with the neck musculature, especiallythe M. longissimius dorsi, to which it attaches.Other urodeles have only one parietal ossifi-cation center (Larsen 1963; Worthington andWake 1971). In Apateon, epaxial musculatureprobably attached to the postparietal (as sug-gested by posterior shelves bearing musclescars), which is aligned in a similar way andlocated at the same position as the posteriorparietal anlage of the urodeles cited above. Theresemblance of this bone primordium withthe postparietal of early tetrapods and tem-nospondyls has recently been discussed in de-tail (Schoch 1998).

Quadratojugal. A quadratojugal is absentin Ranodon, but Lebedkina (1979) reported abone she referred to as the quadratojugal inSalamandrella. It occupies the position of thequadratojugal in other tetrapods, but duringlater development it fuses with the quadrateossification. The first anlage of this primordi-um is elongated, is sagittally oriented, and liesin close proximity to the distal end of thesquamosal. The latter overlaps it and forms asquamous suture. It remains unclear whetherthis primordium represents a true quadrato-jugal, as it does not occur in other salaman-ders. In Apateon, a true quadratojugal is pre-sent and looks rather different from the pri-mordium in Salamandrella. It does not under-lap the squamosal, it is initially short andbroad, and growth proceeds mainly in the an-terior direction, tending to contact the jugaland maxilla later in development. In urodelesthe quadrate region and maxilla never meet(Larsen 1963). The compound quadrate ele-ment in Salamandrella has a massive, globulartrochlear part and an elongated, flat, andknifelike medial part that contacts the squa-mosal. In Apateon, as in most basal tetrapods,the quadratojugal is a dorsolaterally curvedplate with an anterolateral process that by latelarval stages is wedged in between the squa-mosal, maxilla, and jugal. The quadrate re-mains unossified and hence is unknown inApateon. There is no evidence among Paleozoicstem-amniotes and temnospondyls that thequadrate ever fused to the quadratojugal.

Nasal. The nasal arises from two indepen-dent ossification centers in Ranodon (Lebed-kina 1979), which are situated medial and lat-


eral to the long ascending process of the pre-maxilla (Fig. 3). This condition is probably de-rived within urodeles, because in othersalamanders there is only one nasal primor-dium (Larsen 1963; Reilly and Altig 1996). InRanodon, the two anlagen of the nasal fuse ear-ly and grow beneath the contact between thepremaxilla and frontal, until the nasal finallyseparates these elements. After the metamor-phic climax, the nasal is much wider posteri-orly than anteriorly and contacts the prefron-tal, lacrimal (if present), maxilla, frontal, andpremaxilla. The premaxilla overlaps it slightlyin the anteromedial region. A similar topolo-gy and morphology are attained rather earlyin the ontogeny of Apateon, where the nasaldevelops from only a single primordium ori-ented transversely and located close to the an-terior margin of the frontals. The latter fail tocontact the ascending processes of the pre-maxillae throughout ontogeny. Interestingly,the adult morphology of the nasal is remark-ably similar in Ranodon and Apateon.

Prefrontal. This bone is the only element inthe circumorbital series that is retained in themajority of urodeles, and its modes of originand growth are similar in Ranodon and Apa-teon. In both genera, it forms at the anterolat-eral edge of the frontal. The initial primordi-um has a curved outline, which forms themargin of the orbit. During later stages itbroadens and develops a marked anterior pro-cess, which forms only facultatively, depend-ing on ossification rate and final body size.The first contact it forms is with the frontal,then with the maxilla (or lacrimal) and finallywith the nasal. The mode of growth, as well asthe sequence in which elements develop con-tacts, is identical in both taxa. However, thedevelopmental trajectory proceeds much fur-ther in branchiosaurids than in urodeles. As aresult, the contact with the nasal may not beestablished and a large area of the snout re-mains unossified in most urodeles.

Lacrimal. The lacrimal is present as an in-dependent element in only a few urodele gen-era (Larsen 1963; Trueb 1993) and its fate inothers is uncertain. Lapage (1928) showed thattogether with the septomaxilla, which formssomewhat later, its presence is correlated withthat of the nasolacrimal duct, which in basal

tetrapods appears to be represented by agroove on the lacrimal (Boy 1972, 1974, 1988).The mode of ossification is largely unknownin Apateon, as the element already has its char-acteristic shape by its first appearance. In Ran-odon, Lebedkina showed that the lacrimalstarts to ossify shortly after the prefrontal byforming a tiny bony bar. The element laterelongates anterolaterally and wedges in be-tween the maxilla and nasal; the resulting to-pology is similar to that of branchiosaurids,although the bone is somewhat narrower andsmaller in Ranodon.

Septomaxilla. The formation of this ele-ment in urodeles has been extensively studiedby Schmalhausen (1968) with Ranodon sibiricusas the main focus. Lapage (1928) and Larsen(1963) have commented on the septomaxilla insalamanders in general. In Apateon this boneappears only in very large specimens. Unlikein Ranodon, the external, sculptured part of theelement attaches to the lacrimal and maxilla.

Maxilla. The first anlage of the maxilla en-compasses the tooth-bearing dental shelf andis succeeded by the formation of the dorsalprocess, which soon contacts the prefrontal bymeans of connective fibers. In Apateon thesame morphological transformations occurand are followed by a marked longitudinalgrowth of the dental shelf. In larger larvae ofbranchiosaurids, the quadratojugal is contact-ed by a long dental shelf, a situation not foundin urodeles. In Ranodon, the maxilla remainssimilar to that of small branchiosaurid larvaein being nearly as short as the premaxilla andhaving a rudimentary ascending process.

Stapes (Columella). The stapes is wellknown in many fossil amphibians, and in Tri-assic stereospondyls it reached extreme sizesof more than 100 mm length (Schoch 2000;Schoch and Milner 2000). Although most tem-nospondyls have stapes with two proximalheads (Bolt and Lombard 1985), similar to ex-tant anurans, the weakly ossified ear ossiclesof dissorophoid larvae often resemble sala-mander stapes in being poorly differentiatedand in having a single large head (Boy 1995;Schoch 1999). Apateon has a short stapes thatossifies long after the completion of the der-mal skull roof. Poorly differentiated at first, ithas a broadened proximal head in larger


growth stages and is perforated by a stapedialforamen (Boy 1972). Apparently, the shaft os-sifies first and then the footplate follows. InRanodon, the stapes ossifies first in the regionof the footplate and then growth proceeds dis-tally to form a comparably short shaft (Lebed-kina 1979). Larsen (1963) reported that thismode of ossification is common among uro-deles, whereas the relative time of appearanceof the stapes varies broadly among salaman-ders (Kingsbury and Reed 1909).

Bones Exclusive to Apateon. The palatineand ectopterygoid are absent in salamanders(Schoch 1998), although the former has some-times been presumed to occur in larval stages(Larsen 1963; Trueb 1993). The supratempor-al is also clearly absent in all urodeles.Schmalhausen (1968) hypothesized that theposterior part of the parietal, which is similarto the postparietal (Schoch 1998), might bethe supratemporal. The supratemporalshould, however, be sought in the region dor-sal to the prootic, which lacks dermal ossifi-cations in Ranodon and other hynobiids. Thelatest elements to appear in branchiosauridsare the postfrontal, postorbital, tabular, andjugal; these are all absent in salamanders.They have in common that their first primor-dia are thin, curved bars that parallel themargin of the orbit and posterior skullboundary, respectively. The growth of the ju-gal is most peculiar: it starts with a rhom-boidal, entirely isolated primordium andonly late in ontogeny does it contact the post-orbital, maxilla, and quadratojugal (Schoch1992). The question whether the separatebonelet in the cheek of Salamandrella actuallyconstitutes a quadratojugal cannot be re-solved at present.

Bones Exclusive to Ranodon. Urodeles aremore similar to anurans and caecilians, andquite distinct from branchiosaurids, in thatparts of their neurocrania ossify early. In Ran-odon, the sphenethmoid, prootic, exoccipital,and quadrate all form during metamorphosis,or even prior to this event, which takes placeat about the same time as the appearance ofthe prefrontal, lacrimal, and maxilla. Wor-thington and Wake (1971) mentioned three os-sification centers in the otic region of Rhyaco-triton larvae and stressed their uncertainty

about the homology of these bones. They sug-gested that they were replacement ossifica-tions of the neurocranium, referred to as thepterotic, prootic, and exoccipital. By contrast,in Apateon, all dermal elements of the craniumossify well before even faint traces of bone oc-cur in the neurocranium. Although bone hasbeen recognized in the sphenethmoid andquadrate regions of large Apateon specimens,the auditory capsules and palatoquadrate re-gion remain entirely unossified.

Developmental Sequences

The chronology of ossifications in the uro-dele cranium reveals a relatively stable pattern(DeBeer 1937; Lebedkina 1979). There are sev-eral groups of bones, each characterized bytheir coordinated appearance within the os-sification sequence. The parietals, frontals,and squamosals, for instance, always formearly in larval development. In Apateon, thesame can be seen: the sequence of bone ap-pearance is not gradual, but stepwise, andfalls into well-defined clusters.

A consistent sequence within each of thesebone groups is not found, however. The pari-etal, for instance, may appear in concert withor slightly after the frontal, as does the squa-mosal. Obviously these bone groups consti-tute developmentally regulated and function-ally integrated units, which may shift as awhole within the developmental sequencerather than act in a dissociated fashion. If com-pared with the closely related Salamandrellakeyserlingii, the earliest stages of Ranodon sibir-icus are similar with the exception that the cor-onoid and dentary appear before the ptery-goid and vomer. This demonstrates that thegross resolution of fossil ontogenetic series isnot necessarily poorer than the sequences ob-servable in Recent urodeles.

Whereas the tooth-bearing elements (vo-mer, pterygoid, dentary, and coronoid) form afunctionally integrated jaw apparatus (theyappear shortly after the opening of the mouth[see Lebedkina 1968a]), the frontals, parietals,squamosals, prearticulars, and angulars areassociated with the jaw-closing musculature(the adductor mandibulae internus and pos-terior), as Lebedkina (1979) demonstrated. Inother developmentally linked bone clusters,


the functional context remains poorly under-stood and is probably more complex.

Similarities. As exemplified by the generaRanodon and Apateon, hynobiid salamandersand branchiosaurid temnospondyls share thefollowing sequence of ossification (Figs. 1, 2,5):

1. Pterygoid (palatine process), coronoid,dentary, parasphenoid

2. Premaxilla, vomer3. Frontal, squamosal, parietal4. Postparietal in Apateon, posterior parietal

primordium in Ranodon5. Nasal6. Prefrontal, lacrimal7. SeptomaxillaThe lacrimal is absent in most salamanders,

as is the posterior parietal primordium; how-ever, the latter needs thorough developmentalstudies, which have not been carried out formost other urodele species. In direct-devel-oping plethodontid salamanders, the generalossification sequence is quite different, al-though Wake and Hanken (1996) showed thateven there, parts of the larval pattern havebeen conserved.

Differences. Ranodon and Apateon differquite considerably in the appearance of cer-tain bones, as follows:

1. The prearticular and pterygoid (quadrateprocess) appear later in Ranodon (stage 3) thanin Apateon (stage 2).

2. The maxilla appears very late in Ranodon(stage 5), as in many urodeles, but at stage 2in Apateon. However, in Amphiuma, Rhyacotri-ton, and Ambystoma, the maxilla forms rela-tively early in ontogeny, whereas in sirenids itis a tiny ossicle and in proteids it is absent al-together (Larsen 1963).

3. The ectopterygoid is the last tooth-bear-ing element to appear in branchiosaurids (ap-pearing between stages 3 and 4), but is clearlyabsent in all salamanders.

4. The supratemporal appears betweenstages 3 and 4 in Apateon; there is no unequiv-ocal evidence of this bone in any urodele(Schoch 1998).

5. The postfrontal, postorbital, jugal, andtabular are absent in all salamanders; they ap-pear between stages 6 and 7 in the develop-mental sequence of Apateon.

6. Bone formation in the neurocraniumstarts much earlier in Ranodon (and most uro-deles) as compared with Apateon. In the latter,only the earliest stages of sphenethmoid os-sification are actually known. There are, how-ever, numerous temnospondyls with endocra-nial ossifications comparable to urodeles, no-tably dissorophoids (Amphibamus, Micropholis,and Doleserpeton). This suggests that Apateonand branchiosaurids in general are an excep-tion among temnospondyls in the slow com-pletion of endocranial ossifications. The pre-sent phylogenetic concept of temnospondylssupports this, as mapping of braincase char-acters on an independently derived phyloge-ny demonstrates (Schoch 1999, 2002). Accord-ing to these studies, the sphenethmoid, otic,and exoccipital regions were substantially os-sified in most temnospondyls and are knownfrom small growth stages in a range of taxa.

Relative Truncation of Developmental Trajecto-ries in Ranodon. The developmental trajecto-ries of most bones are much simpler in Rano-don as compared with Apateon. Although mor-phological transformations are essentiallysimilar in early development, later phases ofontogeny appear to be truncated in Ranodon(Figs. 3, 4). This is suggested by the study ofthe parasphenoid, the vomer, and the ptery-goid:

1. The parasphenoid, especially the basalplate, differentiates very slowly in Ranodon.This is remarkable because the morphologicalchanges of the element are so similar in thetwo genera (position and morphology of firstprimordia, formation of cultriform process,patterning of basal plate, ascending processes,and carotid channel). The cultriform processremains relatively wide even after metamor-phosis, a feature typical of medium-sized Apa-teon larvae. The basal plate becomes widerthrough metamorphosis, and in that resem-bles that of branchiosaurids closely. However,it retains poorly ossified posterior and lateralmargins, which are more elaborate in manybranchiosaurids and most other temnospon-dyls.

2. The larval vomer starts to obliterate longbefore it has reached a morphology similar tothat of large Apateon. The adult vomer, whichforms rapidly during metamorphosis, is to-


pologically quite different from that of bran-chiosaurids and most other temnospondyls(Schoch 1998).

3. The palatine ramus of the pterygoid is re-sorbed early in Ranodon, a phenomenon fre-quent among transforming urodeles (Larsen1963). However, in neotenes of Ambystomamexicanum and Dicamptodon ensatus, the pter-ygoid and vomer are more heavily ossifiedand appear to have proceeded much furtheralong the larval ontogenetic trajectory. Inthese taxa, a distinct quadrate ramus isformed that is quite similar to that of temnos-pondyls, and the dentition of the pterygoidhas changed from numerous larval to a fewadult teeth, which are arranged in a singlerow.

Relative Prolongation of Developmental Trajec-tories in Ranodon. In one case, a developmen-tal trajectory of Ranodon (and other urodeles)is extended relative to that of Apateon. The ala-ry process of the premaxilla grows at an ac-celerated rate and forms a suture with thefrontal in Ranodon. This situation is clearly de-rived, because throughout Paleozoic choana-tes, anurans, and caecilians the alary process(if present) is small and well separated fromthe frontal by the nasal. In Ranodon, the alaryprocess thus proceeds along the trajectory ev-ident in Apateon, but goes far beyond this inproducing an extremely elongated process,which changes even the topology of the skullelements. In salamanders of other families,this trajectory is even more complex, as Larsen(1963) and Wake and Larson (1987) have dem-onstrated in detail.

Discussion

The similarities of ossification patterns insalamanders and temnospondyls are pro-found and contrast strongly with the situationin anurans (Trueb 1985; Hanken and Hall1988) and caecilians (Wake and Hanken 1982;Reiss 1996). Urodele larvae are, as Boy (1974)concluded from a more limited data set, es-sentially similar to small temnospondyls. Thissimilarity is not restricted to morphology andthe spatial patterning of bone formation, butalso concerns the timing of developmentalevents. In fact, these ossification sequences areremarkably similar even in details, suggesting

that developmentally linked bone clustersmight have been phylogenetically conserved.The morphology of small larvae of other tem-nospondyl clades (Cochleosauridae, Saurer-petontidae, Eryopidae, Actinodontidae) sug-gests that many features of branchiosaurid lar-vae are in fact plesiomorphic (Credner 1882;Steen 1938; Boy 1974, 1988; Milner 1982).

Homology Assessment. Hynobiids appear tohave one of the most complex ossification se-quences among urodeles, as measured by thenumber of bone primordia initially present inearly ontogeny, yet this does not necessarilymean that they are plesiomorphic in this re-spect. It is as parsimonious to assume thatbone primordia have split in phylogeny as toassume that they represent the ancestral con-dition. Clearly, the significance of each ossifi-cation needs to be evaluated separately. Themain criteria to be met are obviously out-group comparisons regarding (1) topologicalidentity, (2) similar ontogenetic patterns, (3)clear phylogenetic polarity, and (4) evidenceon the occurrence of a bone in the primitivecondition of the studied clade, as assessed bycongruent character distribution. The last cri-terion is the most difficult one, because itneeds extensive knowledge of representativetaxa within the clade.

The lacrimal and prefrontal of salamandersare likely to be homologs of the lacrimal andprefrontal in other tetrapods. In the retentionof these elements as separate bones in theskull roof, hynobiids are probably indeed ple-siomorphic with respect to those salamanderslacking these elements, because they satisfythe topological and ontogenetic homology cri-teria. Whereas the prefrontal is present in rep-resentatives of all but two salamander families(the sirenids and proteids), the lacrimal is pre-sent only in three urodele clades—the hyno-biids, dicamptodontids, ambystomatids—andin the genus Rhyacotriton (Larsen 1963; Wor-thington and Wake 1971). The nasal is also ab-sent in some urodeles, and it differs in the ear-ly patterning of anlagen (Larsen 1963). How-ever, both its position and its occurrence inmany salamanders strongly suggest it to behomologous with the lacrimal of other tetra-pods.

The homology is much less clear in the cases


of the quadratojugal, posterior parietal, andpalatine. The quadratojugal has been reportedonly in Salamandrella and a few other urodeles(Papendieck 1954), and there it fuses at an ear-ly stage with the quadrate. Its morphology ispoorly established before the fusion andtherefore cannot readily be compared withprimordia of the true quadratojugals in othertetrapods. The posterior parietal also fuses atan early stage with the main body of the pa-rietal, and it has only been found in a singlespecies, Ranodon sibiricus. Although it meetsall topological and ontogenetic homology cri-teria, its distribution among taxa does not givea clear phylogenetic signal. The so-called pal-atine of larval salamanders has been observedin a range of taxa (Trueb 1993), but only rarelyhas it been proven to form from a separate an-lage (hynobiids [Lebedkina 1979]). In sum, thepresent findings might turn out to be helpfulin addressing homology problems in sala-manders, but only (1) if branchiosauridsproved to be closely related to salamanders,and (2) if a congruent distribution of charac-ter-states within the Urodela can be con-firmed. In some other cases, we are probablyconfronted with effects of what has beentermed latent homologies (Hall 1995; Wake1996)—intriguing and tantalizing, but ulti-mately not decisive evidence.

Phylogenetic Polarity and Heterochrony. Theossification sequence preserved in branchio-saurids has revealed characters that are en-tirely different from the static morphologicalfeatures usually dealt with in paleontologicalstudies. From this perspective, orthodox char-acters appear to be mere snapshots of ontog-eny, and their fossilization seems rather ser-endipitous. In amphibians, both fossil and Re-cent, this is a significant problem, because lifecycles are complicated and differ substantiallybetween clades. Consideration of this problemraises serious questions about the reliability ofcharacter recognition in cladistics, as long asthis uses static morphological features.

Further, the present findings demonstratethat similar developmental patterns may re-sult in rather different morphological condi-tions. There are two alternative reasons forthis: either (1) an essentially similar develop-mental trajectory has been truncated so that it

stops at an earlier state in one taxon as com-pared with another, or (2) the chronologicalsuccession of events on the trajectory has beenaltered, even though the events themselves arestill similar. Both cases are likely to occur inthe studied example. However, without deter-mining phylogenetic polarity, further inter-pretation of these patterns is of little help.

Outgroup comparison seems to be the onlyway to meet this problem, but as branchio-saurids are the only case among extinct basaltetrapods in which early ossification sequenc-es have been fossilized, the only conceivableoutgroups are distant taxa such as extant dip-noans, Latimeria, and cladistian actinoptery-gians. However, these are highly derivedthemselves and their use as outgroups in thepresent case is at least difficult to assess. Thiswould require a detailed study with a differ-ent focus that is far beyond the frame of thepresent paper. The phylogenetic hypothesesproposed for the origin of extant amphibiansand their relationships to fossil taxa are radi-cally different (Milner 1988, 1993; Laurin andReisz 1997), and with the presently availablemorphological characters there is little chanceto resolve the problem.

There are nonetheless related questions thatcan be addressed with knowledge from thefossil record of basal tetrapods, and in partic-ular with additional ontogenetic data derivedfrom other temnospondyls. This source of in-formation is, however, restricted to rather gen-eral observations regarding the compositionof the skull in basal tetrapods and the patternof growth during the late larval period.

1. Although the maxilla develops much laterin Ranodon than in Apateon, the two taxa sharein common the slow posterior growth of thedental shelf. Salamanders vary in the early an-lage and also have different growth rates of thetooth-bearing shelf, but they never reach thetruly ancestral state in which the maxilla iselongated from small larval stages onwardsand firmly integrated into the cheek. The lat-ter condition is found in all temnospondylsexcept branchiosaurids (Steen 1938; Boy 1974;Boy and Sues 2000). Likewise, there is noknown microsaur, anthracosaurid, or sey-mouriamorph with such a foreshortened max-illa, which suggests that the primitive condi-


tion was a maxilla that integrated rapidly intothe cheek portion of the skull. The similarityin the slow completion of the maxilla may bea true synapomorphy of salamanders andbranchiosaurids, but a similar foreshortenedmaxilla does also appear in lysorophians(Wellstead 1991).

2. The absence of postfrontal, postorbital,tabular, and jugal is especially interesting, be-cause these elements formed at about the sametime and they were the last bones to appear inthe cranial ossification sequence of branchio-saurids. These bones form part of the ancestralcomplement of the skull in tetrapods, as vir-tually every basal tetrapod clade demon-strates. Thus, there can be little doubt that theoccurrence of these elements in branchiosaur-ids is a plesiomorphic character state. Giventhat this pattern is the primitive condition, sal-amanders must represent the derived state inwhich the bones are absent. Thus, truncationof the branchiosaurid trajectory prior to theformation of these bones would result in thesalamander condition. This idea matches ob-servations of the small branchiosaurid Apateondracyiensis, which lacks a jugal in the adultstage and whose ontogeny appears to havebeen truncated with respect to A. caducus (Boy1987). The absence of the jugal, postorbital,and postfrontal in the heavily paedomorphiclysorophians (Wellstead 1991) is another ex-ample.

Acknowledgments

I thank N. S. Lebedkina and S. V. Smirnovfor stimulating discussions, as well as theirhospitality during my stay in Moscow. A. R.Milner and M. I. Coates reviewed an early im-mature version of this manuscript, whichmade me re-think several points and focusmore deeply on various subjects. J. A. Boy, K.Padian, D. B. Wake, F. Westphal, W.-E. Reif,and W. Maier have supported this and relatedprojects in many ways. I finally thank the tworeviewers who have helped improve the con-tents and shape of the article substantially,and D. Unwin, F. Witzmann, and N. Atkins forfurther helpful comments on the revised man-uscript.

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The early formation of the skull in extant and Paleozoic amphibians