Seminars in Cell & Developmental Biology 21 (2010) 424–431

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Seminars in Cell & Developmental Biology

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Review

Amphibian development in the fossil record

Nadia B. Fröbischa,∗, Jennifer C. Olorib, Rainer R. Schochc, Florian Witzmannd

a Department of Organismal Biology & Anatomy, University of Chicago, 1027 E 57th Street, Culver 108, Chicago, IL 60637, United Statesb Jackson School of Geosciences, The University of Texas at Austin, 1 University Station C1100, Austin, TX 78712-0254, United Statesc Staatliches Museum für Naturkunde Stuttgart, Rosenstein 1, 70191 Stuttgart, Germanyd Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Museum für Naturkunde, Invalidenstraße 43, 10115 Berlin, Germany

a r t i c l e i n f o

Article history:Available online 12 November 2009

Keywords:OntogenyDevelopmentOssification sequence

a b s t r a c t

Ontogenetic series of extinct taxa are extremely rare and when preserved often incomplete and difficultto interpret. However, the fossil record of amphibians includes a number of well-preserved ontogeneticsequences for temnospondyl and lepospondyl taxa, which have provided valuable information about thedevelopment of these extinct groups. Here we summarize the current knowledge on fossil ontogenies ofamphibians, their potential and limitations for relationship assessments, and discuss the insights theyhave provided for our understanding of the anatomy, life history, and ecology of extinct amphibians.

PaleozoicLepospondyls

© 2009 Elsevier Ltd. All rights reserved.

TemnospondylsTetrapods

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4242. Why are fossil ontogenies more common in amphibians than amniotes? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4253. Ontogenies in Paleozoic amphibian taxa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426

3.1. Ontogenies in the temnospondyl fossil record. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4263.1.1. Skull development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4263.1.2. Postcranial development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4263.1.3. Bone histology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427

3.2. Ontogenies in the lepospondyl fossil record . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4283.2.1. Aïstopods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4283.2.2. Nectrideans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4283.2.3. Microsaurs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 428

4. Mesozoic and Cenozoic fossil amphibians . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4294.1. Stereospondyls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4294.2. Fossil crown-group representatives. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 429

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 429

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 429

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 430. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 430

they represent only a minute fraction of the amphibian diver-

5. Metamorphosis and developmental trajectories . . . . . . . . . . . . . . . . . . . . . .6. Discussion and conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction

Athough the three groups of modern amphibians, frogs, sala-manders, and caecilians, are of great importance for modernecosystems and have evolved many different modes of life,

∗ Corresponding author. Tel.: +1 773 834 4774; fax: +1 773 834 8901.E-mail address: nfrobisch@uchicago.edu (N.B. Fröbisch).

sity that was present in Earth’s history. In the past 365 millionyears since the emergence of the first tetrapods, ‘amphibians’have displayed an impressive diversity in terms of morphology,size, and ecology and dominated many Paleozoic and Mesozoicecosystems.

Amphibians are a paraphyletic group of tetrapods, which ple-siomorphically depend on water for the deposition of their eggsand the development of their larvae (Fig. 1). They are divided into

1084-9521/$ – see front matter © 2009 Elsevier Ltd. All rights reserved.doi:10.1016/j.semcdb.2009.11.001

N.B. Fröbisch et al. / Seminars in Cell & Developmental Biology 21 (2010) 424–431 425

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ig. 1. Phylogeny depicting the current hypothesis of lower tetrapod relationshipollowing Laurin and Reisz [1]. Temnospondyl relationships following Witzmann et

odern amphibian groups are indicated by symbols of respective modern taxa.

wo major groups, Temnospondyli and Lepospondyli, in additiono a grade of basal forms. In our current understanding of tetra-od relationships, amniotes are considered more closely relatedo Lepospondyli than to the very diverse group of temnospondylmphibians [1,2]. A controversy surrounds the origins and rela-ionships of modern amphibians and it remains unsettled whetherrogs, salamanders, and caecilians form a monophyletic group,s supported by molecular studies, and whether they fall withinemnospondyls or lepospondyls [1,3–8]. However, recent evidenceupports the hypothesis that at least frogs and salamanders areerived from dissorophoids, a clade of small or miniaturized taxaithin temnospondyls with shortened skulls and enlarged orbits

6,9].Ontogenetic data are extremely rare in the fossil record

nd fossil developmental sequences are inherently incompletend/or difficult to interpret. The vast majority of fossil onto-enetic sequences are known for temnospondyl taxa, includingasal forms such as the edopoid Cochleosaurus, as well as a

arge number of derived taxa (dissorophoids, eryopoids) [10].ecause ontogenies are particularly well preserved for certainissorophoid taxa, ontogenetic data have also been drawn uponor comparison with extant amphibians and in the discussionf lissamphibians origins [4,11–18]. However, beyond being andditional source of data in the framework of this controversy,ntogenies of fossil amphibians have provided a wealth of infor-ation on the biology of these organisms that the study of

dults alone could not have provided. This includes insights intoariant developmental trajectories and the evolutionary mecha-

isms acting on them [16,19–21], the evolution of metamorphosisnd life history pathways [22–26], as well as insights into thetilization of different habitats at various ontogenetic stagesnd food web interactions between different amphibian taxa27–29].

ospondyl relationships and the relationships of anamniotes to amniote tetrapods0]. Fossil clades that have been suggested to be closely related to some or all of the

2. Why are fossil ontogenies more common in amphibiansthan amniotes?

Most Paleozoic and early Mesozoic amphibians are knownfrom deposits (lagerstätten) that formed under aquatic conditions:channel-fills of creeks and rivers, floodplains of larger streams,ponds and lakes, brackish marshes, and even shallow marineregions [30]. Often these taxa are preserved in their original envi-ronments. Some outstanding examples are the pond and lakedeposits of the Variscan orogen, a large mountain range coveringEurope in the Carboniferous and Permian. These lacustrine depositsformed under stagnating conditions and were subject to few exter-nal influences. In the deeper regions of these lakes, bituminousmudstones formed which often preserved complete skeletons ofamphibians in exquisite detail: in addition to the bones, the skin,external gills, eye pigments, and sometimes even color patternsof the skin are still present in some form. In such deposits, lar-vae of various sizes are frequently preserved together with adultsof the same species, sometimes the smallest larvae outnumberingeverything else [29]. These lagerstätten have produced hundredsor thousands of specimens of branchiosaurids [31,32], and recentefforts have further focused on various size classes of other taxa[20–22,33–35]. Ideally, samples used as the basis for a reconstruc-tion of the ontogeny of a species should be derived from a singlelocality and horizon, to rule out both microevolutionary changesand geographic differences within the extinct species.

In the Paleozoic, amniotes were usually preserved under dif-ferent conditions because they inhabited dry, often upland areas

and their skeletons were only rarely washed into the larger lakeswhere preservation was more favourable. This also holds true formany lepospondyl taxa, which were often small and terrestrial ascompared to many temnospondyl taxa. Those lepospondyl taxa forwhich fairly good growth series are known (see Section 3.2) were at

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east semi-aquatic and are found in lacustrine, anoxic deposits. Eggsnd small juveniles of amniotes (and terrestrial lepospondyls) areery rare, because the often coarse-grained sediments containingmniote skeletons did not permit the preservation of tiny juvenilesr eggs with embryos. The main reason for the different preser-ation of ontogenies in amphibians and amniotes and terrestrialepospondyls is therefore a strong taphonomic bias.

. Ontogenies in Paleozoic amphibian taxa

.1. Ontogenies in the temnospondyl fossil record

Ontogenetic data in the form of ossification sequences arenown for a number of taxa with different sizes, ecologies, andevelopmental trajectories. Development of the skull and postcra-ium has been described and discussed in detail in a series of papers

or Sclerocephalus [33,34,36], Cheliderpeton [37,38], Archegosaurus35], the eryopid Onchiodon [39,40], zatracheids [21,41] and dis-orophoids, in particular micromelerpetontids, branchiosaurids,nd amphibamids [14,19,20,26,31,32,42–45].

.1.1. Skull developmentThe development of the skull has attracted some major atten-

ion in the last three decades, after the pioneering studies of Jürgenoy on branchiosaurid and eryopoid temnospondyls [33,39,42,43].

n large samples of branchiosaurids, Boy [43] recognized that suc-essively larger specimens contained increasing numbers of bonesn their skulls and identified several phases of skull formation.xamination of a larger body of material from one locality and hori-on served to reconstruct the cranial development in two closelyelated branchiosaurids in more detail [31]. This revealed that ateast in this group, bone formation proceeded along a rather uni-orm path (trajectory), with marginal jaw bones, palate elements,

edial skull roof bones, cheek elements, and circumorbital bonessurrounding the eye) forming in successive phases, complementedy associated changes in the axial and limb skeletons. The early for-ation of jaw and palate bones coincided with the appearance of

arval teeth on these elements, suggesting that feeding had alreadyommenced in these small larvae. This parallels the ontogeny ofodern salamanders that have a larval phase, and a comparison

evealed that branchiosaurids and hynobiid salamanders pass(ed)hrough remarkably similar stages of skull formation [16]. Apart

Fig. 2. Development of the bony skull in selected aquatic and terrestrial temnospondy

opmental Biology 21 (2010) 424–431

from the necessities of early feeding, developmental constraintsare more likely to account for these large-scale similarities thanrelationship [17], although branchiosaurids form part of the group(Dissorophoidea) that probably gave rise to salamanders and frogs[9,46]. In other temnospondyls, cranial development is not pre-served in as much detail as in branchiosaurids. It is also evidentthat the skull was completed much faster in these other taxa, withsmall larvae resembling adults more closely than did the larvae ofbranchiosaurids [20,34].

Cranial development has also been studied in larger taxa(e.g., Onchiodon, Sclerocephalus, Archegosaurus, Watsonisuchus, Ben-thosuchus), which were more similar to giant salamanders orcrocodiles and reached sizes between 1 and 2 m [33,35,39,40,47,48](Fig. 2). In these, the smallest known larvae already had relativelycomplete dermal skulls but short snouts, large orbits, and simplesutures. The braincase and hyobranchial skeleton formed long afterthe completion of the dermal bones, and ornament changed fromsimple pits into polygonal ridges [33].

3.1.2. Postcranial developmentGenerally, the postcranial elements of temnospondyls show

a predominantly anterior to posterior sequence in ossification,reflecting the anterior to posterior direction of the expression ofHox genes [see e.g. 49] (Fig. 3). In most taxa, there is a stark contrastbetween the slow ossification and differentiation of the postcra-nial skeleton and the early formation of the skull where all dermalbones are already formed and sutured in the smallest known larvae.The limb elements, especially the humerus, in larvae of eryopidsand basal stereospondylomorphs [sensu 10], are short, undiffer-entiated, and extremely poorly ossified and further differentiationand ossification proceeded very slowly. In larval and juvenile zatra-cheids, postcrania are also poorly ossified as compared to thedermal skull, but show fast development and early differentiationof the more robust limbs [21]. In contrast, the limbs of dissorophoidlarvae are relatively much longer, more slender, and better ossified.Unique to branchiosaurids is the delayed formation of the dermalskull, whereas the development of the postcranium and in par-

ticular that of the girdles and limbs, is much faster than in othertemnospondyls for which growth series are known [16,19,31]. Out-group comparison with the finned sarcopterygian Eusthenopteron[50] and with discosauriscid seymouriamorphs [51] shows that theslow development of the postcranium with respect to the early for-

l taxa which preserve ontogenetic series. Relative skull size of taxa not to scale.

N.B. Fröbisch et al. / Seminars in Cell & Deve

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ig. 3. Development of the postcranial skeleton in temnospondyls frommall aquatic larva/juvenile to semi-terrestrial/terrestrial adult, exemplified byrchegosaurus.

ation of the dermal skull as seen in the majority of temnospondylsan be regarded as plesiomorphic for tetrapods.

The first elements to ossify in the vertebral column are the neu-al arches, which develop from laterally paired anlagen seen inmall larvae with their ossification starting in the anterior trunkegion. Ossification further proceeds posteriorly in the trunk andontinues in the tail (Fig. 3). The anterior to posterior ossificationf the tail skeleton is delayed, which is readily visible in speci-ens with the outline of the caudal fin preserved. Therefore, the

ostsacral column consists mainly of cartilage for a long period inntogeny (Fig. 3). The multipartite vertebral centra begin to ossifyistinctly later than the arches, whereby the intercentra develop as

aterally paired elements that fuse subsequently at the midline.The ribs begin ossification in the anterior part of the trunk and

ater than the respective neural arches, but as in the latter, ossifi-ation proceeds in an anterior to posterior direction. In adults ofedium- to large-growing forms, the ‘thoracic’ ribs are propor-

ionally long and curved and bear hook- or blade like uncinaterocesses.

In the pectoral girdle, formation of the dermal elements (inter-lavicle, clavicles, and cleithra) already takes place in small larvaefter the initial ossification of the humerus and the anterior arches

lopmental Biology 21 (2010) 424–431 427

and ribs. In contrast, ossification of the endochondral scapulocora-coid begins distinctly later as a single element of ill-defined outline.An exception to this pattern is seen in branchiosaurids, in which abony scapulocoracoid can be determined prior to the interclavicle.In all taxa, full ossification of the scapulocoracoid does not occurbefore the adult stage and a large amount of cartilage persists espe-cially in the coracoid portion of the adults of primarily aquatic taxalike Archegosaurus.

In the pelvic girdle, a bony ilium is already visible in small larvae;its further differentiation is faster in taxa with terrestrial ratherthan aquatic adults. The ischium starts to ossify later and is a pairedelement that fuses subsequently, while the pubis is the last elementof the pelvic girdle to ossify. In many rather aquatic forms, the iliumand ischium do not co-ossify, and the pubis remains completelycartilaginous.

Ossification of the limbs commences with the humerus, priorto the formation of the pectoral girdle and the femur. Gener-ally, limb ossification proceeds in a proximodistal direction withthe exception of the mesopodial elements, which ossify latest inontogeny or remain cartilaginous even in the largest known spec-imens (Fig. 3). The specific order of ossification in the limbs, inparticular in the autopodial regions, is usually only incompletelyresolved. However, based on exceptionally well-preserved mate-rial of the branchiosaurid genus Apateon much of the ossificationsequence in the limbs of this taxon was resolved [14]. This revealeda general preaxial to postaxial direction of ossification, a patternpreviously exclusively known from modern urodeles that is in con-trast to the conservative postaxial to preaxial direction of digitdifferentiation in all other tetrapods.

3.1.3. Bone histologyIn addition to morphological investigations of fossil growth

series, long bone histology and skeletochronology have become apowerful tool to infer biological parameters like growth rate, indi-vidual age, and mode of life of extinct tetrapods, although it hasthus far primarily been applied to fossil amniotes [52]. In recentyears, several authors have begun to apply skeletochronologicalstudies also to long bones of early non-amniotic tetrapods [53–56].In poikilothermic animals, information about life history can begathered from the pattern of skeletal growth marks, i.e., the zones(periods of high growth rate), annuli (periods of slowed growth),and LAGs (lines of arrested growth, which indicate a temporarycessation of growth). The long bones (mostly femora) investigatedin extinct amphibians show a cyclical growth pattern in the formof regularly alternating growth marks. The individual age of eachinvestigated specimen can be estimated by counting the numberof LAGs.

Sanchez et al. [54] showed by histological investigation of thefemora in a growth series of the seymouriamorph Discosauriscusthat this basal tetrapod has a developmental trajectory similar toextant salamanders. After an extended larval period with slow bonegrowth, sexual maturity was not reached before nine to 10 years.In branchiosaurids, Sanchez et al. [55] were able to histologicallydemonstrate a paedomorphic condition in the long bones by thepersistence of calcified cartilage and of the Kastschenko line, theboundary between the innermost layer of periosteal bone and theendosteal bone.

Apart from these ontogenetic inferences, long bone histologyalso reveals paleoecological data. The occurrence of zones, annuli,and LAGs can be interpreted in many cases as resulting from

palaeoenvironmental influences on bone deposition in an annualperiodicity. They thus indicate a seasonal climate in the habitat theanimals lived in. Skeletochronology has just started to be appliedfor temnospondyls and other basal tetrapods, and much additionaldata on the ontogenies of these extinct animals can be expected.

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.2. Ontogenies in the lepospondyl fossil record

Although there is renewed interest in determining the relation-hips among lepospondyls and other tetrapod groups, only scantbservations exist about lepospondyl development and much ofhis information comes in the form of short notes accompany-ng more broadly focused work [57 Nectridea,58,59 Microsauria,60ysorophia]. The few detailed studies of juvenile lepospondyls haveo far included only the aïstopods Phlegethontia [61–63] and Oesto-ephalus [64], the microsaurs Utaherpeton [65] and Microbrachis66,67], and the nectridean Diplocaulus [68–70]. Even fewer stud-es directly report ossification sequences, which currently consist ofata on the cranial development of Phlegethontia [61] and prelim-

nary information on the postcranial development of Microbrachisnd Hyloplesion [71]. There is little information available aboutysorophoid ontogeny, a group once considered part of Microsauria,nd nothing is known about development in acherontiscids or ade-ogyrinids.

Based on our limited knowledge of lepospondyl development,embers of the group are generally characterized as direct devel-

pers, a pattern of growth shared with early amniotes [72]. Thisharacterization is probably correct because the lepospondyl taxahat have been studied exhibit rapid ossification of the skeleton,specially early formation of the vertebrae at small size, when com-ared to more gradually growing temnospondyls [73]. Vertebraere completely ossified even in the smallest individuals known andrches and centra ossify simultaneously [63,72]. Vertebral ossi-cation likely occurs directly from the perichordal tube, similaro vertebral development in many modern tetrapods and teleosts72]. However, there seems to be a certain degree of variation inhe pattern of formation of vertebral elements between differentepospondyl taxa; microsaurs and lysorphians ossify their neuralrches and centra separately and these elements originate fromndochondral bone, while nectrideans and aïstopods ossify thems a single unit, which is likely of perichondral origin (A.R. Milner,ersonal communication).

Early ossification of the skeleton, particularly of the postcra-ium, is a developmental pattern common to not only aïstopods,ectrideans, and microsaurs, but also plethodontid salamandersnd other tiny, living tetrapods. As a result of his work on the minia-urized salamander Thorius, Hanken [74] suggested that adult sizean be regulated through the termination of growth at any size viaarly onset of ossification. Therefore, it is likely that precocial ossi-cation in lepospondyls is intimately tied to the small size of thesenimals relative to temnospondyls.

.2.1. AïstopodsCurrently, the only cranial ossification sequence known for any

epospondyl is that of the aïstopod Phlegethontia [61–63]. A growtheries of eight individuals demonstrates that ossification of theermal skull elements is delayed relative to endochondral bone61], a situation that differs from most temnospondyls and livingetrapods. The smallest specimen examined possesses completelyssified vertebrae and an ossified posterior braincase, although thenterior portion of the braincase is not fully formed [61]. Amonghe dermal elements, the smallest individual exhibits an ossifiedrontal, prefrontal, maxilla, complete lower jaw, and partial pala-oquadrate. Anderson [61] suggested that the evolutionary trendoward reduction of the dermal portions of the skull within theïstopoda mirrors the lag between the endochrondal and dermalssification observed in the skull of Phlegethontia and is poten-

ially tied to miniaturization in the group. Moreover, as in anurans,he rear of the braincase serves as an anchor point for the epaxial

usculature in aïstopods and therefore may provide a functionalonstraint for the early ossification of the braincase (J.D. Anderson,ersonal communication). Supplementing developmental data for

opmental Biology 21 (2010) 424–431

Phlegethontia, some information exists on growth in Oestocephalus.For example, during development in the latter, the jaw suspenso-rium is reported to shift posteriorly to end up behind the skull table[73], possibly signifying a change in diet between juveniles andadults. In this same taxon, the caudal vertebrae ossify from ante-rior to posterior [64] and the formation of the dorsal osteodermsproceeds from posterior to anterior, similar to scale developmentin living caecilians [73].

3.2.2. NectrideansExtensive growth series of nectrideans are known only for Batra-

chiderpeton and Diplocaulus. Therefore, knowledge of nectrideandevelopment is limited and what does exist comes mainly fromstudies of growth in Diplocaulus. In general, even juvenile nec-trideans tend have well ossified skeletons and smaller specimensonly lack ossified carpals and tarsals [68,73].

One of the only lepospondyl taxa that has been the focus ofdetailed, large-scale allometric studies is Diplocaulus magnicornis.In one study of cranial growth, Olson [69] showed that whereasmuch of the anterior portion of the skull grows isometrically, moreposterior areas, and especially the characteristic tabular horns,experience strong, positive allometric growth, probably in asso-ciation with a locomotory shift between juvenile and adult stages.Additionally, Rinehart and Lucas [70] found evidence for an “onto-genetic saltation” or modified metamorphosis in Diplocaulus thatwould have occurred around a skull length of 40 mm. They sug-gested that the juvenile or “short skull” stage in Diplocaulus wasequivalent to the adult form of more primitive taxa (peramorpho-sis) like Keraterpeton, Batrachiderpeton, and Diceratosaurus [70].

3.2.3. MicrosaursMicrosaurs have recently become the renewed focus of detailed

analyses because of their controversial association with both earlyamniotes and living caecilians. However, despite the large diversityof microsaur taxa in the fossil record (30+ genera) and the existenceof a number of growth series (i.e., Microbrachis and Hyloplesion)there is a lack of basic information about microsaur ontogeny andonly a handful of studies on microsaurs focus solely on develop-ment.

One such study was centered on Utaherpeton, and althoughsample size was low, it contributed valuable data on vertebraldevelopment in lepospondyls [65] as it is the only lepospondylto exhibit evidence of vertebrae developing from multiple parts.Moreover, the unambiguous presence of haemal arches in boththe juvenile and adult of Utaherpeton provided one of the firstuncontested points of evidence that the holospondylous centrumof lepospondyls is the pleurocentrum and not the intercentrum.

Recently, Microbrachis was the focus of a study on tail growthin microsaurs [66], which demonstrated that the tail of Micro-brachis increases in relative length during ontogeny. Milner [66]suggested that the terminal caudal vertebrae were slow to ossifyand that examples identified as tail regeneration in this taxon [59]were actually individuals with incompletely formed distal caudalsadded during lengthening. The large number and size range of avail-able Microbrachis specimens have also allowed for detailed study ofcranial growth [67]. Whereas Zanon [67] did not extend his obser-vations to functional explanations, Carroll [73] noted that duringgrowth in the related taxon Hyloplesion, the cheek region expandsposteriorly, similar to changes in some temnospondyls, which wasinterpreted as a gradual change in diet from smaller to larger prey[73].

A follow up to these studies, focused on postcranial allome-try and ossification sequence in Hyloplesion and Microbrachis, iscurrently underway by one of us (JCO). Preliminary data suggeststhat limb and girdle development in these microsaurs was gener-ally similar to that of temnospondyls, except for a small number

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f heterochronic shifts probably related to specialized locomotion71].

. Mesozoic and Cenozoic fossil amphibians

.1. Stereospondyls

The stereospondyls form a clade of temnospondyls that survivedhe Permo-Triassic extinction event and reached global distributionuring the Triassic. Stereospondyls were the major top predatorsf early Mesozoic ecosystems, with the bulk of taxa reaching 2–4 mength and some exceeding this (e.g. 5–6 m long Mastodonsaurus).n most stereospondyls, only adults are known, but there are aew taxa in which juveniles and larvae are preserved, showinghat these crocodile-like amphibians underwent remarkably slowevelopment with only minor proportional changes in the skullnd limb skeleton. Because most taxa were aquatic as adults, theyrobably remained in the same habitat throughout their lives [25].

.2. Fossil crown-group representatives

The first crown-group salamanders are known from the Mid-le Jurassic of China. Several taxa, including the cryptobranchidhunerpeton, are known from a large number of exquisitely pre-erved specimens ranging from small larvae to well-developeddults. Both developmental pathways known in modern salaman-ers, neoteny and metamorphosis, have been identified in these

urassic taxa [75,76].The earliest crown-group frog, Prosalirus bitis, is known from the

arly Jurassic [77,78]. Although all early crown-group represen-atives show distinct anuran characteristics and can for the mostart be assigned to one of the modern groups, they are usuallynown from isolated elements or a few partially articulated spec-mens. The Lower Cretaceous deposits in the Shomron region ofsrael produced the first ontogenetic series of the pipid frog Shom-onella jordanica, with distinct tadpole larvae and the typical anuranetamorphosis into froglets well documented in the assemblage

79,80].In contrast to salamanders and frogs, for which informative fos-

ils are known from at least some sites of Jurassic and Cretaceousge, the fossil record of caecilians is extremely scarce. The earliestaecilian, Eocaecilia micropoda, which still possesses legs, is knownrom a number of complete skulls, jaw fragments and postcranial

aterial of postmetamorphic individuals [77,81]. Apart from Eocae-ilia, only isolated elements, and no fossil ontogeny, are known.

. Metamorphosis and developmental trajectories

Like many modern salamanders, Paleozoic and Triassic tem-ospondyls probably hatched from eggs laid in the water andassed through a carnivorous larval period. Relatively few taxahanged to a terrestrial existence as adults; the bulk of known taxaemained in the water or around the water–land interface [25].

Paleozoic amphibians did not undergo a drastic metamorphosiss modern amphibians do, but passed through slow, incrementalhanges instead [43]. Later this hypothesis was confirmed and aet of changes was identified that were shared by many of theseaxa: dermal ornament (from radial pitting to polygonal ridges)nd the reorganization of the hyobranchial apparatus [82,83]. Theatter involves the resorption of the ‘larval’ branchial denticles and

emodelling of the branchial arches, indicating the closure of gilllits (end of aquatic feeding period by suction feeding) and loss ofxternal gills.

A broader examination of temnospondyl ontogenies revealedhat profound morphological transformation was rare and confined

lopmental Biology 21 (2010) 424–431 429

to a few clades which had amphibious or terrestrial adults, such aseryopids, zatracheids, and dissorophoids [21,24]. Most other taxahad ontogenies similar to that of Sclerocephalus, which remained inthe water and preyed on bony fishes, as indicated by intestinal con-tents [33]. Recently, the study of ontogenetic trajectories revealedthe structure of temnospondyl ontogenies: most trajectories wereflat with few changes (ossification of new bones, morphologicalchanges) added gradually [25,26]. In branchiosaurids, the trajec-tory was greatly modified: whereas most species were neotenicwith a stagnating trajectory [22], at least one species was capableof transforming quickly, giving way to a terrestrial adult. This is thefirst example of a drastic metamorphosis similar to that of modernfrogs and many salamanders [26] (Fig. 4).

Lepospondyls also appear to have had relatively flat, grad-ual ontogenetic trajectories. Allometric changes in the skull andpostcranium did occur, which signify shifts in diet in some cases,but lepospondyls do not appear to have undergone a dramatic con-centration of developmental events, nor large changes in habitatduring ontogeny. Only one lepospondyl, the microsaur Micro-brachis, is known to possess branchial plates (denticles), althougha few other microsaurs and nectrideans, in addition to Micro-brachis, have lateral lines. In Microbrachis the lateral lines arepresent throughout ontogeny and even very large individualsretain branchial plates, suggesting that this taxon may have beenneotenic, but non-metamorphosing [59,84].

6. Discussion and conclusions

With the relative wealth of ontogenetic data available for fossilamphibians, a comparison with the ontogenies of modern taxa isan obvious step to further the discussion of amphibian evolution,especially given the controversial origins of modern amphibiansfrom the diverse Paleozoic groups.

Although metamorphosis from an aquatic larva into a ter-restrial adult is a characteristic, and in some forms dramatic,feature of amphibian development, until recently only very lit-tle was known about the evolution of metamorphosis and whenand how the complex changes and intricate timing associatedwith the metamorphosis of modern amphibians may have evolved.Now we know that most Paleozoic taxa for which ontogenies areknown did not show a condensed metamorphosis as seen in themodern forms and that branchiosaurids are thus far the only Pale-ozoic group in which it could be demonstrated [25,26]. Moreover,despite the fact that modern amphibians share certain patternsof morphological change and show a similar hormonal control ofmetamorphosis [85,86], it remains unclear whether a modern pat-tern of metamorphosis was inherited from a common ancestorand was subsequently modified during the separate evolutionaryhistory of the three extant clades or if it evolved convergently.Generally, homoplasy is prominent in many aspects of amphibianmorphology and development and can be difficult to differentiatefrom true synapomorphies in discussions of amphibian evolution[87,88].

Fossil ontogenies, in particular ossification sequences of bran-chiosaurids, which have been suggested to be close relatives tosome or all of the modern groups (see Section 1), have been com-pared to modern amphibians. A number of similarities have beenrecognized in the timing and sequence of events associated withthe development of the bony skull [16,18] and the limb skeleton[14,44] of branchiosaurids and salamanders, such as the general

order of ossification of dermal skull bones and preaxial dominancein the sequence of ossification of the limb skeleton. These findingsprovide valuable insights about the evolution of amphibian devel-opment through deep time and potential support for their closerelationships with batrachians (salamanders + frogs) and possibly

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aecilians. However, the discussion of these shared similarities inphylogenetic context have revealed that it is often problematic

o assess character polarity and pinpoint their evolutionary originsue to analytical problems and the exceptionality of the ontoge-etic dataset available for branchiosaurids [13,14,17,44,63,89].

Apart from the role fossil ontogenies play in the discussion of theontroversial lissamphibian relationships, the relative abundancef data on the ontogeny of temnospondyls provides importantnsights into the biology of this extremely diverse fossil clade and

much broader perspective of their ecology and evolution thandults alone could provide. Due to a preservational bias only veryimited data are available on the ontogeny of lepospondyls [63]nd new research offers much needed insights into the develop-ental patterns in this clade [71]. Furthermore, new methods to

nalyze various aspects of ontogenetic data have been proposedn recent years [90]. The application of these modern methods toossil datasets or combined datasets that include fossil and extantaxa provide new tools [13,14,17,91], which will certainly furtherur understanding of fossil ontogenies and the use of ontogeneticata for phylogenetic assessment.

cknowledgments

Much of the research summarized in this review paper has ben-fited greatly from many fruitful and constructive discussions withur colleagues and we would like to thank J. S. Anderson, J. R. Bolt,. A. Boy, R. L. Carroll, H. C. Maddin, A. R. Milner, N. H. Shubin, and T.irgurdsen. We thank J.S. Anderson, A. R. Milner, and an anonymouseviewer for their constructive comments, as well as M. Sánchezor his helpful suggestions as editor. Funding for this project wasrovided by a Research Fellowship of the Deutsche Forschungsge-einschaft (DFG) to NBF.

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