a reevaluation of the early history of the frogs. part i

A Reevaluation of the Early Historyof the Frogs. Part I

MAX K. HEGHT

SOME of the results of a symposium,Problems in salientian phytogeny,

were published in this journal in 1957. Ofthe three papers published, two (Bratt-strom, 1957; Jameson, 1957) were essen-tially reviews of the literature. One articleby Orton (1957) reviewed her interestingideas on the utilization of tadpole mor-phology in the problem of frog phylogeny.From the viewpoint of paleontology, themost important paper in the symposiumis that by Brattstrom which summarizesall the classic phylogenetic concepts foundin most accepted texts (Romer, 1945; Col-bert, 1955; Piveteau, 1955). In considera-tion of our admitted lack of knowledge(Brattstrom, 1957; Laurent, 1948) on suchbasic facts as the anatomy of living frogsand the incomplete fossil record, the phy-logenetic tree presented by Brattstrom ismisleading because it hides the gaps inour knowledge.

The purpose of this paper is to pointout recent discoveries in salientian paleon-tology and to evaluate the contributionsof these discoveries to the problems ofclassification, phylogeny, and zoogeogra-phy in this group.

Protobatrachus and the Origin of theFrogs

Morphologically the Salientia are amongthe most distinct Tetrapoda. They arecharacterized by their saltatorial means oflocomotion and associated adaptationswhich enable them to exploit this majorchange in the biomechanics of tetrapodlocomotion. The first true frogs appear inthe Jurassic already bearing the majorcharacteristics of the group. Many work-ers have been impressed by the time gapbetween the supposedly ancestral lower

Triassic Protobatrachus and the earliestJurassic frogs. It is for this reason that Idecided to reconsider the status of Pro-tobatrachus and reexamine the type atthe Museum of Natural History in Paris,1

If Protobatrachus is considered an actualsalientian (Piveteau, 1937; Watson, 1941;Romer, 1945; Colbert, 1955; Eaton, 1959),then this time gap between the experi-mental ancestral type and the biomechani-cally perfected descendant type becomesmore impressive when compared with theevolution of similar new adaptationaltypes in other groups. If we assume thatthe evolution of the frogs may have beensimilar to other groups, then one mightexpect that the initial and intermediatephases of the evolution of major newadaptations were passed through quiterapidly.

Since Piveteau's complete study in 1937,many workers have tacitly accepted Pive-teau's conclusion that the lower TriassicProtobatrachus is an intermediate formbetween frogs and the primitive amphib-ians. Protobatrachus is, indeed, some-times regarded as having the same signifi-cance for the origin of frogs as Archaeop-teryx has for the origin of birds.

Watson (1941) went far beyond Pive-teau and created a complete phylogeneticline for the frogs including preprotobatra-choid stages in the form of Amphibamus

1 The author wishes to acknowledge the aidof the National Science Foundation (N.S.F.Research Grant G 7467) and the AmericanPhilosophical Society which made this studypossible. The author also wishes to thankProf. J. P. Lehman for permission to examineProtobatrachus and for the use of the facili-ties of his institution; Dr. I. Griffiths for hisstimulating discussion and criticism; and Dr.D. Marien for his criticism of the final manu-script.

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40 SYSTEMATIC ZOOLOGY

andMiobatrachus (the Eoanura of Romer,1945). Gregory (1950) has criticized theseconclusions and in effect removed Mio-batrachus and Amphibamus from the an-cestral stock of frogs, although Bratt-strom (1957) ignored this and includedthem in the trunk of his phylogeny. SinceWatson's Origin of the frogs only Griffiths(1956) has discussed the relationships ofProtobatrachus. He considered it a larvalform or metamorphosing tadpole.

Before the significance of Protobatra-chus can be understood, the preservationof the specimen must be considered. It isnot a true fossil in the sense that here ispreserved the actual remains of an am-phibian. It is a nodule which, split open,reveals the dorsal and ventral impressionof the skeleton of an amphibian. The con-tact between bone and matrix is alwayssmooth whereas the interface betweencartilage and matrix is rough. It is pos-sible to determine the degree of ossifica-tion because the differences between thetwo types of contacts are clear.

Protobatrachus was considered by Pive-teau as a form basal to and actually be-longing to the ancestral group of theSalientia. His conclusion was based onthe following assemblage of characteris-tics:

1. the presence of a frontoparietal bone,2. the presence of a sphenethmoid and

a posterior cartilaginous area,3. the nerve foramina in the ethmoidal

region and eye muscle scars resem-bling those of Rana or other frogs,

4. the lack of a parietal or pineal fora-men,

5. the large orbit and the reduction ofthe bones of the circumorbital region,

6. the presence of a frog-like pterygoid,7. the presence of a frog-like parasphe-

noid,8. the presence of a shortened vertebral

column,9. the presence of a frog-like pectoral

girdle,

10. the presence of an ilium with ante-riorly projecting blade for attach-ment to the sacrum,

11. the presence of a short tail,12. the presence of the typically en-

larged tarsal bones indicating thefrog-like tibiale and fibulare (as-tragalus and calcaneus of olderauthors).

A reexamination of Protobatrachus byDr. I. Griffiths and myself has revealedcertain features not discussed or describedby Piveteau or Watson. They are:

1. The presence of an imprint of thelower jaw is revealed in the ventral sec-tion of the type. This is easily seen inthe photographs (Piveteau, 1937) and wasindependently discovered and pointed outto me by Drs. H. Pusey and I. Griffiths.The jaw impression clearly indicates aweakly developed thin structure and thepresence of what is probably a dorsallyopen Meckelian groove filled with carti-lage. If this interpretation is correct,there may be a distinct resemblance be-tween this imprint and the lower jaws offrogs. It is impossible to say if teeth wereabsent or present.

2. Piveteau (1937) recorded the pres-ence of three caudal vertebrae. There areclear impressions of at least six vertebraewhich decrease in size posteriorly, al-though the last three are more obscurethan the first three. The scattering ofthese elements could indicate that theremay have been other vertebrae but thesewere separated in the preservation of thefossil. This last statement is not an ob-servation but my interpretation.

3. The frontoparietal as depicted byPiveteau has a longitudinal suture alongits entire midlength. Watson (1941) con-sidered it a fused structure and indicatesno such suture. In the type, there is,along the midline of the posterior half ofthe frontoparietal imprint, a faint lineamid the impression of the dermal orna-mentation. It may or may not representthe posterior portion of a suture. Further-more both Piveteau and Watson illustrate

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HISTORY OF THE FROGS 41

the posterior portion of the frontoparietalas being slightly narrower than is actu-ally the case in the fossil. Actually, thelateral wings of the frontoparietal lie be-hind and exterior to the otic region, acondition certainly not characteristic offrogs. The imprint of the dorsal surfaceof the frontoparietal has marked rugosi-ties which have been interpreted as der-mal ossifications, such as occur in pelo-batid frogs. Within this pattern, lying inthe midline slightly posterior to the half-way point between the anterior and pos-terior borders of the frontoparietal, is aclearly demarked ovoid area. The natureof the ridges surrounding this area sug-gest that there was a depression, perhapscovered by some thin tissue. This struc-ture lies not exactly in the median longi-tudinal axis but slightly to the right. Ifthis should represent the parietal foramen,it would be a structure not characteristicof most adult modern frogs, although it isknown in adult Xenopus.

4. In the reconstruction by Piveteau(1937) there are indicated clear suturelines which he interprets as the contactsbetween the frontoparietal and the pre-frontal. Lying anterior and medial tothem is a depression with a rugose sur-face on the contact face. This rugosesurface could be interpreted as a contactbetween cartilage and matrix. If this sur-face is a natural surface contact betweenskeleton and matrix, then the identifica-tion of Piveteau and Watson of the der-mal nasal bone can be questioned.

5. Piveteau (1937, 1955) states that thesphenethmoid has the same relationshipto the nerve foramina as in modern frogs.He describes foramina for the second,third, fourth, and fifth cranial nerves. Onexamination of the type I could not dis-cern these foramina or for that matter dis-tinguish between foramina and whatrepresents cartilage-matrix contacts. Ifone does assume that Protobatrachus issimilar to frogs, then one can find suchsimilarities, but, on the other hand, ifone does not make that assumption, then

the foramina are difficult to find, andhomologies virtually impossible.

6. Piveteau (1937) indicates that theretractor eye muscle insertion scars arepresent on the parasphenoid and that theyare similar to those in Rana. These im-pressions, if present, are faint indeed.They can only be interpreted as such im-pressions if one knows that Protobatra-chus is a frog and that they do exist.

7. The vertebral impressions are wellseparated by large intervertebral piecesof matrix. Some of these pieces of matrix,which have replaced the non-ossified in-tervertebral elements, bear conical an-terior or posterior extensions, perhaps anindication that the notocord was continu-ous or nearly so. These conical projec-tions are clearly present on the ventralsection at the level of the first, second,third, fifth, fifteenth, and sixteenth verte-brae.

8. The pectoral complex is not exactlyas outlined by Piveteau (1937) and is inneed of further study. This entire arearepresents a complex surface and is diffi-cult to outline on a flat surface as illus-trated by Piveteau. On the left side anarea is called the coracoid plate and liesnearer the head of the humerus andagainst the impression of what is thedentary portion of the lower jaw. It isset off at a slightly tilted plane. The im-pression called the scapulocoracoid whichis anterior and interior to the humerus isa complexly surfaced squarish structure.The identification of this structure mustbe revised due to the work of Ritland(1955). Impressions of what may becalled the suprascapula and cleithrummay also be identified. Anterior to thescapulocoracoid of Piveteau is a small barwhich has been called the clavicle. Onthe right side the general region is quitesimilar in plan. The scapulocoracoid areais more or less similar in shape. There isan indication of a clavicular area but noindication of the coracoid plate. The pres-ence of two areas identified as coracoidplate and scapulocoracoid clearly indi-

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cates the need for a reconsideration ofhomologies, and the general complex na-ture of the surfaces causes one to proceedwith caution.

From the above discussion it appearsthat a reevaluation of the significance ofthe characteristics of Protobatrachus isneeded. An analysis of the distinguishingfeatures of the fossil reveals a mixtureof very advanced frog-like characters andsome very primitive amphibian features.Piveteau points out that the palatal com-plex of Protobatrachus is very similar tothat of frogs, although it is not empha-sized that it is just as similar to thepalatal complex of branchiosaurs (Heyler,1957, Pigs. 6, 7, 8). The most character-istic frog-like feature of Protobatrachusis the presence of a frontoparietal, gen-erally regarded as a key character of theSalientia. The question that arises iswhether or not the frontoparietal ofProtobatrachus actually represents thesame structure that is found in frogs.Firstly, the frontoparietal is more exten-sive posteriorly than in living frogs, sug-gesting a more complex structure. If thisis a more complex bone than that of frogs,it perhaps is composed of frontals, parie-tals, postparietals, and perhaps possiblythe tabulars. This can only be determinedby the position in some unknown fossilancestor, perhaps similar to the branchio-saurs (Heyler, 1957, Fig. 4). Secondly,the existence of a large compound bone,the frontoparietal, could be associatedwith the large orbits and the reduction ofthe circumorbital region. The evolutionof a single rigid dorsal element couldmerely be a mechanism to strengthenthe skull and allow for the expansion ofthe orbital region at the expense of thecircumorbital bones. Therefore, the oc-currence of the frontoparietal or fronto-parietal complex, reduction of the cir-cumorbital complex, and the enlargedorbits could well be a single functionalcomplex independently evolved in twodifferent phylogenetic lines of opticallyoriented amphibians.

The presence of a frog-like ilium is thesecond of the key characters which re-late Protobatrachus to the frogs. In frogs,the anteriorly extended ilium for attach-ment of the limb musculature is a majoradaptation for jumping. Associated withthis anterior prolongation of the ilium isthe enlarged and firm attachment of thesacral diapophyses to the sacrum. InProtobatrachus, the sacral diapophysesare not enlarged and are clearly not fusedto the sacrum. In modern frogs there isa clear sliding action between the iliumand the sacral diapophyses (Whiting,1961) but no such movement is function-ally possible between the diapophysis andthe sacrum, but instead complete fusionis found in all living frogs.

Piveteau (1937) has further suggestedthat the early adaptation to jumping wasalready indicated in the tarsus of Proto-batrachus by the presence of enlarged tar-sals. Yet in modern frogs these bonesbelong to the proximal series and not tothe geographic distal series as in Proto-batrachus. (The digits and metatarsalsare not preserved.) In order to identifythese bones as part of the proximal series,Piveteau was forced to interpret theproximal bones as sesamoid bones and toassume that the true distal bones aremissing. Single sesamoid bones are some-times found in frogs, but they usually arenot paired structures nor do they lie be-tween the tibiale and fibulare and the tibiaand fibula. Consequently, in the specimenof Protobatrachus, the two proximal im-pressions are more likely to represent thetrue proximal tarsal elements. If this is so,then there are two possible conclusions.Firstly, if Protobatrachus is an ancestralfrog, this may indicate that the homolo-gies of the enlarged tarsals of frogs is in-correct. Alternatively, if these bones arenot homologous to the enlarged tarsals inthe frog (but do represent elements inthe more distal series), then the simi-larities in the tarsus of Protobatrachusand the modern frogs are the result ofconvergent evolution.

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HISTORY OF THE FROGS 43

The Relationships of Protobatrachus

The analysis of the above discussedcharacters would indicate the followingpossible relationships:

1. Protobatrachus is a representativeof a group intermediate between theprimitive Amphibia and the modernfrogs. As a result it may possiblyrepresent one of the following con-ditions:

a. Protobatrachus is an adult ter-restrial form already showingsaltatorial adaptations.

b. Protobatrachus is an adultaquatic form showing salta-torial preadaptations.

c. Protobatrachus is a tadpole ora metamorphosing tadpole.

2. Protobatrachus is a form whichbears certain key characters of themodern Anura, but these have beenindependently evolved and are notindicative of relationships to thefrogs.

It is impossible at this time to deter-mine which of the above relationshipsactually represent the true status of Pro-tobatrachus. The second hypothesis, aninterpretation based on convergent re-semblances, is contingent on the interpre-tation of the enlarged tarsals of Proto-batrachus as belonging to the distal rowof tarsals. Hypothesis lc, the interpreta-tion of Protobatrachus as a tadpole, is con-sidered unlikely due to the well-ossifiedcondition of the fossil. Hypothesis la,which is the implied interpretation ofPiveteau, is also considered unlikely be-cause of the lack of rigidity in the verte-bral column and the apparent weaknessbetween the sacral diapophysis and thesacral vertebra. Hypothesis lb, Proto-batrachus as an aquatic form ancestralto the modern frogs, would be acceptableif the method of swimming would be asculling type of movement of the hindlimbs.

Basically the problem of frog ancestry

is a question of whether the adult salien-tian ancestor was an aquatic form pre-adapted for saltation or a terrestrial formutilizing the saltatorial locomotion as aspecialized escape mechanism. Eaton(1959) suggests the latter possibility. Thesaltatorial adaptation of frogs is uniqueamong vertebrates because frogs are oneof the few vertebrates that hurtle theirbodies into space to land in an area beyondtheir range of vision. It therefore seemslikely that this early adaptation was pri-marily an escape mechanism of a riparianorganism which was jumping into an en-vironment, probably the aquatic medium,where it was unnecessary to have in-formation as to the point of landing, be-cause it was a more or less uniform area.In other words, it made little differenceto the frog ancestors where it landed aslong as it left the position it occupiedpreviously.

In conclusion, it can be stated that Pro-tobatrachus is an enigma. The presenceof a frontoparietal and elongated iliumindicate anuran affinity, but these couldbe explained as the result of convergentevolution. The usual interpretation thatProtobatrachus represented a terrestrialsaltatorial form is inconsistent with theevidence of a non-rigid bony vertebralcolumn associated with a weak sacrum.Lastly there remains the unsolved prob-lem of the true homologies of the enlargedtarsals. The identification of these tarsalsis dependent on the discovery of new ma-terial. The classic textbook presentationof Protobatrachus as a form which is with-out doubt an intermediate between mod-ern frogs and the ancestral amphibians isno longer a certainty.

The Jurassic, Cretaceous, and earlyTertiary evolution of the frogs will be dis-cussed in a forthcoming article in thisjournal.

REFERENCESBRATTSTROM, BAYARD H. 1957. The phylogeny

of the Salientia based on skeletal morphol-ogy. Systematic Zool., 6:70-74.

COLBERT, EDWIN E. 1955. Evolution of the

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vertebrates. John Wiley and Sons, NewYork, 479 pp.

EATON, THEODORE H., JR. 1959. The ancestryof modern Amphibia: a review of the evi-dence. Univ. Kansas Publ. Mus. Natur.Hist, 12:155-180.

GRIFFITHS, IVOR. 1956. Status of Protobatrachusmassinoti. Nature, 177:342-343.

GREGORY, JOSEPH T. 1950. Tetrapods of thePennsylvanian nodules from Mazon Greek,Illinois. Amer. Jour. Sci., 248:833-875.

HEYLER, DANIEL. 1957. Revision des Bran-chiosaurus de la region d'Autun. Ann. Pale-ontol., 43:47-111.

JAMESON, DAVID L. 1957. Life history andphylogeny in the salientians. SystematicZool., 6:75-78.

LAURENT, RAYMOND. 1948. L'osteologie desBatraciens dans ses rapports avec la syste-matique. XIII Congres Zool., Paris, RapportSect. Vb: 372-348.

ORTON, GRACE L. 1957. Larval evolution andfrog classification. Systematic Zool. 6:79-86.

PIVETEAU, JEAN. 1937. Un amphibien du Triasinferieur; essai sur Torigine et 1'evolutiondes amphibien anoures. Ann. Pal6ontol., 26:133-177.1955. Traits de Paleontologie, Tome V.Masson et Cie., Paris, 1110 pp.

RITLAND, RICHARD M. 1955. Studies on thepostcranial morphology of Ascaphus truei.I. Skeleton and spinal nerves. Jour. Mor-phol., 97:119-178.

ROMER, ALFRED S. 1945. Vertebrate paleon-tology. Univ. Chicago Press, Chicago, 687 pp.

WATSON, D. M. S. 1941. The origin of the frogs.Trans. Roy. Soc. Edinburgh, 60:195-213.

WHITING, H. P. 1961. Pelvic girdle in amphib-ian locomotion. Symposia Zool. Soc. Lon-don, 5:43-57.

MAX K. HECHT is Research Associate inVertebrate Paleontology in the American Mu-seum of Natural History and Assistant Profes-sor of Biology at Queens College, Flushing67, New York.

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a reevaluation of the early history of the frogs. part i

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