Early evolution and fossil history

The appearance of limbed vertebrates—the stegocephalians

The origin of amphibians and amniotes (reptiles, birds, and mammals) must be sought among stegocephalians (i.e., four-limbed vertebrates with digits), which appeared about 370 million years ago (mya) in the Devonian. The group of bony vertebrates from which tetrapods (the group that includes extant stegocephalians) evolved is known informally as osteichthyans, and includes two groups of vertebrates—the actinopterygians and sarcopterygians. Actinopterygians are ray-finned fishes, the group containing nearly all bony fish that are familiar today. Sarcopterygians, or "lobe-finned" fishes, contains three living groups—coelacanths, lungfishes, and tetrapods. Our closest known relatives that retained paired fins are panderichthyids. The ancestor of panderichthyids and tetrapods lacked the dorsal and anal fins typical of other lobe-finned fishes, and, unlike them, its skull was not divided into anterior and posterior parts by an intracranial joint. In addition, the cranium contained a new dorsal roofing bone, the frontal.

Panderichthyids (Panderichthys and Elpistostege) were large, lobe-finned fishes about 39 in (1 m) long from the Late Devonian of Europe and North America. Unlike its osteolepi-form relatives (e.g., Eusthenopteron), panderichthyids had a massive, flattened head and body, and a long, rather pointed snout with one external narial opening near the margin of the jaw on each side of the skull—a feature they shared with early stegocephalians. Basal ray-finned fishes (e.g., Polypterus and the bowfin Amia), lungfishes, and tetrapods possess lungs as a means of breathing; therefore, it is presumed that all early osteichthyans possessed lungs. In the lineage leading to modern ray-finned fishes, the lung was modified into a swim bladder (an organ of buoyancy), but in the lobe-finned fishes, lungs were retained. The challenge facing the early aquatic ancestor of tetrapods was to develop a mechanism for ventilating the lungs in a terrestrial environment.

The earliest known stegocephalians are moderate-sized animals: Ichthyostega (61 in; 1.5 m long) and Acanthostega (19.7 in; 0.5 m long) from Greenland, and Tulerpeton (ca. 26.4 in; 0.67 m long) from Russia. Based on the remains of other animals associated with these stegocephalians and features of their anatomy, it seems likely that they were aquatic. Acanthostega and Ichthyostega probably lived in freshwater or brackish environments, whereas Tulerpeton inhabited a marine environment. For much of the twentieth century, stegocephalians were thought to have originated in freshwater, but an increasing number of early amphibians have been found in coastal, presumably brackish and saltwater environments. Some classical Permo-Carboniferous (Garnett, Hamilton, and Robinson, Kansas, in the United States) and Devonian (Miguasha, Quebec, Canada) fossiliferous localities that previously were interpreted as freshwater environments, now are known to have been coastal, lagoonal, deltaic, or estuarine environments.

Early stegocephalians had many features associated with an aquatic lifestyle. All retained a lateral-line system, a series of sensory receptors in the skin that sense mechanical disturbances in the water and that are typical of fishes, and larval and aquatic amphibians today. Acanthostega seems to have retained functional internal gills in addition to lungs. Both Acanthostega and Ichthyostega had finned tails resembling that of Panderichthys and probably similarly used to provide propulsive force for swimming. The backbones of these stegocephalians were poorly developed and probably not capable of supporting the weight of the animal on land. Ichthyostega had a substantial rib cage. The overlapping ribs would have provided protection for internal organs, but would not have been sufficiently flexible to facilitate ventilation of the lungs in a terrestrial environment. The limbs were short and stout, and the forelimbs markedly larger than the hind limbs. The limbs seem to have been capable of only a restricted range of movement, and are thought to have been positioned more to the side of the body than beneath it. The hands and feet were paddlelike, having six to eight digits, depending on the species. Thus, it seems likely that in these Devonian vertebrates, the limbs may have been used to walk on a submerged substrate, perhaps in intertidal areas or in obstructed environments such as mangrove swamps. The locomotor system of these animals may be thought of as preadapted for a terrestrial lifestyle. The presence of limbs, digits, pectoral and pelvic girdles, and a rib cage that were useful in aquatic habitats provided the morphological features that their descendants could elaborate for successful exploitation of terrestrial habitats.

Archaic amphibians and other early stegocephalians

There are three groups of early stegocephalians: stem-tetrapods, amphibians, and reptiliomorphs. Stem-tetrapods include all stegocephalians that appeared before the divergence

between amphibians and reptiliomorphs, a divergence that ultimately resulted in the appearance of the lissamphibians and amniotes (reptiles, birds, and mammals), respectively. Stem-tetrapods include all known Devonian stegocephalians and perhaps many Carboniferous and Permian ones, as well. There is considerable uncertainty about the relationships of many of these taxa, because the phylogeny that was long accepted by most paleontologists was challenged in the late 1990s. Nevertheless, it is clear that a major evolutionary radiation of stegocephalians took place at the end of the Devonian and at the beginning of the Carboniferous, and that all of the main lineages (including amphibians and reptiliomorphs) existed by the Lower Carboniferous. However, reptiliomorphs may not be represented in the fossil record before the Upper Carboniferous.

Diversity of post-Devonian stegocephalians

Baphetids (formerly known as loxommatids) include five genera of seemingly aquatic stegocephalians from the Mississippian and Pennsylvanian (340–305 mya) of Europe and North America. These fossils are known primarily from skulls, which typically are broad and flat with a strange keyhole-shaped orbit. Baphetids may be allied with stem-tetrapods.

The three genera of crocodile-like colosteids, which are approximately contemporaneous with the baphetids, are important, because they once were considered to be closely related to the temnospondyls. However, the skulls of these fossils from Australia and North America lack a squamosal notch, a feature that characterizes temnospondyls, and its absence

in colosteids and the presence of a lateral-line organ suggest an aquatic existence.

Temnospondyls are a large group of more than 150 described genera; they extend from the Mississippian to the Lower Cretaceous, a span of about 200 million years. Most of the early temnospondyls and all of the Mesozoic representatives were aquatic, but others were amphibious, and some are thought to have been terrestrial. Among the latter are the dissorophoids, which are noteworthy because they have been argued to be closely related to living amphibians. Temnospondyls ranged in size from less than 12 in (30 cm) to more than 9.8 ft (3 m) in length. Many, if not all, dissorophoids had aquatic larvae with external gills. Some larval and/or paedomorphic (i.e., having larval or juvenile features maintained in sexually mature adults) dissorophids had bicuspid (and possibly pedicellate) teeth, as do lissamphibians; hence, dissorophids are thought by some scientists to be closely related to lissamphibians. Other paleontologists consider temnospondyls to be stem-tetrapods. Temnospondyls had a large opening in the palate (interpterygoid vacuity) that may have been involved in a buccal pump mechanism that is similar to that used by all lissamphibians to ventilate their lungs. The stapes (middle ear bone) of most temnospondyls is more slender and oriented more laterally than that of earlier stegocephalians. Because of this, some researchers think these animals possessed a tympanum (eardrum) in the otic notch (or squamosal embayment) of the skull. If this hypothesis is correct, then the absence of a tympanum in caecilians and salamanders must be secondary (i.e., having resulted from

an evolutionary loss). The vertebrae of early temnospondyls retained the rhachitome pattern that is primitive for stegocephalians. Rachitomous vertebrae had a large, ventral, crescentic intercentrum and small, paired, dorsal pleurocentra that supported the neural arch; such vertebrae are poorly suited to a terrestrial lifestyle. In Mesozoic temnospondyls, the vertebral column was consolidated to form the stereospondylous pattern, characterized by a large intercentrum, along with a small pleurocentrum that sometimes was cartilaginous. The functional reason for this strengthened vertebral column is unclear, because most, if not all, Mesozoic temnospondyls were strictly aquatic.

Embolomeres ranged in length from 12 in (30 cm) up to 9.8 ft (3 m) and were mostly aquatic and amphibious predators. The fossil record of embolomeres extends from the Upper Carboniferous into the Triassic, and they are known from Europe, North America, and Russia. Their vertebrae are composed of cylindrical intercentra and pleurocentra. Because they have a massive stapes, it is thought that embolomeres lacked a tympanum, but the stapes may have conducted low-frequency ground-borne and water-borne sounds. Embolomeres are important because earlier they were thought to be related to amniotes. However, now they are considered by many scientists to represent another group of stem-tetrapods.

Seymouriamorphs are another group of stem-tetrapods that was formerly thought to be closely related to amniotes. This relatively small (12 genera), but widespread, group is known from the Permian of North America, Europe, and Asia, and is represented by larvae bearing external gills and adults (ca. 3 ft [90 cm] long). The absence of lateral-line organs and gills in the adults suggests that they were terrestrial. Adult seymouriamorphs had a long, slender stapes, which suggests that they might have had a tympanum, and a rib architecture that suggests the capacity for costal ventilation of the lungs.

Diadectomorphs are represented by eight genera in the Upper Carboniferous and Lower Permian. Once considered to be amniotes, they now are thought to be closely related to them. These animals attained lengths of 6.5 ft (2 m). In addition to some carnivorous or piscivorous forms, diadectomorphs include some of the earliest herbivorous stegocephalians, the diadectids.

An assemblage of small amphibians (most less than 12 in [30 cm] long) comprising five groups (aïstopods, nectrideans, "microsaurs," adelogyrinids, and lysorophids) forms an evolutionary grade informally known as "lepospondyls." These animals are known from the Lower Carboniferous to the Upper Permian. Some seem to have been strictly aquatic (e.g., many nectrideans, adelogyrinids), whereas others (e.g., the "microsaurs" Pantylus and Tuditanus) apparently were amphibious or terrestrial. Most lepospondylous amphibians either lacked or had only a small otic notch or squamosal embayment (e.g., aelogyrinids); thus, they must have lacked a tympanum. If these amphibians include the closest known relatives of lissamphibians, then the ancestor of caecilians and salamanders probably lacked a tympanum, and the tympanum of anurans may have appeared only in the Triassic. The name of the group derives from the structure of their vertebrae, which are dominated by a large, cylindrical pleurocentrum that fused to the neural arch early in development, as it does in lissamphibians. In some lepospondyl amphibians, a small crescentic intercentrum remains, but in others it is lost, as it is in most lissamphibians.

Lissamphibia

The oldest known lissamphibians, a group consisting of the caecilians, salamanders, anurans, and their fossil allies, date from the Triassic, some 250 mya. The fossil record of this group is extremely scanty. Indeed, in the Triassic, which lasted about 37 million years, only two species of lissamphibians are known and both are closely related to anurans. Not all paleontologists agree that Lissamphibia is a natural group, but most neontologists consider it to be monophyletic. Regardless of which phylogenetic arrangement one prefers, there is a gap of several tens of million years between the sister group (i.e., dissorophoids or lysorophids) and the earliest known lissamphibian. Beginning in the Jurassic (206 mya) fossil lissamphibians become more common; however, the best-represented groups are those that inhabited an aquatic environment.

Salientia (anurans and Triadobatrachus)

Triadobatrachus, the oldest fossil lissamphibian, is from the Lower Triassic of Madagascar. It is known from a single specimen, a largely complete and articulated skeleton (4.2 in [10.6 cm] long), which reveals it to be closely related to anurans. It shares many cranial features with frogs and toads, but it differs from them by having a longer trunk, a less specialized pelvic girdle, shorter limbs, and a short tail. Another, slightly younger fossil, Czatkobatrachus, from the Lower Triassic of Poland, is based on a few, isolated bones; thus, little can be said about its affinities or phylogenetic position. Beginning in the Lower Jurassic, there are fossil representatives of each of the modern orders. However, the record for caecilians and the general quality of fossil salamanders are exceedingly poor in contrast to that for anurans.

Triadobatrachus is considered to be closely allied to anurans (frogs and toads). Together, these animals compose a taxonomic group known as Salientia. The earliest known anurans, Prosalirus and Vieraella, are from the Lower Jurassic of Arizona (United States), and Argentina, respectively, and approximately contemporaneous with Eocaecilia, the stem-caecilian. Each of these moderate-sized (2 in [50 mm] and 1.25 in [30 mm] in snout-vent length, respectively) frogs differs from the larger Triadobatrachus in having a shorter trunk, urostyle, lacking a tail, and possessing long hind limbs

in which the ankles are modified to form an extra limb segment. Unlike Triadobatrachus, these frogs clearly were capable of saltatorial (i.e., jumping, hopping) locomotion typical of extant anurans.

One genus, Eodiscoglossus, is represented by Middle Jurassic remains from Great Britain. This rather large frog (3.25

in [80 mm] in snout-vent length) is remarkably similar to living discoglossids, especially species of Discoglossus.

By the Late Jurassic, the fossil record of anurans is much more diverse taxonomically and geographically. Eobatrachus and Comobatrachus are known from Wyoming (United States), and Enneabatrachus from Wyoming and Utah (United States); all are of uncertain affinities. Notobatrachus, from several localities in Patagonia in Argentina, is one of the most important Middle–Late Jurassic finds, because it is represented by whole, articulated skeletons and numerous individuals, including juveniles and subadults. This frog was large, reaching a snout-vent length of about 5.7 in (14.5 cm). It has several primitive features, including free ribs on some of the vertebrae, a poorly developed sacrum, a relatively short pelvic girdle, and stout, relatively short hind limbs. This frog is thought to be ancestral to all living anurans. Two other taxa, Callobatrachus and Mesophryne, were described from Jurassic/Cretaceous fossil beds of China; the former is allied with discoglossids, but the affinities of the latter are unknown. The oldest fossil pipoid is Rhadinosteus from the Late Jurassic of Utah.

The Cretaceous produced a proliferation of anurans. Among the more significant Lower Cretaceous finds are the discoglossid Eodiscoglossus from Spain, and a variety of pipoid frogs—Thoraciliacus, Cordicephalus, and Shomronella (larvae) from Israel. Middle/Upper Cretaceous anurans include gobiatids from Mongolia and Uzbekistan, pipoid frogs from Argentina (Saltenia and Avitabatrachus) and Niger (Pachybatrachus), and leptodactylids

(Baurubatrachus and Estesius) from Brazil and Bolivia, respectively.

The Tertiary record of anurans is too extensive to recount here. Suffice it to say that most major families are represented by fossil remains from Europe, Africa, Asia, and North America.

Gymnophionans (caecilians and Eocaecilia)

Extant apodans or caecilians comprise a peculiar group of limbless, snake-like amphibians that are terrestrial or aquatic and specialized for burrowing; they possess a tentacle on each side of the head beneath the reduced eye. Most scientists consider caecilians to be the most basal of the lissamphibians. The Lower Jurassic (about 204 mya) fossil Eocaecilia from Arizona is thought to be a stem-caecilian. It differs from extant members of the group in having small, well-ossified limbs and girdle elements that are absent in living caecilians. Although the eyes were larger, and the skull contained more bones than living species, the lower jaw and the jaw-closing mechanism seem to resemble those of living representatives. The only other fossil remains associated with gymnophionans are vertebrae from the Upper Cretaceous of the Sudan, Early Paleocene of Bolivia, and Late Paleocene of Brazil. These fossils provide little useful information except that the modern families of caecilians had begun to differentiate by the late Mesozoic.

Urodeles (salamanders and related fossils)

Fossil urodeles are known from Middle Jurassic–Lower Cretaceous (about 180–127 mya) lake and lagoon deposits of Europe, the Upper Cretaceous–Eocene (about 90–35 mya) flood-plain deposits of North America, and the Eocene-Miocene (about 35–5 mya) brown-coals of Europe. In addition, there are remains from the Cretaceous of Bolivia, the Sudan, Niger, and Israel. Laccotriton, Sinerpeton, Jeholotriton, and Liaoxitriton are salamanders from the Upper Jurassic/Lower Cretaceous of China. With three exceptions mentioned below, all these remains clearly are caudate, i.e., belonging to salamanders. The affinities of Albanerpetontidae from Middle Jurassic–Miocene deposits of northern continents are equivocal. This group may represent a peculiar, early offshoot of the salamander lineage, or a separate lissamphibian group, the origin of which preceded the phylo-genetic divergence between caudates and anurans. The phylogenetic status of Ramonellus from the Lower Cretaceous of Israel is unknown. A third taxon, Triassurus, was described from the Triassic of Uzbekistan. If the latter poorly preserved remains prove to be those of a urodele, then the group would have originated in the Triassic or earlier.

The earliest fossil remains of salamanders that can be definitely identified as caudates are the Jurassic remains from China, the karaurid salamanders, Karaurus and Kokartus, from Kazakhstan and Kirghizstan, and Marmorerpeton from England. The extant groups of salamanders are represented by a surprising number of fossils. (1) Sirenidae: Upper Cretaceous and Paleocene of North America; Cretaceous remains of several taxa from southern continents may also be related to sirenids;(2) Hynobiidae: Upper Pliocene of Kazakhstan; (3) Cryptobranchidae: Paleocene of Mongolia and Russia, Upper Oligocene–Pliocene of Europe, Upper Paleocene–Upper Miocene of North America, with Pleiocene–Pleistocene occurrences of Cryptobranchus in North America; (5) Salamandroids Ambystomatidae, Amphiumidae, Dicamptodontidae, Plethodontidae, Proteidae, Rhyacontritonidae, and Salamandridae): Stem-salamandroids from Lower Cretaceous of Europe; Amphiumidae from Paleocene–Pleistocene of North America; Dicamptotontidae from Paleocene of Canada; Salamandridae from Upper Paleocene and onwards of Europe and Upper Miocene of East Asia, and Neogene of North America. In addition, there are three groups of fossil caudates of uncertain affinities: batrachosauroids from Mid-Cretaceous–Lower Pliocene of North America and Europe; scapherpetontids from Upper Cretaceous, Paleocene, and Eocene of North America, and possibly Cretaceous of Asia; and dicamptodontid-like salamanders from Paleocene–Miocene of Europe.

Resources

Books

Duellman, William E., and Linda Trueb. Biology of Amphibians. New York: McGraw-Hill Book Co., 1986.

Estes, Richard. Handbuch der Paläoherpetologie, Vol. 2. Stuttgart: Gustav Fischer Verlag, 1988.

Heatwole, Harold, and Robert L. Carroll, eds. Amphibian Biology. Vol. 4, Palaeontology. The Evolutionary History of Amphibians. Chipping Norton, Australia: Surrey Beatty & Sons Pty. Limited, 2000.

Sanchíz, Borja. Encyclopedia of Paleoherpetology. Part 4, Salientia. Munich: Verlag Dr. Friedrich Pfeil, 1998.

Schultze, Hans-Peter, and Linda Trueb, eds. Origins of the Higher Groups of Tetrapods. Controversy and Consensus. Ithaca, NY: Comstock Publishing Associates, Cornell University Press, 1991.

Periodicals

Báez, Ana Maria, Linda Trueb, and Jorge O. Calvo. "The Earliest Known Pipoid Frog from South America: A New Genus from the Middle Cretaceous of Argentina." Journal of Vertebrate Paleontology 20 (2000): 490–500.

Gao, Ke-Qin, and Yuan Wang. "Mesozoic Anurans from Liaoning Province, China, and Phylogenetic Relationships of Archaeobatrachian Anuran Clades." Journal of Vertebrate Paleontology 21 (2001): 460–476.

Laurin, Michel. "A Reevaluation of the Origin of Pentadactyly." Evolution 52 (1998): 1476–1482.

——. "The Importance of Global Parsimony and Historical Bias in Understanding Tetrapod Evolution. Part I—Systematics, Middle Ear Evolution, and Jaw Suspension." Annales des Sciences Naturelles, Zoologie 13ème Série, 19 (1998): 1–42.

Laurin, Michel, Marc Girondot, and Armand de Ricqlès. "Early Tetrapod Evolution." Trends in Ecology and Evolution 15 (2000): 118–123.

Laurin, Michel, and Rodrigo Soler-Gijon. "The Oldest Stegocephalian from the Iberian Peninsula: Evidence that Temnospondyls Were Euryhaline." Comptes Rendus de l'Académie des Sciences de Paris, Sciences de la vie/Life Sciences 324 (2001): 495–501.

Linda Trueb, PhD

Michel Laurin, PhD