Palaeontology: Chinese salamanders tell tales

ROBERT CARROLL

Robert Carroll is at the Redpath Museum, McGill University, 859 Sherbrooke Street West, Montreal H3A 2K6, Canada.
e-mail: robertc@shared1.lan.mcgill.ca


A palaeontological treasure trove of over 500 specimens will help in understanding the evolutionary history of salamanders and their relationships with other amphibians.

On page 574 of this issue1, Gao and Shubin report the discovery of hundreds of superbly preserved salamander skeletons from a 150-million-year-old pond deposit in China. The specimens include both larval and adult stages. They will help to answer questions about the evolutionary relationships and geographical distribution of the 10 living families of salamanders, as well as about the ancestry of salamanders — the order Caudata (urodeles) — as a whole. The urodeles are one of three orders that comprise the modern amphibians, the others being frogs and a limbless group known as the caecilians. The age of this deposit is based on radiometric dating and association with other fossils common to the Upper Jurassic (see Fig. 1 for timescale).

Figure 1 Geological timescale showing the overall pattern of amphibian evolution, and the time of occurrence of the fossils discussed by Gao and Shubin and shown in Fig. 2. 1, Eocaecilia micropodia. 2, Valdotriton gracilis. 3, The newly described1 Chinese species. 4, Prosalirus bitis. 5, A Lower Triassic amphibian, close to the ancestry of frogs.
 

More than 500 specimens were collected from an area of less than 10 m2 that had been buried by a volcanic eruption. The specimens include two species whose growth stages illustrate the main life-history strategies of modern salamanders. One exhibits the pattern of metamorphosis common to many living amphibians: aquatic larvae possessing external gills, with the gills being lost in larger, more fully ossified specimens that are presumed to be terrestrial. The second species, like members of many modern salamander families, was apparently neotenic — that is, it reached sexual maturity without metamorphosing into a fully terrestrial form. That some examples of this species had reached maturity can be seen from the high level of ossification of the bones in the wrists and ankles. But the gill supports are also ossified, indicating that the creature still relied on external gills for aquatic respiration.

The fossils are immediately recognizable as salamanders from their body and limb proportions, as well as from details of the skull anatomy. They also share with modern salamanders a unique aspect of limb development, in which the two most anterior elements of the distal row of bones in the wrist and ankle are fused to form a single bone, known as the basal commune, that supports the first two digits. No group of vertebrates other than salamanders has this specific configuration.

The closest relationships of the Chinese specimens with living salamanders lie within the most primitive families, the Hynobiidae and Cryptobranchidae, which together constitute the superfamily Cryptobranchoidea. The Chinese fossils and cryptobranchoids share the retention of several bones that are lost in more advanced salamanders (including the lacrimal bone, which bears the lacrimal duct, and a separate angular bone in the lower jaw). But the fossil specimens appear to be even more primitive in their retention of a separate coronoid bone in the adult and the presence of more than three caudal vertebrae bearing ribs. Given the close affinities of the Jurassic species with the cryptobranchoids, Gao and Shubin argue that the initial radiation of all later salamander lineages occurred in Asia, before they spread to Europe and North America.

The primitive position of the Chinese species is evident from Gao and Shubin's phylogenetic analysis, which combines skeletal data from fossils and modern families with molecular evidence from living amphibians. But the consensus trees provide little resolution of the specific pattern of interrelationships of the more advanced families. Further study of these and other Mesozoic salamanders from China should allow the sequences in which the families diverged to be more reliably established.

The ancestry of salamanders remains highly contentious, and the newly discovered fossils should help here, too. It is generally accepted that salamanders shared with frogs and caecilians (which have greatly elongated bodies but lack limbs, and are restricted to the wet tropics) an immediate common ancestry that was distinct from that of all other terrestrial vertebrates. But the various hypotheses about the Palaeozoic ancestry of salamanders differ considerably2, 3.

The Chinese fossils and living cryptobranchoids show a host of features that indicate a long period of evolution after they had diverged from the ancestors of frogs and caecilians. The limb proportions of primitive salamanders are similar to those of most Palaeozoic amphibians, but they show no evidence of the jumping habit of frogs or the snake-like body of caecilians that were already established by the Lower Jurassic4, 5 Fig. 2. Whereas frogs had evolved a highly derived tadpole by the Lower Cretaceous, with a distinctive filtering apparatus for feeding on microscopic plant material, salamanders retained gradual metamorphosis without a distinct change in diet between the larvae and adults.

Figure 2 Comparison of the body proportions and limb structures of a fossil salamander, caecilian and frog. a, Valdotriton gracilis8, a salamander from the Lower Cretaceous of Spain. This species broadly resembles the Upper Jurassic salamander, described by Gao and Shubin1, which underwent metamorphosis from an aquatic larval stage to a terrestrial adult. b, A caecilian (Eocaecilia micropodia) and, c, a frog (Prosalirus bitis) from the Lower Jurassic of Arizona. The distinct anatomy and way of life of Jurassic salamanders, caecilians and frogs, and the presence of a putative frog ancestor from the Lower Triassic, suggest that separate ancestral lineages for all three orders should be sought among Palaeozoic amphibians. Scale bars are 1 cm. Parts a, b and c are reproduced from refs 8, 5 and 4, respectively.   
 

The high degree of adaptive and structural divergence of the modern amphibian orders does not necessarily mean that they did not ultimately have a common ancestry. But it does point to the importance of establishing the specific ancestry of each of the three lineages, and how they may be related to the great diversity of Palaeozoic amphibians. In most aspects of their body proportions and feeding apparatus, primitive living salamanders resemble the Palaeozoic branchiosaurs6 — small, immature amphibians with external gills. Like modern salamanders, many branchiosaurs were neotenic; this is a lifestyle that is not possible for frogs because they cannot reproduce before metamorphosis7.

We have no fossil from the Upper Permian or Triassic to link the essentially modern salamanders of the Jurassic with any putative Palaeozoic ancestors. But the Chinese specimens now provide a way to compare the two — including not only the adult anatomy, but also the generally untapped information from larval stages and patterns of development that can also be studied in branchiosaurs.

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References
1. Gao, K.-Q & Shubin, N. H. Nature, 410, 574-577 (2001). |  |
2. Milner, A. Herpetol. Monogr. 7, 8-27 (1993).
3. Laurin, M. & Reisz, R. in Amniote Origins (eds Sumida, S. S. & Martin, K. L. M.) 9-59 (Academic, San Diego, 1997).
4. Shubin, N. H. & Jenkins, F. A. Nature 377, 49-52 (1995).
5. Jenkins, F. A. & Walsh, D. M. Nature 365, 246-249 (1993).
6. Boy, J. A. & Sues, H.-D in Amphibian Biology Vol. 4, Palaeontology: The Evolutionary History of Amphibians (eds Heatwole, H. & Carroll, R. L.) 1150-1197 (Surrey Beatty, Chipping Norton, New South Wales, 2000).
7. Wassersug, R. J. Am. Zool. 15, 405-417 (1975).
8. Evans, S. E. & Milner, A. R. Phil. Trans. R. Soc. Lond. B 351, 627-646 (1996).


Nature © Macmillan Publishers Ltd 2001 Registered No. 785998 England.