So here we are: anuran diversity part II – you have to have read part I (here) for the following to make proper sense. Yesterday I showed my video of Tiger the secretary bird (filmed at the International Bird of Prey Centre, Gloucestershire, last week) to anybody that would watch, and in the wee small hours I even completed the first draft of a paper on yet another new Wealden theropod (as always, more on that in due time). I remain perpetually busy with those pesky ichthyosaurs. Oh yeah, and happy wedding anniversary me and Tone (yes, we got married on Halloween. Don’t ask). Anyway, anurans…

Conventionally regarded as intermediate between discoglossids and neobatrachians are the so-called transitional anurans: the pipoids (clawed frogs and relatives) and pelobatoids (spadefoot toads and relatives). If pipoids and pelobatoids are sister-taxa (a possibility supported by shared characters of the frontoparietals and cranial musculature), they can be united in a group termed Mesobatrachia (Ford & Cannatella 1993)*. Several recent studies (Gao & Wang 2001, Pugener et al. 2003, Haas 2003, Frost et al. 2006) have found no support for a special pipoid + pelobatoid clade; most have found pipoids to be more basal (viz, further away from Neobatrachia) within Anura than discoglossids, and Pugener et al. (2003) found pipoids to be the most basal anurans, further down the tree than even leiopelmatids. This view seems radical today, but it has generally been supported by those who have classified anurans on the basis of larval morphology: pipoids have ‘Type 1′ larvae following Orton’s (1953, 1957) scheme (Type 1 larvae lack keratinous oral structures and have paired spiracles). The node-based name Pipanura has been proposed for the Mesobatrachia + Neobatrachia clade (Ford & Cannatella 1993): Pipanura is thus the clade name for all anurans excepting leiopelmatids in those phylogenies where pipoids are more basal than discoglossids but more crown-ward than leiopelmatids, but Pipanura would be synonymous with Anura in those phylogenies where pipoids are the most basal anurans (a possibly useful cladogram depicting some of these inferred relationships is shown below).

* Mesobatrachia was employed by Ford & Cannatella (1993) as a node-based name for the clade that contains pipoids and pelobatoids, rather than for a ‘pelobatoid-pipoid only’ clade. Mesobatrachia therefore exists, no matter what the exact relationship between pipoids and pelobatoids, although its content differs widely according to the favoured phylogeny. It includes all anurans if Pugener et al. (2003) are correct, for example.

The African clawed frogs, the dwarf clawed frogs [one is shown in the adjacent image], and their South American relatives are all grouped together in Pipidae. Pipids are tongueless, have flattened bodies and (excepting Pipa) clawed feet*, and are highly aquatic. They include both highly familiar anurans (Xenopus laevis, the African clawed frog, is known worldwide as a laboratory animal), and among the most bizarre (such as the surreal Surinam toad Pipa pipa, a species that keeps its developing eggs and larvae within skin pockets on its back, and possesses a very odd, depressed, hyperossified skull [see Trueb et al. (2000) for more on the latter: P. pipa shown at top of article]). Rhinophrynus dorsalis, the Burrowing toad (the only extant member of a formerly more diverse clade), appears to be a close relative of the pipids and shares with them fused skull roof bones, enlarged otic capsules and other characters. DNA sequence data and the morphology of the tadpoles (among many other shared characters, they have paired spiracles and lack keratinized jaw sheaths (Haas 2003)) also unites these animals, and together they form the clade Pipoidea (this is essentially the same as the group that Cope (1889) named Aglossa; the name Xenoanura Savage, 1973 has also been used for this clade). Pipoids have a rich fossil record extending back to the Upper Jurassic.

* Given that claws are generally absent in lissamphibians and are better associated with amniotes, you might be wondering what implications the structures present in pipids have for the evolution of amniote claws. Maddin et al. (2007) looked at this issue and showed that pipid claws were non-homologous with those of amniotes. Besides pipids, claws in lissamphibians are also present in some hynobiid, ambystomatid and plethodontid salamanders.

Pelobatids and pelodytids – the spadefoot toads and parsley frogs – are generally (but not universally) united in a clade termed Pelobatoidea (Anomocoela Nicholls, 1916 is also sometimes used for this group). The shape of the sternum and the presence of a palatal process on the maxilla have been suggested as pelobatoid synapomorphies. All pelobatoids possess vertical pupils, have free-living, aquatic tapoles, and many members of the group are well-known for being specialised for burrowing and for tolerating high levels of water loss. Unlike the anurans we’re most familiar with (nearly all of which are members of Neobatrachia), male pelobatoids grasp the females around the waist (this is termed inguinal amplexus), rather than behind the forelimbs (this is termed axilliary amplexus)*. The megophryids (or megophryines) of SE Asia are also members of Pelobatoidea; the best-known megophryids are highly cryptic ‘horned’ anurans of tropical forest floors. Scaphiopodids – the two genera of North American spadefoot toads – are also members of Pelobatoidea, and they share with pelobatids a specialised digging spade; it’s actually an enlarged, keratinized metatarsal tubercle supported internally by the prehallux.

* Inguinal amplexus is also practised by various other anurans (including sooglossids, some bufonids and various taxa conventionally included in Leptodactylidae), but has apparently arisen independently from that seen in pelobatoids. The picture above shows Mexican spadefoot toads Spea multiplicata engaged in inguinal amplexus.

In some characters, pelobatoids are quite similar to neobatrachians, and some studies find the two groups to be sister-taxa in a clade that can be called Acosmanura Savage, 1973 (Cannatella & Hillis 2004, Roelants & Bossuyt 2005, San Mauro et al. 2005, Frost et al. 2006). In contrast to other anurans, pelobatoids and neobatrachians possess palatine bones, and the tadpoles of both groups exhibit just a single row of keratodonts on the oral labia and a single spiracle located on the animal’s left side. However, some workers have questioned the homology of the palatines in pelobatoids and neobatrachians, and some have argued that pelobatoids are most closely related to discoglossids (Gao & Wang 2001).

This cladogram depicts a sort of rough consensus of views on anuran phylogeny, though note that studies differ on the relative positions of some of the clades. Pipoids are more basal than leiopelmatids according to some studies, for example. Following Ford & Cannatella (1993), Anura is the node-based clade that includes all extant frogs and toads; Mesobatrachia is the node-based clade that includes pipoids and pelobatoids (Ford & Cannatella regarded these two as sister-taxa, but if they’re far apart – as shown here – then Mesobatrachia is more inclusive); Pipanura is the node-based Mesobatrachia + Neobatrachia clade (and, as shown here, is thus redundant with respect to an inclusive version of Mesobatrachia); and Bombinanura is the node-based clade that includes bombinatorids + discoglossids and neobatrachians. The name Costata Lataste, 1879 was used for the discoglossid + bombinatorid clade by Frost et al. (2006). Frost et al. also used the new name Sokolanura for the Costata + Acosmanura clade, though they didn’t say whether it it node-, stem- or apomorphy-based. If it’s node-based it’s synonymous with Bombinanura. Acosmanura Savage, 1973 was used by Frost et al. (2006) for the Anomocoela + Neobatrachia clade.

All of the anurans we’ve looked at so far are outside of Neobatrachia, the anuran clade that includes pretty much all the more familiar species, and in fact about 96% of all extant anuran species. All non-neobatrachians were formerly united in a group called Archaeobatrachia*, but, because it is now generally agreed that this group is paraphyletic (a few recent molecular studies have found it to be monophyletic), its use is generally discouraged. Neobatrachians are united by fusion of some of the carpals and by various characters of musculature and genetics. As might be expected with any radiation of organisms that consists of literally thousands of species, it has proved difficult to come to a consensus on neobatrachian phylogeny, and massive complications have been introduced by convergence, parallelism and reversals. Consider how many clades belong to Neobatrachia (the following isn’t a complete list, just a cherry-picking of some of the groups): true treefrogs (hylids), rhacophorid treefrogs, the American leptodactylids and Australasian myobatrachids, toads (bufonids), narrow-mouthed frogs (microhylids), glass frogs (centrolenids), poison-arrow frogs (dendrobatids), reed and lily frogs (hyperoliids), ranids, squeakers (arthroleptids), ghost frogs (heleophrynids) and paradox frogs (pseudids). Some of these groups consist of hundreds of species and multiple genera: microhylids, which you might not have even heard of, include more than 420 species in about 70 genera.

* Although the original use of this term (Reig 1958) was quite different: Reig used Archaeobatrachia for discoglossids, rhinophrynids and pelobatoids alone.

And it’s neobatrachians that I aim to cover next.

Refs – -

Cannatella, D. C. & Hillis, D. M. 2004. Amphibians: leading a life of slime. In Cracraft, J. and Donoghue, M. (eds), Assembling the Tree of Life. Oxford University Press (Oxford), pp. 430-450.

Cope, E. D. 1889. The Batrachia of North America. Bulletin of the United States National Museum Bulletin 34, 1-525.

Ford, L. S. & Cannatella, D. C. 1993. The major clades of frogs. Herpetological Monographs 7, 94-117.

Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De Sá, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P., Drewes, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. & Wheeler, W. C. 2006. The amphibian tree of life. Bulletin of the American Museum of Natural History 297, 1-370.

Gao, K. & Wang, Y. 2001. Mesozoic anurans from Liaoning Province, China, and phylogenetic relationships of archaeobatrachian anuran clades. Journal of Vertebrate Paleontology 21, 460-476.

Haas, A. 2003. Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics 19, 23-90.

Maddin, H. C., Musat-Marcu, S. & Reisz, R. R. 2007. Histological microstructure of the claws of the African clawed frog, Xenopus laevis (Anura: Pipidae): implication for the evolution of claws in tetrapods. Journal of Experimental Zoology (Mol Dev Evol) 308B, 259-268.

Orton, G. L. 1953. Systematics of vertebrate larvae. Systematic Zoology 2, 63-75.

- . 1957. The bearing of larval evolution on some problems in frog classification. Systematic Zoology 6, 79-86.

Pugener, L. A., Maglia, A. M. & Trueb, L. 2003. Revisiting the contribution of larval characters to an analysis of phylogenetic relationships of basal anurans. Zoological Journal of the Linnean Society 139, 129-155.

Reig, O. A. 1958. Proposiciones para una nueva macrosistematica de los anuros. Nota preliminar. Physis 21, 109-118.

Roelants, K. & Bossuyt, F. 2005. Archaeobatrachian paraphyly and pangaean diversification of crown-group frogs. Systematic Biology 54, 111-126.

San Mauro, D., Vences, M., Alcobendas, M., Zardoya, R. & Meyer, A. 2005. Initial diversification of living amphibians predated the breakup of Pangaea. The American Naturalist 165, 590-599.

Trueb, L., Púgener, L. A. & Maglia, A. M. 2000. Ontogeny of the bizarre: an osteological description of Pipa pipa (Anura: Pipidae), with an account of skeletal development in the species. Journal of Morphology 243, 75-104.