Oh, to be a so-called 'transitional anuran'

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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.

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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.

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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).

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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.


More like this

"(Xenopus laevis, the African clawed frog, is known worldwide as a laboratory animal)"

...and is becoming notorious, nearly worldwide, as an invasive. I have collected the tadpoles in Irvine, California, for example.

[from Darren: believe it or don't, we also have them feral here in the UK (definitely in Wales and on the Isle of Wight). See, for example...

Lever, C. 1977. The Naturalized Animals of the British Isles. Hutchinson & Co, London.

Measey, G. J. 1998. Diet of feral Xenopus laevis (Daudin) in South Wales, U.K. Journal of Zoology 246, 287-298.

- . & Tinsley, R. C. 1998. Feral Xenopus laevis in South Wales. Herpetological Journal 8, 23-27.]

By Sven DiMIlo (not verified) on 31 Oct 2007 #permalink

I think I never saw a blog
So keen to celebrate the frog.

A blog that finds the anurans'
A tale at least as cool as man's;

A blog that looks at tetrapods
Which, over eons, beat the odds;

A blog that posts on what may be
Transitional morphology;

Reporting on the Pipoid classic,
Whose family tree has roots Jurassic.

I have found frogs, in wood and bog
But learned much more within this blog.

You're married? Truly you are a bastard Darren.

Rhinophrynus dorsalis, the Burrowing toad (the only extant member of a formerly more diverse clade)

Only one member (and/or one ghost lineage) is known from any given time, even though that time stretches back to the Late Jurassic. (The whole tree is in my paper.)

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.

Having Bombinanura ( = Discoglossanura...) as part of Pipanura rather than the other way around is not consensus. It is currently a minority view. I even used to think it was unique to Frost et al. (2006)...

(a few recent molecular studies have found [Archaeobatrachia] to be monophyletic)

This is considered an indicator of long-branch attraction by the latest paper that found it.

microhylids, which you might not have even heard of, include more than 420 species in about 70 genera.

They're probably cheating by not being monophyletic, though...


Hi, Cuttlefish! :-)

By David Marjanović (not verified) on 01 Nov 2007 #permalink

Thanks for those comments David. I did think of passing the text to you for checking first, but couldn't be bothered. I mean.. a peer-reviewed blog article? On Pipanura and all that: I was looking at Haas (2003), Pugener et al. (2003) and Frost et al. (2006) when deciding that Pipanura should include Bombinanura/Discoglossanura... is it really a minority view? (granted, it certainly used to be).

PS - does the article look properly formatted? Some people are saying that everything is squished down the bottom of the page.

Haaah! :-) Having the text peer-reviewed by me would not have been a good idea, because I've never seen Haas (2003) or Pugener et al. (2003). However, I don't see how using only "primarily larval characters" differs from deliberately throwing data away, the way it was done in ye olden times when some people used, say, only braincase characters and others used only tooth characters and all argued over which characters were "important".

Actually, I think I've not even seen Cannatella & Hillis (2004). And today, er, yesterday was a holiday over here, so I couldn't have gone to the university and check.

The formatting is perfect. MSIE 7 on Windows XP. I'll check again tomorrow in the university, where it's Safari on Mac OS X.

By David Marjanović (not verified) on 01 Nov 2007 #permalink

However, I don't see how using only "primarily larval characters" differs from deliberately throwing data away

Sorry if I created the impression that those recent studies are based on 'larval characters only', they're not. Well, ok, Orton (1953, 1957) classified anurans on this basis and Hecht (yes, the palaeontologist) argued that this was the only sure-fire way of elucidating their phylogeny, and agreed with Orton that taxa with Type I larvae were more basal than those with Type II, and so on (Hecht 1963). When you get the chance, do definitely read Pugener et al. (2003) (abstract). They ran larval-only, adult-only, and combined data sets, and all analyses recovered pipoids as the most basal anurans (the combined data set failed to support neobatrachian monophyly; am going to comment on that later). Looks pretty good to me.

Ref - -

Hecht, M. K. 1963. A reevaluation of the early history of the frogs. Part II. Systematic Zoology 12, 20-35.

What other blog has references within an edit?

And, Darren, do you really think anyone who reads this blog is the least bit surprised you'd have been married on Halloween?

[from Darren: hmm :)]

By Mike from Ottawa (not verified) on 01 Nov 2007 #permalink

Sorry if I created the impression that those recent studies are based on 'larval characters only', they're not.

I was judging Haas (2003) from its title... I'll read Pugener et al. (2003) in about 15 hours. :-)

Hecht (yes, the palaeontologist)

The one of Tarsitano and Hecht (1980)?

By David Marjanović (not verified) on 01 Nov 2007 #permalink

I just found we have Pugener et al. (2003) here in the lab. It's a thick paper... I'll read it later.

By David Marjanovi? (not verified) on 02 Nov 2007 #permalink

Finished all but the last 4 pages. Well, the amount of characters is low (146) and the taxon sampling (20 + 1) is poor: not one fossil (even though they talk about some), no Leiopelma, only three neobatrachians, the derived salamander Ambystoma talpoideum alone forming the whole outgroup. As long as morphological analyses stay so much smaller than molecular ones, they should be taken rather lightly. Also, all characters were unordered, even though some should have been ordered. This means that intermediate conditions were interpreted by the program as terminally derived ones, possibly leading to spurious clades.

Speaking of fossils, why didn't you mention the palaeobatrachids? They're boring, but at least they have a good fossil record :-)

It's also interesting that the first author spells herself Pugener in this paper, but cites herself as Púgener in three others. It's not the case that the Zool. J. Linn. Soc. had something against accents on capital letters -- "Analía" is printed just fine. ~:-|

By David Marjanović (not verified) on 02 Nov 2007 #permalink

Speaking of fossils, why didn't you mention the palaeobatrachids?

I wanted to lay off the fossil history but, yeah, I suppose I could have mentioned them. I don't think they're boring - those giant Miocene tadpoles (150 mm long) are pretty cool.

On Pugener, one of my biggest pet peeves is workers who have different names according to different publications. I have no idea why the accent appears and disappears according to the publication - very frustrating.

And the Hecht is, yes Max K. Hecht. He should be better known for his stuff on anurans, choristoderes and crocodylomorphs than for his birds-can't-be-dinosaurs stuff, but such is the curse of being outspoken on avian origins. Then again, if you hold non-standard and erroneous views on one subject, does this mean that your other work should be looked at with an exceptionally sceptical eye?

does this mean that your other work should be looked at with an exceptionally sceptical eye?

Of course not. I'm just prone to confusing people (like Andrew Milner, his wife Angela Milner, and the other Andrew Milner, or the two people called Rainer Schoch...) and wanted to prevent myself from getting yet another false impression.

[from Darren: sorry David, I wasn't directing that question at you - it was meant to be rhetorical.]

By David Marjanović (not verified) on 03 Nov 2007 #permalink

Pipids are tongueless (how many tetrapods are tongueless?) *and* they have claws that aren't homologous to amniote claws.

Damn. They /are/ interesting.

(If the claws aren't homologous, how do they arise?)

Doug M.

If it leaps at all, then yes. Only Leiopelma and Ascaphus do what's described in your link.

By David MarjanoviÄ (not verified) on 25 Nov 2010 #permalink