So here we are, back with the anurans. In the previous article on neobatrachians (here), we looked at the basic division of the neobatrachians into the mostly New World Hyloidea, and the mostly Old World Ranoidea. While the characters historically used to differentiate hyloids (an arciferal pectoral girdle and procoelous vertebrae) are now understood to be primitive within neobatrachians, recent molecular studies have revealed good support for a clade that more or less corresponds with traditional Hyloidea. Many anuran workers have included within Hyloidea the Australasian southern frogs (or myobatrachids) and the huge assortment of American neobatrachians conventionally lumped together in the group Leptodactylidae; some workers have found the Seychelles frogs (or sooglossids) to be basal members of the clade as well. This is the scheme I pretty much followed in the previous article.
However, a close association of Seychelles frogs and southern frogs with a group of neobatrachians that we might term the ‘core hyloids’ is not agreed upon by everyone: Darst & Cannatella (2004) found support from mitochondrial DNA for a ‘core hyloid’ clade that includes eleutherodactylines, glass frogs (centrolenids), toads (bufonids), phyllomedusine and pelodryadine treefrogs, and horned frogs (ceratophryines or ceratophryids), and they argued that Hyloidea should best be used as a node-based name for the clade that includes these groups, but not necessarily the other groups traditionally included within Hyloidea.
The monophyly of ‘core hyloids’ seems generally agreed upon, with one interesting area of agreement being the inclusion within the clade of the South American dendrobatids or poison-dart frogs, or poison-arrow frogs, or poison frogs (Hay et al. 1995, Ruvinsky & Maxson 1996, Darst & Cannatella 2004, Frost et al. 2006). Dendrobatids have actually been one of the most controversial groups within neobatrachian phylogeny: like ranoids, and unlike most hyloids, they possess firmisternal pectoral girdles (see the previous anuran article) and Ford & Cannatella (1993), confident of the classification of these frogs among the ranoids, used dendrobatids as one of several specifiers in their phylogenetic definition of Ranoidea. While a reasonably long list of studies have indeed included dendrobatids among the ranoids, a roughly equal number have grouped them with various hyloid lineages, so use of Dendrobatidae as a phylogenetic specifier is not appropriate, and regret about the decision was expressed by Cannatella & Hillis (2004).
One of the most speciose and widespread neobatrachian groups is Hylidae, the treefrogs: an immense group of over 860 species from the Americas, Australasia, tropical Asia, Europe and northern Africa. Treefrogs have conventionally been grouped together on the basis of claw-shaped terminal phalanges: they also possess intercalary elements (accessory digit segments located between the distal and penultimate phalanges), though the latter also occur in glass frogs (more on those in a moment). Most treefrogs are green arboreal frogs with expanded toe pads, but many are terrestrial, some (like the American burrowing treefrogs Smilisca and some Australian Litoria species) are burrowers, and some (like the paradox frogs) are aquatic. Several recent studies have looked at hylid phylogeny (Darst & Cannatella 2004, Faivovich et al. 2005, Wiens et al. 2005, Frost et al. 2006): the details differ, but the more recent of these works conclude that Hylidae includes a pelodryadine + phyllomedusine clade, and a far larger and more diverse hyline clade. The most divergent hylids are the bizarre leaf frogs, monkey frogs or phyllomedusines, a group of tropical American taxa that superficially resemble slow-climbing primates like lorises (indeed one taxon is named Pithecopus; another is named Philomantis lemur).
As we saw in the article on horned treefrogs (here), experts disagree as to whether horned treefrogs and other marsupial treefrogs are part of Hylidae or not. While the exact relationships of marsupial treefrogs remain controversial (as does their monophyly), they are almost certainly ‘core hyloids': Wiens et al. (2005) found them to be close to eleutherodactylines, and not allied to other hylids. This means that the intercalary elements and claw-shaped phalanges present in marsupial treefrogs are convergent with those of hylids. As we saw earlier, marsupial treefrogs are of course well known for keeping their eggs and/or young in dorsally located pouches. Yes, frogs with pouches.
Treefrogs have a fossil record going back to the Palaeocene, and this and various other lines of evidence shows that most hyloid lineages originated either late in the Cretaceous or early in the Cenozoic. There are very few fossils to show for this though! [image above shows the phyllomedusine Phyllomedusa iheringii].
Previously classified in their own ‘family’ are the paradoxical frogs (or pseudids, or pseudines… or pseudaens). These are slippery-skinned, mostly aquatic South American frogs, best known for the fact that their tadpoles reach sizes that can exceed those of metamorphosed adults (a 250 mm tadpole might metamorphose into a 70 mm adult) [adjacent image shows lar- – small tadpole of Pseudis paradoxa]. Particularly elongate intercalary elements help add length to their long, webbed digits. Though previously thought to have diverged from a common ancestor that also gave rise to hylids and glass frogs (Ford & Cannatella 1993), molecular data now seems to show that paradoxical frogs are deeply nested within Hylidae, and in fact within Hylinae (Darst & Cannatella 2004, Wiens et al. 2005, Frost et al. 2006).
Whence all those ‘leptodactylids’?
As noted a few times in these anuran articles, the large and diverse assemblage of hyloids conventionally grouped together as Leptodactylidae is quite clearly not a clade. Frost et al. (2006) found hylids to be the sister-taxon to a hyloid clade that they named Leptodactyliformes: along with glass frogs, horned frogs, poison-arrow frogs and toads, it includes several clades previously included within Leptodactylidae, most of which consist of obscure South American frogs (I’ll be covering at least some of these groups in articles that will appear in January 2008). The term Leptodactylidae was restricted by these authors to a leptodactyliform clade that includes the nest-building frogs (Leptodactylus) and a host of other taxa, most of which are terrestrial, superficially ranid-like frogs that build foam nests [adjacent picture shows the Brazilian Yellow painted frog L. flavopictus].
The eleutherodactylines – a tropical American group of often tiny forest-floor frogs, most of which produce large terrestrial eggs that undergo direct development – were found by Frost et al. (2006) to be basal among the ‘core hyloids’ (more so than hylids and leptodactyliforms), and similar results were reported by Cannatella & Hillis (2004) and Darst & Cannatella (2004). Eleutherodactylines were conventionally included in Leptodactylidae, but the older name Brachycephalidae Günther, 1858 is increasingly used for them. They’re best known for including the smallest of all tetrapods: there are a couple of species from Cuba and Brazil that have SVLs of 10 mm or slightly less (9.8 mm in Brazilian Psyllophryne didactyla). Continuing the superlatives… this is a huge group, with over 820 species.
Green-boned glass frogs
Glass frogs, or centrolenids, are wide-skulled, long-limbed arboreal little frogs (SVL 20-60 mm) of Central and South American cloud and rain forests. Most lay eggs on vegetation overhanging water, or on rocks above the water surface. Their eyes are set on the tops of their heads, they have adhesive disks on their digit tips, and – while they are generally greenish on their dorsal surface – they derive their common name from the fact that they lack pigment on their ventral surface, meaning that their undersides are essentially transparent. I have no idea why this is, and I’m not sure that anyone else does. Even stranger, most (perhaps all) species have green bones. Green bones. Their terminal phalanges are T-shaped (this is also the case in a few other neobatrachian groups, like poison-arrow frogs), the males of some species possess spines on their upper arms (these are used in territorial combat), and the two uniquely elongate ankle bones that characterise anurans (the tibiale and fibulare) are fused into a single element [adjacent image shows a species of Hyalinobatrachium: note the transparent ventral surface].
This isn’t a small or insignificant group: there are about 140 named species (a number that has increased from about 65 since the late 1980s), with multiple additional ones recognised but awaiting description (Cisneros-Heredia & McDiarmid 2006, pp. 12-13). Though often allied with hylids, data from mitochondrial DNA now indicates that glass frogs are more closely related to toads and leptodactylids sensu stricto (Darst & Cannatella 2004, Frost et al. 2006). It has also been suggested that glass frogs are the sister-taxon of Allophryne ruthveni (Austin et al. 2002), a controversial and problematical toothless hyloid that has often been given its own ‘family’, Allophrynidae (a second species of Allophryne has recently been discovered, but I don’t think it’s been published yet. Please let me know if you know otherwise).
Poison-arrow frogs and toads
Finally, ‘core hyloids’ also include the poison-arrow frogs, or dendrobatids, and the toads, or bufonids. Studies disagree as to whether these two clades are close kin, or whether dendrobatids are closer to hylids. As mentioned earlier, the inclusion of dendrobatids within Hyloidea is now agreed upon, despite earlier ideas that they might be ranoids. Restricted to Central and South America, this clade of about 170 species is best known for its brightly coloured, highly toxic taxa. However, most dendrobatids are dull-coloured and non-toxic. In contrast to other anurans, dendrobatids possess a retroarticular process on the mandible and the degree of parental care that they exhibit is particularly complex, with egg-guarding and transport of tadpoles on the parent’s back being characteristic for the group. The taxonomy and phylogeny of dendrobatids is a very active area of research that I’m going to avoid entirely for now [adjacent image shows a Tinging frog Dendrobates tinctorius, often known as the Blue poison-arrow frog D. azureus].
Finally, another huge and highly successful hyloid clade is Bufonidae, the toads. Toads are edentulous hyloids characterised by parotoid glands (large poison glands on the back on the head) and a Bidder’s organ (rudimentary ovaries present in males. Don’t ask). They include over 480 (probably over 500) species. Toads are pretty much cosmopolitan, having spread naturally to all landmasses except the Australo-Papuan region (except Sulawesi), Madagascar and the polar regions. This distribution strongly suggests that they originated during the Upper Cretaceous, and this is supported by other evidence (Pramuk 2006, Pramuk et al. 2001, 2007), including by fossils that are referable to extant genera but date to the Palaeocene [image below shows ‘Toadzilla’, a big Cane toad captured in Australia. Previously Bufo marinus, under the new taxonomy the Cane toad is Rhinella marina].
A huge amount of work has been done on bufonid taxonomy, phylogeny and biogeography, and the largest genus in the group, Bufo (previously containing about 260 species) has recently been split up into multiple smaller genera (Frost et al. 2006). Again, in the interests of getting this series of articles finished I am going to force myself to ignore all of that for now. If toads really did originate in the Cretaceous, and if – as most phylogenies suggest – they are one of the youngest hyloid clades, then we have to conclude that most divergences within Hyloidea, and within Neobatrachia, occurred in the Mesozoic (Marjanovi? & Laurin 2007). At least some of the clades in question, toads among them, seem to have been very conservative during their history given that the oldest fossil forms aren’t that different from extant taxa.
What I’ve just done is a very superficial skim of hyloid diversity, but I hope you get the picture. For now we can say goodbye to this huge and fascinating group of anurans; there are just the ranoids left to go. They might be next. Might not.
Refs – –
Austin, J. D., Lougheed, S. C., Tanner, K., Chek, A. A., Bogart, J. P. & Boag, P. T. 2002. A molecular perspective on the evolutionary affinities of an enigmatic neotropical frog, Allophryne ruthveni. Zoological Journal of the Linnean Society 134, 335-346.
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.
Cisneros-Heredia, D. F. & Mcdiarmid, R. W. 2006. A new species of the genus Centrolene (Amphibia: Anura: Centrolenidae) from Ecuador with comments on the taxonomy and biogeography of glassfrogs. Zootaxa 1244, 1-32.
Darst, C. R. & Cannatella, D. C. 2004. Novel relationships among hyloid frogs inferred from 12S and 16S mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 31, 462-475.
Faivovich, J., Haddad, C. F. B., Garcia, P. C. A., Frost, D. R., Campbell, J. A. & Wheeler, W. C. 2005. Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bulletin of the American Museum of Natural History 294, 1-240.
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.
Hay, J. M., Ruvinsky, I., Hedges S. B. & Maxson L. R. 1995. Phylogenetic relationships of amphibian families inferred from DNA sequences of mitochondrial 12S and 16S ribosomal RNA genes. Molecular Phylogenetics and Evolution 12, 928-937.
Marjanovi?, D. & Laurin, M. 2007. Fossils, molecules, divergence times, and the origin of lissamphibians. Systematic Biology 56, 369-388.
Pramuk, J. B. 2006. Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zoological Journal of the Linnean Society 146, 407-452.
– ., Hass, C. A. & Hedges, S. B. 2001. Molecular phylogeny and biogeography of West Indian toads. Molecular Phylogenetics and Evolution 20, 294-301.
– ., Robertson, J. B., Sites, J. W. & Noonan, B. P. 2007. Around the world in 10 million years: biogeography of the nearly cosmopolitan true toads (Anura: Bufonidae). Global Ecology and Biogeography doi:10.1111/j.1466-8238.2007.00348.x
Ruvinsky, I. & Maxson, L. R. 1996. Phylogenetic relationships among bufonoid frogs (Anura: Neobatrachia) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 5, 533-547.
Wiens, J. J., Fetzner, J. W., Parkinson, C. L. & Reeder, T. W. 2005. Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology 54, 719-748.