Don't worry about the small size of that cladogram; a larger version is included below. Western leopard toad photo by Serban Proches, Common European toad by Accipiter.

One of my long-term goals at Tet Zoo has been to complete my series of articles on the toads of the world actually, this started out as a short-term goal, but it ended up taking rather longer than expected. This enormous, near-globally distributed anuran clade (properly termed Bufonidae) encompasses incredible variation and a huge amount of work has been published on the species involved, on their behaviour and biology, and on how they might be related to one another.

As youll know if youve read any of the previous parts of the series (all of which until now have been published at Tet Zoo ver 2: links below), it seems that crown-toads originated in South America* during the Cretaceous or early Cenozoic. All basal lineages within crown-Bufonidae consist of relatively small species that are poor at dispersing, produce small egg clutches and lack the large parotoid glands otherwise so typical of this clade. These primitive toads have sometimes been grouped together in a non-monophyletic assemblage termed Atelopinae.

* It seems that the earliest toads inhabited western Gondwana prior to the splitting of South America from Antartica (an event that didnt fully occur until the Oligocene). It might therefore be that the very first member of Bufonidae - even the first members of crown-Bufonidae - lived on Antartica. A crown group is the group delimited by extant species; the clade that includes the crown as well as its close fossil relatives is the total group.

At some stage during the Eocene, what Ive termed ver 2 bufonids evolved. In contrast to those earlier lineages, these are typically large to very large toads that produce large to stupendously large clutches, have exotrophous larvae (viz, larvae that feed from the environment, rather than rely on a maternally provided food source), and possess large to enormous parotoid glands. Combined, these features make ver 2 bufonids supremely successful colonisers of new areas. Van Bocxlaer et al. (2010) wrote of them as exhibiting a range-expansion phenotype and described how the evolution of these new features initiated the episode of global colonization and triggered the major radiation of toads (p. 679).

The evolution of the range-expansion phenotype in toads (the key evolutionary events occurred within the part of the tree marked by the grey box), as depicted by Van Bocxlaer et al. (2010).

In the previous parts of this series, I got through all the atelopine toads and then looked at the South American and Caribbean members of the ver 2 clades Rhaebo and Peltophryne. These taxa seem to be outside the enormous clade that includes all the remaining toads. So, what next? Several phylogenetic studies have found an assemblage of African toads to occupy the part of the tree between Rhaebo and Peltophryne and the generally more familiar Old World and American toad lineages Bufo (sensu stricto!), Anaxyrus (Common American toad and kin), Incilius (Central American toads) and Rhinella (the Cane toad and kin). It therefore seems appropriate to consider these African groups next.

Turning part of the tree on its head

However in the time that Ive been writing this series of articles, several major analyses of toad phylogeny and biogeography have appeared. You might say that toad phylogeny became rightfully high profile in 2010, thanks in part to Ines Van Bocxlaer et al.s excellent paper in Science* (Van Bocxlaer et al. 2010). While broadly agreeing on several major aspects of tree shape, the different studies on toad pnhylogeny differ radically in some important respects. This makes it difficult to make generalisations about the position of particular taxa within the tree.

* In saying this I certainly mean no disrespect to the many other authors who have published on toad phylogeny, sometimes in such august publications as Zoological Journal of the Linnean Society, Molecular Biology and Evolution, Zootaxa and Evolution.

Highly simplified toad cladogram (with some hypothesised biogeographic events marked at appropriate places), mostly based on Pramuk (2006) and Pramuk et al. (2008).

Several phylogenies find New World toad clades like Anaxyrus, Incilius and Rhinella to be nested within an Old World clade that includes Bufo (sensu stricto) as well as many African and Eurasian toad lineages. Its generally agreed nowadays that toads originated in the Americas (see caveat above) and later spread into the Old World, but in the scenario resulting from this phylogeny [see above], one Old World lineage (leading to Anaxyrus, Incilius and Rhinella) later migrated back into the Americas, presumably during the Paleogene (Pramuk et al. 2008). In this model, Old World toads are paraphyletic with respect to a young American clade.

The newer phylogenies recovered by Van Bocxlaer et al. (2009, 2010) switch this relationship, however, and find Anaxyrus, Incilius and Rhinella to be outside the clade that includes all Old World toads. In this scenario resulting from this phylogeny, the ancestors of Anaxyrus, Incilius and Rhinella never left the Americas, and Old World toads are monophyletic, not paraphyletic with respect to Anaxyrus, Incilius and Rhinella.

Highly simplified competing toad cladogram (again, with some hypothesised biogeographic events marked at appropriate places), this time mostly based on Van Bocxlaer et al. (2010).

Well come back to this issue again later on, but for now Im going to stick with the way in which the text was originally arranged. That is, well get through the various African and many Eurasian lineages before getting to Rhinella and so on. Time, then, to look at the various African toads. As well see, many of these are peculiar, poorly known little animals, often of uncertain phylogenetic placement and conservation status. If youre blogging about them, theres the added complication that theyre obscure enough to be rarely illustrated or photographed

Time to deal with the Africans

At least some African toads seem to belong to an endemic African clade (as yet unnamed) (Frost et al. 2006, Van Bocxlaer et al. 2009, 2010). For convenience, Ill refer to it from hereon as the African clade. Frost et al. (2006) and Pramuk et al. (2008) found the African clade to be deeply nested within Bufonidae, close to Bufo sensu stricto and to the young American clade, while Van Bocxlaer et al. (2009, 2010) found it to be the sister-group to all remaining Old World lineages.

Tadpole of the Chirinda forest toad Mertensophryne anotis. Yes, it has a freakin' ring on its head. From Channing (1978).

The African clade consists of several toad lineages traditionally included in Bufo but recently given their own names for the usual reason (this being that they dont group close to Bufo sensu stricto in phylogenies). These are Amietophrynus Frost et al., 2006, Capensibufo Grandison, 1980, Vandijkophrynus Frost et al., 2006 and Mertensophryne Tihen, 1960 (and perhaps Schismaderma Smith, 1849 too). Some of them are very odd (check out the tadpole shown in the adjacent image).

Well be looking at them in the next article.

For previous articles in the Tet Zoo toads series see...

For previous articles on hyloid anurans see...

Refs - -

Channing, A. 1978. A new bufonid genus (Amphibia: Anura) from Rhodesia. Herpetologica 34, 394-397.

Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De S, 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.

Pramuk, J. (2006). Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence Zoological Journal of the Linnean Society, 146 (3), 407-452 DOI: 10.1111/j.1096-3642.2006.00212.x

- ., Robertson, J. B., Sites, J. W. & Noonan, B. P. 2008. Around the world in 10 million years: biogeography of the nearly cosmopolitan true toads (Anura: Bufonidae). Global Ecology and Biogeography 17, 72-83.

Van Bocxlaer, I., Biju, S. D., Loader, S. P. & Bossuyt, F. 2009. Toad radiation reveals into-India dispersal as a source of endemism in the Wester Ghats-Sri Lanka biodiversity hotspot. BMC Evolutionary Biology 2009, 9:131 doi:10.1186/1471-2148-9-131

- ., Loader, S. P., Roelants, K., Biju, S. D., Menegon, M. & Bossuyt, F. 2010. Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science 327, 679-662.