Once more, we return to those wonderful, phenomenally successful, charismatic beasts.... the toads. As you'll know if you've read the previous articles in the toads series, it seems that most basal divergences within crown-Bufonidae happened in South America. So far as we can tell right now, crown-toads are ancestrally South American, and all of their early history happened on this continent [Rhaebo blombergi image below from here].
All of the basal toads looked at so far - the relatively small, slender-limbed, shallow-snouted members of the clades Melanophrynicus, Atelopus, Osornophryne, Dendrophryniscus, Truebella, Andinophryne, Oreophrynella and Frostius - look rather different from the 'typical' stout-bodied toads that we're more familiar with. Indeed, some authors have suggested that most or all of these 'basal toads' should be grouped together in a toad subfamily termed Atelopinae (recent phylogenetic studies generally agree that no such monophyletic entity exists, however). Having gotten the 'atelopines' out of the way, we now start looking at the more 'typical' toads. As we'll see below (and later), toads in this enormous clade are different in many important respects from 'atelopines' and might be regarded as 'Bufonidae ver 2'.
Introducing the 'Bufo guttatus group'
A group of nine (as of August 2010) South American toads traditionally included in Bufo and known as the 'Bufo guttatus group'* share a number of morphological characters. These include absence of cephalic crests (for a discussion of cephalic crests in toads see the article on skulls, crests, snouts and giant poison glands), the production of yellowish-orange skin secretions, hypertrophied testes (!!) and an omosternum (Frost et al. 2006). The omosternum is an anteriorly projecting component of the pectoral girdle, located along the midline, anterior to the clavicles. A few other toads have an omosternum (including Nectophrynoides, Werneria, Capensibufo and species in the Incilius valliceps group), but none of them seem closely related to the 'Bufo guttatus group' [image below, from Kaplan (2004), shows the pectoral girdle (in ventral view) of a typical toad** (at left) - without omosternum - compared to an omosternum-bearing ranid frog at right (omosternum is marked 'o'). cl = clavicle; co = coracoid; e = epicoracoid; p = procoracoid; s - sternum].
* And sometimes as Cope toads (Frost 2009), presumably because Cope published the name Rhaebo.
** While labelled here as Bufo woodhousii, remember that the deconstruction of Bufo sensu lato requires that we use the name Anaxyrus woodhousii for this North American species. See The resurrection of Anaxyrus.
All species within this group have short, rounded snouts and broad skulls. Molecular studies have found them to be outside the clade that includes the Eurasian and American toads traditionally included in Bufo (Pauly et al. 2004, Pramuk 2006, Pramuk et al. 2008, Van Bocxlaer et al. 2009): this seems to confirm previous suggestions that the members of the 'Bufo guttatus group' are an ancient lineage that diverged from other toads early on in the Cenozoic (as in, in the Eocene).
Recognising the 'Bufo guttatus group' as a distinct lineage well removed from Bufo proper means that a new generic name is needed: Rhaebo Cope, 1862 is available and was used for these toads by Frost et al. (2006). Rhaebo might be particularly close to Peltophryne (see below), or it might be the sister-taxon to Andinophryne [the latter taxon was previously discussed here]. In fact, Mueses-Cisneros (2009) named the new Venezuelan species R. andinophrynoides on account of a strong similarity with Andinophryne [photo of R. guttatus used above from here] [R. caeruleostictus from Ecuador shown below, from Hoogmoed (1989). Scale bar = 1 mm].
While most Rhaebo species are 'average' in size for a toad (SVLs = approximately 70-80 mm), the Colombian giant toad or Blomberg's toad R. blombergi [shown at very top] of Colombia and Ecuador is gigantic, with some specimens exceeding 240 mm in length. Some authors say that Blomberg's toad is the largest known toad, but this isn't right given that a few exceptional Cane toads have exceeded 300 mm SVL (unless there are some record-holding Blomberg's toads that I haven't read about). Despite its size, Blomberg's toad was only named in 1951. John Funkhouse learnt of this species from Rolf Blomberg in 1950 (Blomberg had heard about it from local Ecuadorian people), and specifically went out in search of it. Obviously, he was successful in finding it (Shuker 2002).
West Indian toads
Eleven toad species from the West Indies were traditionally included in Bufo sensu lato and known as the 'Bufo peltocephalus group'. These species are ecologically diverse, with some inhabiting dry scrubland and others being denizens of well-watered, forested habitats. They're morphologically diverse too, with some being small (28 mm SVL) with weakly ossified, open-plan skulls, and others being large (190 mm SVL), with heavily ossified, box-like skulls [for pictures see skulls, crests, snouts and giant poison glands]. As Pramuk (2002) noted, marked morphological disparity among close relatives is often commoner in island-endemic amphibians and reptiles than it is in their mainland relatives.
Pregill (1981) was one of the first authors to properly argue that these toads formed a clade: a clade that could easily be distinguished from the other members of Bufo sensu lato. One of the strangest features of these toads is that their maxillae have extended anteriorly to fill in the space normally occupied by the premaxillae along the midline of the upper jaw. The premaxillae themselves have been displayed dorsoposteriorly (Pramuk 2000, 2002). Pregill (1981) argued that the old generic name Peltophryne Fitzinger, 1843 should be resurrected for these animals [adjacent photo of Puerto Rican crested toad P. lemur from wikipedia].
Phylogenetic work indicates that the divergence between Peltophryne and other bufonids happened early on within bufonid evolution, probably early in the Cenozoic (Pramuk 2006, Pramuk et al. 2008, Van Bocxlaer et al. 2010). Rhaebo may be equally old, and in fact Peltophryne and Rhaebo may be sister-taxa (Van Bocxlaer et al. 2010). An alternative hypothesis is that Peltophryne belongs in a clade with Pseudepidalea (the Green toad and kin), the Afro-Asian Duttaphrynus species and Schismaderma (the African red toads) (Frost et al. 2006). Peltophryne may first have colonised the Caribbean region during the Paleocene or Eocene, and apparently prior to the formation of the modern Caribbean islands.
While at least some Peltophryne species are terrestrial, burrowing toads (they use their heavily ossified heads to seal their burrow entrances), the Cuban long-nosed toad P. longinasus is unusual in being semi-arboreal (Pramuk 2002).
Bufonidae ver 2
There's one more thing worth saying about Rhaebo and Peltophryne, and in fact it makes them rather significant. Most of the toads we've looked at so far have been relatively small anurans that produce tiny egg clutches and lack parotoid glands. In contrast, Rhaebo and Peltophryne are among the oldest members of the clade that I referred to above as 'Bufonidae ver 2': toads that are large to very large, 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 [diagram below - from Van Bocxlaer et al. (2010) - shows how the appearance of several key traits triggered the evolution of the 'optimal range-expansion phenotype'. The major global expansion of 'ver 2' toads then followed].
We don't know why toads evolved these novel features, but - in combination - they have allowed 'ver 2' toads to be supreme survivors, colonists and dispersers (Van Bocxlaer et al. 2010). Indeed, as discussed recently by Van Bocxlaer et al. (2010) - one of several new studies which shows how sexy toads are as research objects - 'ver 2' toads exhibit a 'range-expansion phenotype' that allows some species to be notoriously adaptive and exceptionally good at expanding their ranges. In very strong contrast, 'atelopine' toads generally have small ranges and are extremely vulnerable to extinction. We'll be coming back to this story several times again. And, on that note, we'll be coming back to toads in general some time soon - there is still a lot to get through.
For previous articles in the Tet Zoo toads series see...
- Toadtastic - the invasion begins!
- Bidder's organ and the holy quest for synapomorphies
- Our sex lives in words and pictures (or, On the reproductive biology of the Bufonidae)
- Skulls, crests, snouts and giant poison glands: the heads of toads
- Toads of the world: first, (some) toads of the north
- The Natterjack, its life and times
- The resurrection of Anaxyrus
- South America, land of toads, part I: harlequins, redbellies and plump toads
- South America, land of toads part II: tree toads, Truebella, Frostius... oh, and did I mention the COMMUNAL NESTS?
For previous articles on hyloid anurans see...
- Britain's lost tree frogs: sigh, not another 'neglected native'
- Ghost frogs, hyloids, arcifery.. what more could you want?
- Green-boned glass frogs, monkey frogs, toothless toads
- It's the Helmeted water toad!
- Horn-headed biting frogs and pouches and false teeth
- More wide-mouthed South American horned frogs
- We need MORE FROGS
Refs - -
Frost, D. R. 2009. Amphibian Species of the World: an Online Reference. Version 5.3 (12 February, 2009). Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/ American Museum of Natural History, New York, USA.
- ., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De SÃ¡, 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.
Hoogmoed, M. S. 1989. On the identity of some toads of the genus Bufo from Western Ecuador, with additional remarks on Andinophryne colomai Hoogmoed, 1985 (Amphibia: Anura: Bufonidae). Zool. Verh. Leiden 250, 1-32.
Kaplan, M. 2004. Evaluation and redefinition of the states of anuran pectoral girdle architecture. Herpetologica 60, 84-97.
Mueses-Cisneros, J. J. 2009. Rhaebo haematiticus (Cope 1862): un complejo de especies. Con redescripciÃ³ def Rhaebo hypomelas (Boulenger 1913) y descripciÃ³n de una nueva especie. Herpetotropicos. MÃ©rida, Venezuela 5, 29-48.
Pramuk, J. B. 2000. Prenasal bones and snout morphology in West Indian bufonids and the Bufo granulosus species group. Journal of Herpetology 34, 334-340.
- . 2002. Combined evidence and cladistic relationships of West Indian toads (Anura: Bufonidae). Herpetological Monographs 16, 121-151.
- . 2006. Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zoological Journal of the Linnean Society 146, 407-452.
- ., 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.
Pregill, G. 1981. Cranial morphology and the evolution of West Indian toads (Salientia: Bufonidae): resurrection of the genus Peltophryne Fitzinger. Copeia 1981, 273-285.
Shuker, K. P. N. 2002. The New Zoo. House of Stratus, Thirsk, North Yorkshire.
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
Van Bocxlaer I, Loader SP, Roelants K, Biju SD, Menegon M, & Bossuyt F (2010). Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science (New York, N.Y.), 327 (5966), 679-82 PMID: 20133569
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More pictures here (they were taken by Rolf Blomberg himself, I believe).
Thanks :) I saw these while looking for images but didn't use them because of the scary copyright notice. Let me say again: I really struggle to find good images for these articles, and when I find good photos of obscure herps they are, invariably, fiercely protected by copyright. Am always very grateful to people who allow use of their images for free.
Based on molecular evidence, right?
Yes, all based on hypotheses of when the lineage diverged from the rest of Bufonidae. No fossils (as far as I know). Check Pramuk's papers if you can (I have pdfs if you need them), lots of discussion therein.
As local representative of the PhyloPolice(TM), let me present a warning concerning your use of the terms "crown-Bufonidae" and "ancient lineage". Strictly speaking, if there are any species you consider bufonids, but outside crown-Bufonidae, they must be extinct. I've seen "crown" used to refer to a "derived" or "typical" subclade, and I'm suspicious that you are doing that here. A crown group is a node-based clade whose reference taxa are extant, as opposed to a total group, a branch-based clade consisting of the crown group and any number of extinct stem-groups. So there.
As for "ancient lineage", I repeat the tired refrain that all lineages originating from the same node (divergence event) are equally ancient. You don't know how old Rhaebo and Peltophryne are; at most you know the date at which their lineages and other toads diverged from each other, and the later date at which the lineages whose terminal members two sampled species of a genus diverged from each other. (If we want to discuss extension of species concepts through deep time, that's another rant.)
But I am learning quite a bit about toads. Keep up the good work.
Thanks, local PhyloPolice rep, your comments are duly noted. However...
-- in referring to 'crown-bufonids', I felt that I needed to differentiate between the clade that truly is the crown (viz, the clade subtended by all extant taxa) and 'Bufonidae' of more relaxed, traditional usage (viz, the total group). When I say that 'crown-bufonids are ancestrally South American', I do specifically mean the bufonid crown, as I'm leaving open the option that there are members of the total group that inhabited, say, Antarctica. A few fossils - traditionally regarded as part of Bufonidae - could indeed be outside of the bufonid crown, hence the need to refer specifically to crown-Bufonidae. In other words, I have consistently tried to use 'crown' in the correct manner. I hope this makes sense.
-- as for 'ancient lineage'... again, I see your point (and yes, this is sounding familiar :) ), but I also see the need to sometimes refer to 'genus-level' groups that diverged a long, long time ago relative to others. Granted, the (say) Rhaebo lineage and the 'other ver 2 bufonids' lineage are equally old, but Rhaebo has apparently been going it alone since the Late Eocene, while such genera as (say) Duttaphryne only diverged in the Miocene. Hmm. I suppose the best excuse is that I often need to use a kind of short-hand when expressing these concepts. Forgiveness, master!
I apologize for doubting you on "crown-Bufonidae". Be assured that the citation has been expunged from your record.
As for "ancient lineage" etc., I know you're aware that ranks are arbitrary and that there's nothing special about a clade just because it has a lot of species (or, conversely, because its sister group has a lot). It's so easy to fall into the trap of "few species = primitive" that I think we have to go to extra lengths to avoid the implication. How annoying is it, for example, to see the constant claims that "sharks/crocodiles/whatever have been around since before the dinosaurs" as if that's a meaningful or interesting statement? Nobody would consider it interesting to say "mammals have been around since before Sceloporus", but the other statements are no less vacuous. So let's keep searching for alternative statements that say what you really mean without false implications.
Not sure what's wrong with "sharks have been around since before the dinosaurs"? The Sceloporus version is less interesting chiefly because most people haven't got a clue how old Sceloporus is, or even what it is, unlike dinosaurs.
Alternatively, the molecular dating analysis may have been calibrated with too few internal calibration points with maximum ages.
Which is to say, I'd appreciate the pdf. :-)
See what I mean? Pernicious. You're assuming a rough equivalence between "shark" and "dinosaur". Of course in order to make that true you have to enlarge the meaning of "shark" way beyond the crown group. But why aren't you also enlarging "dinosaur" to include, say, all tetrapods or all sarcopyterygians or (true equivalent) all osteichthyans? The implication behind it is that sharks are primitive, and that modern sharks are just like Devonian sharks. Living fossils, and all that. Which just isn't true.
Now, if you don't like Sceloporus (though I don't see why not, perfectly good genus), how about "Mammals are older than toads"? Does that suddenly inject fascination?
I don't see it. "Archosaurs were around long before my grandmother was born" compares two very different ranks or categories, but it's a factual sentence nonetheless.
So much rancor! Harshman must be from a harsh clan. But science needs rectitude police to keep it honest. Rock on, sir.
"Mammals are older than toads" does inject fascination for me. Heck, any discussion of paleontology that compares when this and that happened intrigues me. For example, modern birds radiated from a small number of species that survived the K-T event. Could we derive a hypothetical set of ur-birds from examination of the fossils and genetics? So cool. And mammals are older than toads - Yeah, that's interesting. What lineages of mammals and lissamphibia crossed that K-T boundary before toads emerged? Later, what mammals would have lived with early toads?
I just like to imagine the world of the past, and knowing what lived at the same time as what else helps paint that picture. I could waste a lot of time on that tolweb and wikipedia is what I'm saying.
Unfortunately you're right. The oldest Peltophryne fossils known are from Pleistocene cave deposits.
Please do send them. thanks!
If I did I wouldn't have asked.
Only to the extent they both have ages.
Dinosauria is not a crown group, so comparing to the crown group of sharks would seem no less abitrary than to a more inclusive group.
Saying that Osteichthyes is the "true equivalent" presumably presumes that Osteichthyes is a total group and that "sharks" is the total group of Chondrichthyes? That would make chimaeroids "sharks", which seems odd. (If the shark, excl chimaeroids and kin, total group has a dinosaurian equivalent, I guess it's Pan-Aves. But saying that taxa are equivalent doesn't seem very meaningful in the first place.)
Given that this concern doesn't seem to work in reverse - if I say Dinosauria is older than Neoselachii, you're not going to accuse me of implying that chickens are living fossils, are you? - I'm not convinced comparisons like this are the problem.
That sharks is older than dinosaurs tells me sharks arose in the Triassic at the latest. That mammals are older than Scelopours tells me nothing, because I don't know how old Sceloporus is.
I would point out (in a respectful, yet amused, fashion) that you yourself have indulged in perniciousness in the recent past. The claim that "Archaeopteryx is a bird" is one that I know that you've defended (and so have I), but these days Archaeopteryx is placed well outside the crown group.
Certainly if one is making claims about sharks and dinosaurs, or any other group, it's helpful to be specific about exactly which group one is referring to, and the meanings of "sharks", "dinosaurs", or even "crocodiles" can be vague. But even if one is explicit with one's definitions, I don't see how there's an implication of equivalence.
As for the statement that "Mammals are older than toads", it does indeed inject fascination. In fact, it mainlines it.
Frankly, I'm a bit suspicious of the usefulness of the "crown group" concept. Suppose that next year it is discovered that the Miocene Mammaliform from New Zealand (which seems to have been outside the Ornithorhynchus+Mus clade) has survived to the present somewhere on the South Island. We''ll all have to remember the 2011 discovery date in order to interpret references to "Crown group mammals."
I am not familiar with the details, so can someone please explain: What are the evolutionary "inventions" that have allowed toads to compete successfully with other amphibians (mainly frogs) and spread beyond their place of origin?
And what limitations do toads have, that have hindered them to completely out-compete non-toad amphibians and render them extinct?
Or is the whole thing stochastic, with one species having little or no advantage over the other?
I'm surprised that anyone finds "mammals are older than toads" to be a fascinating statement. But if so, you could certainly come up with millions of fascinating statements with great ease and keep yourself amused for hours. Crabs are older than bison. Echinoids are older than beetles. And so on.
Now, the point of "sharks are older than dinosaurs" is always to impress us with their great antiquity and their status as living fossils, unchanged since the Devonian. Supposedly. And the idea that that was the point was in fact my point. If you disagree, find such a statement and see what use is made of it. Was I in fact wrong?
Shelton: Actually, the number of bird lineages crossing the K-T boundary is a matter of some debate, and it seems to be going up. Based on Vegavis alone, there's a minimum of 6, and Anseriformes is not one of the oldest divergences.
Andreas: Nobody ever says "Dinosauria is older than Neoselachii", for the exact reason that nobody wants to claim that chickens are living fossils, which is what the point of such a statement would be.
Augray: I hope I have never said that "bird" needs to be attached to the crown group. "Aves", yes. "Bird", no. I hope I've always said that the node we call "bird" has never been well defined. I like to apply it to anything with a flying ancestor whose flight is homologous to flight in Passer domesticus. I also assume that Archaeopteryx fits that requirement, but I'm not sure about Microraptor. Anyway, you mistake just what I'm complaining about, which is the assumptions around "old" and "primitive".
Allen: One can imagine all manner of scenarios, but how likely are they? We can probably discount the risk of a living triconodont at this point. The advantage of crown groups is that we can know a whole lot more about their roots than about the roots of non-crown groups. We can even try to reconstruct their genomes. This makes them easier to define and diagnose.
Sorry if I've drawn any attention away from toads. Phylocop is a tough job.
I've seen a number of statements in popular sources to the effect that "mammals are older/younger than dinosaurs" (under various definitions of "Mammalia"). I seriously doubt the authors were trying to imply that people or chickens are living fossils.
Unknown. It was found in a trichotomy with Ornithorhynchus and Mus. We need more fossils.
Not under the PhyloCode, which will encourage people to make explicit what they mean by "crown-group" when they define a name, and which will provide a default meaning in case authors don't provide any.
Some are mentioned in the post: everything to do with r-strategy -- large clutch size, larvae that feed from the environment instead of living off yolk --, plus large size (which makes all distances shrink).
David, I know I should just go to the Phylocode draft you once linked to and look it up for myself, but could you give a one to four sentence explanation of how Phylocode handles my worry? With "crown as known in 2010 Mammalia" it's fairly easy (even I managed!) to name two internal specifiers that will do the trick, but with clades whose internal structure is less obvious... How many internal specifiers would you want before you were confident you had spanned crown Afrotheria?
You mean toads aren't living fossils? But they're so gnarly looking!
One alternative formulation for crown clades that I've had pointed out to me would be e.g. "the most recent common ancestor of all living species closer to Homo sapiens than Lacerta viridis, Passer domesticus or Chelonia mydas and its descendants" for crown Mammalia.
From the PhyloCode's point of view, what's a 'living species', anyway? I am assuming (correct me if I'm wrong) that recently extinct taxa qualify as 'living', but exactly how recently extinct can they be? Does any species that survived into the Holocene qualify? Or is there some specific cutoff date (e.g., 1758)?
See David's comment at #20. I believe (I'm not closely connected to the PhyloCode discussion) that the default meaning is the species known to be living at the time of the definition's publication (so it doesn't include any taxa living but not yet discovered such as the 'surviving eutriconodont' example above).
Let me re-phrase my question by using an actual example: The thylacine (and the 'family' Thylacinidae, for that matter) went extinct* many years before phylogenetic nomenclature was implemented or even thought of, and was no longer alive at the time when the first phylogenetic definitions of Dasyuromorphia were published. Thus, is Thylacinus cynocephalus a crown taxon or not, as far as the PhyloCode is concerned?
* As the recent 'Rilla Martin's creature' thread here on Tet Zoo demonstrates, there are also people who do not believe that the thylacine is extinct. But that's another can of worms.
As I keep saying, the entire PhyloCode can be read in one good evening. Why don't all y'all just sit down and do it? :-)
Art. 5 explains what "publication date" means.
Thank you, that was (more) helpful (than i deserved).
9.5 is very clear, but I think has the potential to be annoying. It means that, in interpreting older literature, we have to remember exactly when relevant species became extinct. Fictitious example, courtesy of Dartian: suppose Phylocode had been brought in in 1900 and you were now consulting a 1938 paper containing a reference to "Crown Dasyuromorpha." Do you want to have to remember exactly when the last captive Thylacine carked it in order to figure out whether the crown group includes Thylacinidae?
So my worry is that use of the crown group concept may, in practice, make the scientific literature less transparent.
(Or do we assume that information technology will make retrieval of such information too trivial a matter to worry about?)
And yet 'basal' taxa really are disproportionately important in phylogenetics, because their characters have a large effect in reconstructing those of ancestral nodes, and hence relationships to outgroups. A newly discovered species of Rana or Bufo sensu stricto, however old or feakishly derived, tells us less about anuran history and relationships than would a new species of Leiopelma, Ascaphus or Triadobatrachus.