One of the dirty little secrets of biology is that many groups of organisms have never been 'defined' in the phylogenetic sense: a group grows over time as people add new species to it, but they only do this because it 'feels' about right, not because there's any rigorous way of knowing whether those species really belong there or not. Many tetrapod groups - classic examples include Ranidae, Muscicapidae, Colubridae and Scincidae - lack characters that might allow their monophyly to be demonstrated, and modern studies show that various of their constituent members aren't more closely related to each other than they are to members of other groups. Some herpetologists argue that amphibians have been particularly affected by this sort of thing, given that their taxonomy and systematics have been (comparatively speaking) little studied, and that a form of social conservatism has often dominated decisions about taxonomy (Frost et al. 2006, p. 12). Despite the number of species involved, however, toads don't seem affected by this, in part because workers have often used what appears to be a synapomorphy when identifying an anuran as a toad: the presence of a Bidder's organ. Yes, here's another article on toads (aka bufonids) [adjacent image shows a few of the species conventionally lumped together within Bufo (from top to bottom): Common toad B. bufo (courtesy of Neil Phillips), Southern panther toad Amietophrynus pantherinus (from wikipedia), and Slender-legged toad Leptophryne borbonica (courtesy of John C. Murphy)].
Bidder's organ is weird. It's a small structure located close to the gonads: pinkish and with a granular surface texture, it occurs in both sexes and is composed of immature egg cells. Davis (1936) wrote that the Bidder's organ 'has long been the subject of speculation and debate, which was occasionally acrimonious and unscientific to an extraordinary degree', and (so far as I can tell) its origin, function and role in males remains unexplained [Bidder's organ in a male toad shown below, on the right. The organs of a non-bufonid hyloid is shown on the left for comparison. From Davis (1936)].
It has often been stated that the presence of a Bidder's organ is a bufonid synapomorphy. However, both Melanophryniscus (the South American redbelly toads) and the two Truebella species from Peru lack a Bidder's organ, and Melanophryniscus was found by Frost et al. (2006) and Pramuk et al. (2007) to be the sister-taxon to all other toads (it has previously (Cannatella 1986) been regarded as one of the 'atelopids', and close to Dendrophryniscus and Oreophrynella). This means that the presence of a Bidder's organ is actually a synapomorphy for the bufonid clade that includes all bufonids more derived than Melanophryniscus (and presumably Truebella); it is not characteristic for the group as a whole. Several other characters are also shared by the members of this clade (viz, all toads except Melanophryniscus and Truebella), including the production of egg strings and the presence of juxtaposed atlantal cotyles (Frost et al. 2006), but other characters exist that seem to be synapomorphies of Bufonidae as a whole. Toad larvae have a diastema in the papillation on the lower lip, and the lungs of larvae are either absent or rudimentary, for example (Frost et al. 2006).
The Bufo problem
By far the most problematic taxon in bufonid systematics is Bufo which, in 'traditional' classifications, is a virtually globally distributed genus that contains more than 250 species. As is so often the case with huge, traditionally recognised genera of this sort, Bufo of tradition (Bufo sensu lato from hereon) encompasses a pretty substantial degree of morphological disparity, the extremes of which easily 'look distinct enough' to belong to different genera. The giant Cane toad [shown here, from wikipedia], for example, is a thoroughly different beast from the tiny Lugh toad (conventionally B. lughensis) of eastern Africa (SVL less than 33 mm): they look about as different from one another as either does from any of the traditionally recognised non-Bufo bufonid genera.
It's becoming increasingly recognised that many of the genera (and other higher taxa) recognised 'traditionally' have been maintained because of convenience and social inertia, not because good (or any) evidence supports their monophyly. And Bufo s. l. is so morphologically diverse, and so unwieldy and massive, that anuran workers have long taken to referring to 'species groups' within the assemblage (about 40 such groups have been recognised). Alan Channing, in 1978, said that 'splitting a large cosmopolitan genus like Bufo can only aid our understanding of the group' (Channing 1978, p. 396), and from the 1980s onwards it began to be realised that Bufo s. l. is paraphyletic.
Phylogenetic studies have sounded the death knell for the retention of Bufo s. l.: it is evidently radically paraphyletic with respect to many other long recognised toad genera. Either we sink just about all recognised bufonid genera into Bufo (hardly a useful thing to do), or we split Bufo s. l. into its constituent clades, and name those clades accordingly. This latter process is now well underway, as we'll see in the following articles [adjacent image: Asian common toad Duttaphrynus melanostictus with unusually prominent cranial crests. Duttaphrynus is one of numerous genera conventionally included within Bufo s. l. Photo by Andrew Johnson ©, used with permission].
Coming next: SEX!
For previous articles in the toad series see...
And 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 - -
Cannatella, D. C. 1986. A new genus of bufonid (Anura) from South America, and phylogenetic relationships of the Neotropical genera. Herpetologica 42, 197-205.
Channing, A. 1978. A new bufonid genus (Amphibia: Anura) from Rhodesia. Herpetologica 34, 394-397.
Davis, D. D. 1936. The distribution of Bidder's organ in the Bufonidae. Zoological Series of Field Museum of Natural History 20, 115-125.
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.
Pramuk, J. B., 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.
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Interesting post. I'm now toying with the phrase: "useless as a bidder's organ on a male toad."
I want to see the skull of one of those Asian common toads. Any pictures that you know of?
I don't have photos of an individual with crests as big as the one shown above, but I do have pics of other crested toad skulls. Stay tuned - the fourth article in this series is all about cranial anatomy (bony and soft tissue).
I do encounter Asian common toads on a fairly regular basis, but I have never seen one with such distinctive crests!
Cool, looking forward to that.
I don't want to derail the comments too much but I've always had a question about synapomorphies and autapomorphies. Namely that I can recite the definitions but don't have an intuitive understanding of the difference between the 2.
When scientists are working on the phylogeny of a clade, aren't synapomorphies more telling than autapomorphies? A trait isn't useful in describing a clade if it is found only on a single terminal group right? Is it working out the difference between stem and crown groups?
I'm just having a hard time grasping the importance of autapomorphy within phylogenetic nomenclature.
These terms are relative: one clade has autapomorphies, and two or more clades have synapomorphies. The autapomorphies of Dinosauria are synapomorphies of Saurischia and Ornithischia.
Hennig liked terminology very much. It seems that he invented lots of it just for fun.
I see. I kinda of thought that but I was not sure if I was missing anything deeper. Thank you for clearing that up for me, David.
Now, back to the toads!
Regarding non-monophyly of families and genera, amphibians are in no way unique, perhaps not even unusual. To quote one of my favorite authors:
"There are a limited number of families [talkin' 'bout birds here] in which taxon sampling has been dense enough to determine the monophyly of genera. But in those families, paraphyly of genera has been shown to be frequent. The sparse data so far suggest that the larger a genus, and the more genera with the family, the more likely it is that non-monophyly will be found. Most often, as with families, paraphyly results from aberrant species being assigned their own genera. But there are additional cases without such clear causes. The greatest prevalence so far is in the most heavily sampled family with large genera, Picidae, in which at least six genera are non-monophyletic: Colaptes, Piculus, Picoides, Dendropicos, Veniliornis, and Picus (Weibel and Moore 2002; Webb and Moore 2005). Other examples include Eupodotis and Ardeotis in Otididae (Pitra et al. 2002; Broders et al. 2003), Columba and Streptopelia in Columbidae (Johnson and Clayton 1999; Johnson et al. 2001), Larus in Laridae (Pons et al. 2005), Tauraco in Musophagidae (Veron and Winney 2000), and Stercorarius in Stercorariidae (Braun and Brumfield 1998). We can expect many more non-monophyletic genera to come to light as species sampling increases."
[Skip ahead, brother]
"Genera of passerines are also not reliably monophyletic. While this is true also of non-passerines, there are certainly many more visible examples within passerines, and genera are more likely to be split into more widely separated pieces. In an informal poll of bird systematists I conducted at a recent meeting, I asked them to guess what percentage of passerine genera were nonmonophyletic (excluding monotypic genera). The modal answer was 'about half'. Of course the majority of genera have not been rigorously investigated so far, which requires sampling most or all the species in the genus plus many species outside it. A few examples should suffice. In addition to finding New World warblers polyphyletic, Lovette and Bermingham (2002) found six out of seven investigated genera with two or more sampled species to be nonmonophyletic; Driskell and Christidis (2003) found three non-monophyletic genera within Meliphagidae out of sixteen examined; Irestedt et al. (2004a) found three of four sampled genera of Thamnophilidae non-monophyletic, and monophyly of the fourth was not confirmed; and Irestedt et al. (2004b) found two of six sampled genera of Dendrocolaptidae non-monophyletic."
Harshman, J. 2007. Classification and phylogeny of birds. Pages 1-35 in Reproductive biology and phylogeny of birds (B. G. M. Jamieson, ed.) Science Publishers, Inc., Enfield, NH.
And now that we're starting to get those good species samples, lots more cases of generic polyphyly have come to light. See, for example, Chesser, R. T., F. K. Barker, and R. T. Brumfield. 2007. Fourfold polyphyly of the genus formerly known as Upucerthia, with notes on the systematics and evolution of the avian subfamily Furnariinae. Molecular Phylogenetics and Evolution 44:1320-1332.
Hope you'll mention the fantastic Van Bocxlaer et al. (2009) "Toad radiation reveals into-India dispersal as a source of endemism in the Western Ghats-Sri Lanka biodiversity hotspot" BMC Evol Biol. 9: 131. Taxonomy has just moved on so far since the 70s!
Loved the photos too. This is the first time I've seen Ansonia spinulifer live, and what a pretty beast.
Hi Julian - have you been following the comments on the previous article? Van Bocxlaer et al. (2009) has been much cited. Thanks John for lengthy comment - hey, that sounds like an interesting paper, I'm sure interested people* might like to email you for a pdf (hint hint).
* Not me, I have one.
Possibly stupid question: why is lumping everything into [i]Bufo[/i] a bad idea [i]a priori[/i]? There are genera that have way more species and more morphological disparity than Bufonidae...
Hi William. There are several answers.
1) Is it useful - in terms of communication - to have enormous genera containing hundreds of species? Arguably not, as amphibian specialists are always having to devise 'species groups' and 'superspecies' when they need to explain which chunk of Bufo sensu lato they're referring to. One can also make the argument that the recognition of separate genera helps people to better appreciate such things as endemism, conservation priority and diversity: listing a distinctive species as 'just another Bufo' (rather than as a distinct genus-level taxon) can be damaging.
2) Does it reflect phylogeny? Definitely not, as Bufo sensu lato is scattered about the bufonid tree, and does not form a discrete clade separate from all the other named genera. The retention of all these species in one super-huge genus results from conservatism and social inertia, nothing more. Note also that we tend to base stories on the classifications we adopt. The 'Bufo story' is that a big, conservative genus sat around for millions of years without doing much except for developing new, much-alike species. But if that one 'genus' becomes split into 30 or so, the 'story' of the whole clade becomes different.
3) Does it reflect morphological disparity? Are all members of Bufo sensu lato clearly more alike than they are to other putative genera? No, Bufo sensu lato encompasses a huge amount of morphological (and behavioural, ecological and genetic) variation: way more than is present in many other 'genera'. People are clearly inconsistent with regard to what constitutes a genus, but we should try and aim for some sort of consistency.
Hope this helps, sorry if it seems rambling. The tag for italics is 'em' in <> brackets.
John:
It would also be interesting to have an estimate of how much cryptic species-level diversity there is within those traditionally recognised monotypic genera.
4) The clade that consists of the last common ancestor of all traditional Bufo species plus all its descendants already has a name: Bufonidae. What good would it do to turn Bufo and Bufonidae into synonyms?
Technically, <em> is for "emphasis", and your browser gets to decide what it makes of that. Probably without exception, they choose italics⦠but if you want to make really sure italics come out, use <i>, which has the added advantage of being shorter. Obviously, <i> is more appropriate for biological nomenclature than <em>!
Same for bold: <strong> vs <b>.
Some people claim that <i> and <b> are somehow "deprecated" or something. They're full of shit.
BTW, HTML tags have to be closed with a slash: <i>this here in italics</i>.
It would only slightly exaggerate some coding advice I was recently given to say that you should (when writing a webpage, doesn't work for ScienceBlog comments) define a span="nomen" or something like that to apply to all scientific names in your text, in case you suddenly decide that, after all, you'd rather have them in small-caps Fraktur than in italics.
(As you may guess, I don't agree with this piece of advice.)
David:
That's not quite correct; AFAIK, the contents of Bufo sensu lato have never been entirely synonymous with Bufonidae. Traditionally, pretty much every worker has recognised a few other bufonid genera as well. For example, Tihen (1960), whose paper might be considered a representative study from the Bad Old Days*, recognises nine other genera besides Bufo in his Bufonidae sensu stricto (Tihen is ambiguous regarding the inclusion of a few other genera, including the very speciose Atelopus, in Bufonidae).
* If you have access to the JSTOR archives, and if you want to see just how bad those days were, I suggest you have a look at Figure 1 in Tihen's paper.
I should add that I'm not personally of the opinion that the traditional super-Bufo genus should be retained; I'm only pointing out that not even the most reactionary traditionalist would have a historical precedent for lumping all toads into Bufo.
Reference:
Tihen, J.A. 1960. Two new genera of African bufonids, with remarks on the phylogeny of related genera. Copeia 1960, 225-233.
The ICZN, the ICBN, probably the ICNB, and the Phylocode (ICPN) all recommend italics, however.
That's not what I mean -- I mean that, to the best of my knowledge, Bufo sensu lato is paraphyletic to the entire rest of Bufonidae, so if we want to make it monophyletic by sinking its descendant genera into it (as suggested in comment 12), it becomes a synonym of Bufonidae. I'm not talking about historical precedent.
Anyway, we seem to agree that the remaining alternative for making Bufo monophyletic is to do what Frost et al. (2006) did: to restrict it to the former species group Bufo (bufo).
Oh, OK, that makes sense. I can definitely see the conservation benefits of highlighting the diversity and disparity that can get hidden under 'just one genus'.
I was just thinking that if Bufonidae (and other similar groups) was treated as a single genus, further phylogenetic discoveries would require fewer nomenclatural changes.
And I suppose what I was essentially asking is, given that we're trying for a more consistent definition of how much disparity a 'genus' includes (which I do agree with), what a priori reason is there to choose the big-mammals-and-birds model of tiny genera of nearly-identical species (e.g. Panthera, Canis) rather than the insects-and-plants model of big genera including more disparity?
Hi William. Your closing question is a really good one, but not one that I can answer. But I'll try.
We are indeed striving for some sort of consistency across Tetrapoda, but I'm well aware of the fact that tetrapod diversity is a bit of a joke compared to that of some other clades. The most obvious answer is that the concept of the genus is very different across different clades, and that entomologists and botanists have an extraordinarily broad version of what a genus should be. By tetrapod standards, those biologists are 'wrong', but if that's what works for them, well, then that's what works. Personally, I do think that they're wrong, and that their 'genera' are horribly massive... but this is a tetrapodocentric view :)
Are we striving for consistency? I've never noticed.
Anyway, it's probably important to note that the ICZN limits the number of ranks between genus and species to subgenus and "group of species". The botanists don't have that restriction, so they use at least the ranks of section and subsection somewhere between genus and species, something zoologists are not allowed to do. So, botanists can pack more diversity into a genus and still talk about that diversity than zoologists can.
OT: William, I'll bet you're used to posting on those forums that use [] brackets instead of html brackets. It's so easy to forget to switch--don't feel like the lone ranger.
Darren--just another lurker, here, enjoying this series immensely.