For those who work primarily in the West Indies, it can be difficult to imagine a lizard fauna dominated by anything other than anoles. However, if you’re interested in learning more about lizard communities that don’t include anoles, no book fits the bill better than L. Lee Grismer’s recent monograph on the Lizards of Peninsular Malaysia, Singapore and their Adjacent Archipelagos. Grismer takes readers on a tour of Peninsular Malaysia’s impressive lizard diversity, with species-by-species accounts that include morphological diagnoses, notes on coloration in life and among sexes, dot maps, and detailed notes on each species’ natural history. Grismer is the first to comprehensively review Peninsular Malaysia’s 128 lizard species, and his book represents the “first time the entire distribution of this fauna has been precisely mapped.” Of course, Grismer’s book is also chalk full of spectacular photographs, including many of Grismer’s trademark photos of animals in their natural habitat.
Map from Malaysian Bat Education Adventure: http://www.ttu-mbea.org/krau-wildlife-reserve/
Sandwiched between Thailand and Myanmar to the north and Indonesia to the south, Peninsular Malaysia is a geographically, historically, and ecological diverse region that includes numerous mountain ranges, offshore archipelagos, and isolated karstic rock outcrops. The habitats of Peninsular Malaysia range from mangrove forest to lush multi-layered Dipterocarp forest to “post-apocalyptic” oil palm plantation dominated landscapes. Grismer does a great job familiarizing readers with the region by beginning his monograph with detailed information of the region’s biogeography and environmental diversity.
Most importantly, of course, Peninsula Malaysia is home to 128 lizard species, mostly geckos, skinks, or agamids, but also the occasional dipamid, lacertid, varanid, and leiolepid. Some 45% of these species are endemics, the vast majority of which are skinks and geckos that are narrowly distributed in montane habitats, isolated karstic rock outcrops, or off-shore archipelagos. The agamids, however, are likely to attract the immediate attention of anole lovers because this group includes most of the region’s arboreal, diurnal, and often conspicuous, lizards.
Image from http://animals.nationalgeographic.com/animals/reptiles/draco-lizard/
The most diverse agamid radiation in Peninsula Malaysia is Draco, the remarkable genus of gliding lizards that is found throughout much of southeast Asia.
One of the most significant potential impacts of Nicholson et al.’s proposed classification for anoles is that it would lead to changes in the binomials applied to most anole species. For example, Anolis cristatellus would now be Ctenonotus cristatellus and Anolis chlorocyanus would now be Deiroptyx chlorocyanus. The fact that Nicholson et al.’s classification would change so many binomials is the main reason we’re debating their proposed revisions; because binomials are the names that are most widely-used in the literature, changes to binomials are intrinsically more significant than many other types of taxonomic revisions. The plusses and minuses of dividing anoles among multiple genera are discussed in numerous other recent posts on Anole Annals. This post has a somewhat different goal – namely, to explain some of the proposed binomial changes proposed in Nicholson et al.’s classification that do not involve simply swapping one generic epithet for another.
In addition to simply dividing anole species previously recognized as Anolis among a number of new genera, Nicholson et al. introduce at least 48 new binomials that involve changes in the spelling of specific or generic epithets. My purpose is to summarize and explain these changes to the best of my abilities. As you will see, I soon reach the limits of my knowledge of both The Code and Latin and would like to ask readers more knowledgeable readers for enlightenment.
Understanding the majority of the name changes proposed by Nicholson et al. is relatively easy, as long as you take a moment to learn a bit about one of The Code’s article’s pertaining to Latin grammar. Indeed, Nicholson et al. are compelled to change 35 species epithets due to a controversial provision of The Code that necessitates a match between the Latin genders of generic and specific epithets. Most of the changes necessitated by this article of the code in Nicholson et al.’s proposed revision result from moving species from a masculine genus (Anolis) to a feminine genus (Audantia, Dactyloa, and Deiroptyx), and involve changing a trailing “us” to an “a” (e.g., Anolis chlorocyanus to Deiroptyx chlorocyana).A complete list of the species epithets that are being changed to match the Latin genders of their new generic epithets is included at the bottom of this post.
While most of the changes to specific epithets are due to the Latin gender issue, other changes have different explanations. In some cases, the reasons for these other changes are well-justified. Anolis etheridgei, for example, is changed to Deiroptyx darlingtoni because moving this species to Deiroptyx permits use of this species’ original specific epithet that was not previously permitted because it was the same as another species of Anolis (The Code does not permit two species named Anolis darlingtoni).
Nicholson et al.’s reasons for changing the fifteen remaining generic or specific epithets are less clear (at least to someone like me with no knowledge of Latin). From the table below comparing the species epithets in Nicholson et al. to those in the Reptile Database, one generalization one might make is that most of the proposed changes involve vowels. Some specific types of changes are applied more than once (e.g., a “u” is changed to an “i” in the names of both pumilus/pumilis and nubilus/nubilis) but other changes are unique (changing an “o” to an “io” in anfiloquioi/anfilioquioi). I’ve checked the spellings in all of the original species descriptions that I have on hand and found that they tend to match the species names in the reptile database. I believe the names in the original species descriptions are what The Code characterizes as the “correct original spelling.” Based on my crude understanding of The Code, I have the impression that these “correct original spellings” cannot be changed to correct spelling or other grammatical errors that the author may have made either intentionally or unintentionally (only those changes that were not the authors fault, such as type-setting or printing errors can be corrected subsequently). In one case the change might be permissible because it involves an error in the original related to number of people being honored. In one case, an “ii” is changed to an “i” seemingly against the letter of the code. When I asked Nicholson about these changes, she told me that they were all made in accord with “the rules of Latin usage combined with ICZN rules for how you apply name changes.”
Can others out there assist me in interpreting the justification for these proposed name changes?
NOTE: I’m reluctant to even suggest the possibility that some new binomials are the result of typos, but this possibility must be considered in a few cases. Nicholson et al. refer to A. macilentus (Garrido and Hedges 1992) throughout their manuscript, but refer t0 this species as A. maclientus in Appendix IV. The fossil anole from Dominican amber is mentioned only a single time in the body of the paper, where it is referred to as domincanus rather than dominicanus (de Queiroz et al. 1998). Similarly, a new genus name – Norpos – appears in Appendix III and again in Appendix IV when referring to the species parvicirculatus. Tables of the changes to binomial names in Nicholson et al. are below the fold.
Although we’ve been focusing a lot of attention on Nicholson et al.’s new classification for anoles, Daniel Scantlebury recently called attention to the fact that this monograph also contains “a bold hypothesis of the biogeographic history of” anoles. I’m going to focus here on only one aspect of Nicholson et al.’s biogeographic analyses – namely, their use of two remarkable amber fossils to calibrate a Bayesian relaxed clock analysis supporting the hypothesis that anole diversification dates back to the Cretaceous.
Nicholson et al.’s hypothesis that anoles first appeared more than 90 million years ago and that most major clades of anoles originated prior to 70 mybp is likely to be one of the most controversial aspects their hypothesized biogeographic scenario. These extremely old ages are significant because they make anole diversification compatible with a scenario that has long attracted the attention of vicariance biogeographers (Rosen 1975, Savage 1982, Crother and Guyer 1996). Under this scenario, anoles occupied an ancient volcanic arc that originated in the Pacific ~120 mybp and formed a landbridge between North and South America in the Late Cretaceous (75-70 mybp) before moving on to form the present day West Indian islands.
I have characterized the ages for anole diversification in Nicholson et al.’s biogeographic reconstruction as “controversial” and “extremely old” because they are older than the age estimates obtained by most other studies. Hedges et al. (1992) were among the first to use molecular methods to estimate ages for terrestrial vertebrate fauna of the West Indies, and reported ages for anoles and other taxa that were far too young to be compatible with Cretaceous vicariant events and the hypothesized Greater Antillean Landbridge between North and South America. Hedges et al. (1992) suggested instead that anoles arrived in the West Indies via over-water dispersal. Although Crother and Guyer (1996) criticized Hedges et al.’s use of immunological data and their resulting conclusions about over-water dispersal, more recent work has tended to support Hedges et al.’s conclusions by recovering ages for anoles and other terrestrial West Indian vertebrates that are too young to be compatible with the vicariant scenario hypothesized by Savage (1982), Crother and Guyer (1996) and Nicholson et al. (2012).
Daza et al.’s (2012) cladistic analysis of fossil data, for example, includes an update of the time calibrated tree generated by Conrad (2008) from available fossil material; this tree suggests that the Polychrotidae (the possibly non-monophyletic clade that includes anoles and other putative relatives like Polychrus) split from the Hoplocercidae sometime in the Eocene (~50 mybp). Townsend et al.’s (2011) analysis of a multi-locus molecular phylogenetic dataset for iguanian lizards that used a BEAST analysis with 18 fossil calibrations suggests a split between Anolis carolinensis and the Corytophanidae at 50-70 mybp. Most recently, Mulcahy et al.’s (In press) analysis of a multi-locus phylogenetic dataset for squamates in BEAST that relies on 14 fossil calibrations suggests that Anolis carolinensis split from Enyalioides laticeps 25-75 mybp (penalized likelihood analyses conducted by Mucahy et al. suggest a considerably older split between these two species that dates to around 80 mybp).
Recently published trees with estimates for the age of Anolis from Daza et al. 2012, Townsend et al. 2011, and Mulcahy et al. in press.
Why is there a discrepancy between the ages for anoles reported by Nicholson et al. and other studies?
Anole Annals dedicated all of last week to a detailed discussion of Nicholson et al.’s new monograph on anole classification, biogeography and ecomode evolution. Because we had so many interesting posts, our discussion has spilled over into another week. Some of the previously scheduled posts on biogeography and ecomode will be posted later today or tomorrow. Check back later today for more discussion of Nicholson et al.’s hypothesized biogeographic scenario and stay tuned throughout the week as we wrap up our discussion of Nicholson et al.’s important monograph. Remember also that Anole Annals welcomes posts and comments from anyone in the anole biology community about Nicholson et al.’s monograph, or any other topics to anole research.
Below the fold I provide an updated directory of the 18 previous Anole Annals posts pertaining to the Nicholson et al. monograph.
We’re just past midway into a week dedicated to discussion on Nicholson et al.’s new monograph on anole classification, biogeography, and ecomode evolution. We kicked off on Monday with posts about the history and potential future of anole taxonomy. On Tuesday and Wednesday we had four new posts about the merits of adopting Nicholson et al.’s proposed generic revision. George Gorman and Jonathan Losos argued in favor of retaining the traditional classification that places all anoles in Anolis. Todd Jackman and Craig Guyer, meanwhile, provided arguments in favor of dividing anoles among the eight genera proposed by Nicholson et al. It seems premature to try to summarize the resulting discussion, so I hope readers will take the time to check out the posts and associated comments for themselves.
Remember also that its not too late to contribute to the discussion with posts or comments of your own! We never censor posts or comments on the basis of scientific content, but remind members of our community of the importance of keeping the discussion civil and scientific. We’ve post-poned the scheduled posts on time calibration and ecomode evolution to encourage further discussion of the taxonomic issues.
For readers just joining the discussion, I share some links to prior discussions at Anole Annals pertaining to the Nicholson et al. monograph below the fold.
Anole taxonomists: Richard Etheridge, Jay Savage, Ernest Williams, S. Blair Hedges, Craig Guyer, Steve Poe
Anolis has been recognized as an extraordinarily large genus for decades, but Nicholson et al. (2012) are not the first to propose recognition of multiple anole genera. Indeed, all of the generic epithets used in Nicholson et al.’s new classification were coined in 1934 or earlier and most are from the early 19th century. This early proliferation of generic epithets resulted primarily from the fact that a comprehensive systematic treatment of anoles did not appear until the mid-20th century. My purpose here is to review the history of generic level anole classification in the years following Richard Etheridge’s pioneering PhD thesis of 1959/60. I believe that this historical perspective provides necessary context for evaluation of Nicholson et al.’s proposed revisions, and helps explain why the genera in their revised classification appear so rarely in the literature relative to Anolis (see Mahler’s recent post on the topic of genus name usage).
To briefly summarize the history of anole genera, the vast majority of work published over the past half century has formally assigned all, or nearly all, anole species to Anolis. The only noteworthy exceptions to this include (1) assignment of a small number of morphologically unusual species from the mainland, Cuba, or Hispaniola to Phenacosaurus, Chamaelinorops or Chamaeleolis into the 1990s and (2) assignment of species belonging to Etheridge’s β section of Anolis to Norops by some anole biologists working primarily in Central America during the 1990s through the 2000s.
Etheridge’s dissertation, which was completed in 1959 but not available until 1960.
In 1959, Richard Etheridge, a PhD student with Norman Hartweg at the University of Michigan, submitted a thesis that relied on remarkably thorough analyses of skeletal morphology to revise anole classification. At the beginning of this study, Etheridge recognized Anolis as a diverse genus containing over 200 species, but also identified ten other anole genera that contained only one or a few species: Chamaeleolis, Phenacosaurus, Chamaelinorops, Tropidodactylus, Audantia, Mariguana, Diaphoranolis, Xiphocercus, Deiroptyx, and Norops. Etheridge found the first four genera listed above to be “so unusual” morphologically that they warrant continued recognition, but the rest were synonomized with Anolis because his morphological analyses found them “to be not at all separable from Anolis, or to be based on characters so trivial that they are here considered as identical with Anolis.”
Etheridge left the large genus Anolis intact in spite of the fact that, at the beginning of his study, he “thought it very likely that the great number of species in the genus Anolis might be dividied into several groups, and that each of these might reasonably be accorded generic status.” His reason for leaving Anolis intact was that “the relationships of the various species of Anolis have proven to be far too complex to be treated in so simple a manner as the proposal of formal generic groupings.” Rather than naming new genera, Etheridge informally characterized sets of species at “several different hierarchical positions between the genus and species” as “groups,” “complexes,” “sections,” or “series.” The aspect of Etheridge’s classification that drew the most attention was his division of Anolis into α and β sections distinguished primarily on the basis of basis of a striking difference in the morphology of tail vertebrae (see figure above from Etheridge’s disseration).
We’ve already had lots of discussion about Nicholson et al.’s (2012) recent proposal that Anolis be fragmented into eight genera. Throughout the course of this discussion, several posts and comments have suggested that anole biologists might be compelled to implement Nicholson et al.’s proposed generic revision by the International Committee on Zoological Nomenclature (ICZN) and its rules for nomenclature (a.k.a. the ICZN* or The Code) (see comments on recent posts by Losos and Sanger).
Although I must admit at the outset that I am not an authority on The Code or its implementation, I will argue below that the belief that the code compels anole biologists to accept Nicholson et al.’s proposed taxonomic revision is completely false. The ICZN has neither the authority, nor the interest in, policing taxonomic practice and will have no role in determining whether Nicholson et al.’s (2012) new generic classification is accepted or rejected by the community of researchers who study anoles. I believe that the reasons for this are fairly straightforward and uncontroversial, but they do require us to think a little about our taxonomic philosophy and the difference between taxonomy and nomenclature.
Let’s start with some basics for the non-systematists. According to the ICZN, the goal of taxonomy is “the identification and interpretation of natural groups of organisms (i.e., taxa) based on characters (such as morphology, genetics, behaviour, ecology).” One piece of good news for anole biology is that everyone involved in debate over Nicholson et al.’s new classification shares the same fundamental taxonomic philosophy – namely, that taxa should be diagnosed using phylogenetic trees and should correspond with monophyletic groups. We may debate whether certain taxa are supported as monophyletic by the available data, but we all agree that recognition of monophyletic groups is a primary objective of any taxonomic scheme for anoles.
More good news: The Code has no interest in getting involved with taxonomic decisions. I realize that the The Code can be really boring to read, but you don’t have to read more than the first two paragraphs of the introduction to get this message (in a few cases I’ve added my own emphasis by bolding text):
“The 4th edition of the International Code of Zoological Nomenclature … has one fundamental aim, which is to provide the maximum universality and continuity in the scientific names of animals compatible with the freedom of scientists to classify animals according to taxonomic judgments. The Code consists of Articles … [that] are designed to enable zoologists to arrive at names for taxa that are correct under particular taxonomic circumstances. The use of the Code enables a zoologist to determine the valid name for a taxon to which an animal belongs … There are certain underlying principles upon which the Code is based. These are as follows: (1) The Code refrains from infringing upon taxonomic judgment, which must not be made subject to regulation or restraint…”
Rather than concerning itself with taxonomy, which inevitably involves subjective decisions made by systematists that specialize on particular groups of organisms, The Code focuses exclusively on nomenclature, or “the system of scientific names for taxa (such as species, genera, or families) and the rules and conventions for the formation, treatment, and use of those names.” The Code, therefore, merely provides “a set of rules for the naming of taxa that follows an internationally agreed, quasi-legal procedure.”
With this background, we can return to a consideration of Nicholson et al.’s classification and the role that The Code may have in its implementation. Nicholson et al. argue that in order to appreciate and study the phylogenetic diversity of anoles we must formally recognize the taxon that includes all anoles not as a single genus, but rather as a number of related genera. Although determining whether to proceed with the traditional classification involving a single genus or the Nicholson et al. classification that recognizes eight genera might seem to be a distinction between two alternative systems of nomenclature whose outcome is dictated by the The Code, this is not the case. Instead, both alternatives are perfectly compatible with The Code, and the decision about which classification to adopt moving forward is a subjective taxonomic decision that must be made by the community of biologists who study anoles.
All The Code says is that if we anole biologists want to recognize the taxa that Nicholson et al. have diagnosed as genera, we must use the names they have resurrected from the historical literature and applied to these taxa. If I wrote a paper tomorrow that gave a new generic epithet to the same taxon that Nicholson et al. have named Ctenonotus, this new name would be rejected under the rules of priority outlined in The Code. However, The Code respects the right of anole biologists to make the subjective taxonomic decision about whether we want to recognize the taxa diagnosed by Nicholson et al. as genera, or instead recognized them informally as series or species groups, as anole biologists have done for decades. Recall from our earlier passage from The Code that its rules for nomenclature only apply “under particular taxonomic circumstances.”
My fellow anole biologists, we have a taxonomic decision to make and the ICZN is not going to make it for us. It seems that the worst outcome would be fragmentation of the community of anole biologists, with some researchers using the traditional approach and others applying Nicholson et al.’s revised generic classification. More readings and notes are after the fold.
Nicholson et al.’s proposed re-classification of anoles is now a few weeks old and we’ve already had numerous posts on the topic as well as some great discussion. Given the interest in this topic, we’ve decided to dedicate all of next week to discussion of this paper. We invite contributions from all members of the anole community. Because we have mostly heard people speaking out against, we are particularly interested in hearing those who support this new arrangement. Anole Annals is a community forum and we do not edit content of posts from our contributors, but we do expect all contributors and commenters to use their real names (like many blogs, we’ve found that anonymity leads to problems that we’d like to avoid).
Here are some of the topics and posts slated for next week. More are welcome!
Monday: Background Information
Historical Perspective on Fragmentation of Anoles into Multiple Genera – Glor
Does The Code Compel Us to Change Anole Classification? – Glor
Tuesday: Thoughts on the New Taxonomy
It is NOT Time for a New Classification of Anoles – Losos
A Rose is a Rose, but is an Anolis a Dactyloa? – Gorman
Wednesday: Calibration and Biogeography
Evaluating Support for the Hypothesis that Anoles are 90+ Million Years Old – Glor
Mitochondrial Estimates for the Age of Anole Radiations – Scantlebury
Thursday: Anole Ecomodes
Is It Time to Replace Ecomorphs with Ecomodes? – Losos
Dan Rabosky and co-authors have just published an important report on patterns of organismal diversity in PLOS Biology, with one of their main conclusions being that clade age does little to explain species richness. Luke Harmon has a commentary on this article in the same issue of PLOS Biology, and I’ll refer readers there for a general summary of the work’s implications. I wanted to give this article a shout-out here at Anole Annals because they used an anole as their icon for squamates in Fig. 3 (see above).
Inspection of their supplemental Table 2 and consultation with the authors, however, reveals that anoles were inadvertently left out of the final analyses due to a book-keeping error involving use of the timetree age for Iguanidae sensuSchulte et al. 2003 but the species richness for Iguanidae sensuFrost & Etheridge 1989. (A quick taxonomic review for the uninitiated: The family diagnosed as Iguanidae by Frost and Etheridge included only a subset of the species previously regarded as members of the much larger family Iguanidae. Frost and Etheridge assigned Anolis and many of the other genera previously included in Iguanidae to other newly defined families. They considered this taxonomic revision necessary because they did not recover a monophyletic Iguanidae sensu lato. Because molecular phylogenetic analyses do tend to recover a monophyletic Iguanidae sensu lato, some subsequent authors, including Schulte et al. 2003, have advocated retention of Iguanidae sensu lato and treatment of Frost & Etheridge’s families as subfamilies [see Daza et al. 2012 for another perspective on this taxonomic debate].)
If we imagine crudely adding a circle to represent Anolis in Rabosky et al.’s figure 3 (assuming an age of ~50 mybp and species richness of ~400 for the genus), its clear that anoles would be among the youngest, yet also most species rich, of all squamate clades, providing further support for Rabosky et al.’s main conclusion that clade age has little role in explaining clade richness.
When alerted of this issue, Rabosky and his co-authors re-ran their analyses including anoles and their relatives (i.e., Polychridae/Polychrotidae of Frost and Etheridge) as well as all of the other Frost and Etheridge families that were overlooked for the same reason (e.g., Tropiduridae, Phyrnosomatidae). Rabosky sent me a figure that illustrates the position of all these missing clades (in blue), including the clade that includes Anolis (in red) as well as the other squamate clades in the original analysis (in grey). Because many of these clades stem from series of basal branching events within Iguanidae sensu lato and are relatively similar in age, they rather nicely illustrate the reported absence of a correlation between clade age and species richness. Not surprisingly, Rabosky et al.’s overall conclusions about clade age and species richness are unchanged by inclusion of these additional datapoints.
At the end of the day, this discussion nicely illustrates how monkeying around with the names of formal Linnean ranks can cause chaos for anyone who is not intimately familiar with a particular name’s complete history.
Rabosky, D. L., G. J. Slater, and M. E. Alfaro (2012). Clade Age and Species Richness Are Decoupled Across the Eukaryotic Tree of Life PLOS Biology DOI: 10.1371/journal.pbio.1001381
Wrapping up our coverage of the World Congress of Herpetology held in Vancouver last week, I have a report on Nick Crawford’s talk on the genetics of colorful pigmentation in Anolis. Nick began by talking about the basic types of pigments that contribute to anole coloration, which include both pteridines and carotenoids. Synthesis of pteridines is much better understood, thanks largely to work on zebra fish (reviewed in Braasch et al. 2007). Nick first showed preliminary evidence from rtPCR analyses suggesting that specific genes along the pteridine synthesis pathway differ in predictable ways among parts of anoles with different coloration (e.g., white venter, green dorsum, pink dewlap).
Crawford went on to note that pteridines may be less important to dewlap coloration than are carotenoids, but that the latter represent a bit of a black box genetically and developmentally. Crawford then discussed a project in which he uses a bulk segregant approach to ask if regions of the genome associated with color differentiation can be identified by examining genomic sequence data from species with polymorphic coloration. Crawford was particularly interested in the polymorphic Lesser Antillean Anolis marmoratus. He obtained sequence data from two phenotypically distinct populations of this species using the Illumina hiSeq platform. Fortunately this data could be aligned to the A. carolinensis genome, and showed a relatively high degree of synteny with this previously published genome. Analyses of the new A. marmoratus dataset are still in their early stages, but preliminary analyses recover 1,300 fixed SNPs (only 330 of which appear to be exonic) and suggest the presence of genomic islands of differentiation similar to those reported in many other recently diverged species and incipient species.
Note Added in Press:
One talk we failed to cover at WCH was by Chris Schneider on a similar topic. Here’s the Abstract:
Schneider, Christopher (Boston University); Crawford, Nicholas; McGreevy, TJ; Messana, Nick (Boston University, Canada)
The genetic basis of phenotypic variation and divergence in Anolis marmoratus
For those who work primarily in the West Indies, it can be difficult to imagine a lizard fauna dominated by anything other than anoles. However, if you’re interested in learning more about lizard communities that don’t include anoles, no book fits the bill better than L. Lee Grismer’s recent monograph on the Lizards of Peninsular Malaysia, Singapore and their Adjacent Archipelagos. Grismer takes readers on a tour of Peninsular Malaysia’s impressive lizard diversity, with species-by-species accounts that include morphological diagnoses, notes on coloration in life and among sexes, dot maps, and detailed notes on each species’ natural history. Grismer is the first to comprehensively review Peninsular Malaysia’s 128 lizard species, and his book represents the “first time the entire distribution of this fauna has been precisely mapped.” Of course, Grismer’s book is also chalk full of spectacular photographs, including many of Grismer’s trademark photos of animals in their natural habitat.
