Of Ecomodes And Ecomorphs: I. Are The Data Available To Categorize The Habitat Use Of All Anoles?

Anolis lividus. Trunk anole? Trunk-ground? Trunk-crown? Photo by Jonathan Losos

Mainland anoles exhibit a great diversity in habitat use and morphology, a topic we have discussed previously on AA. For this reason, an analysis of patterns of evolution in habitat use across all anoles, not just mainland species, would be very welcome. Nicholson et al. step into the breach by presenting habitat categorizations for a large number of mainland species, as well as for most West Indian species, and then analyzing habitat evolution on their preferred phylogeny. Along the way, they coin a new term, “ecomode,” argue that the ecomorph concept is fatally flawed and should be discarded, and present a scenario for patterns of ecological diversification in both mainland and island anoles. Although I applaud the effort to understand ecological evolution in mainland anoles and welcome the attention this paper brings to an important and little-studied question, I find the conclusions unconvincing. In this post, I discuss whether the data are sufficient to create categories of habitat use and confidently assign species to them; in subsequent points I will discuss the analysis of habitat use evolution and Nicholson et al.’s critique of the ecomorph concept.

What is an “ecomode”? The term is not explicitly defined in Nicholson et al., but it appears to refer to different categories of habitat use. The problem with creating such categories and assigning species to them is two-fold. First, most anole species use a variety of different habitats. I like to say that you can find almost any anole anywhere sometimes. More specifically, most anole species use the trunks of trees, often at different heights, and most can be found on the ground occasionally. How, then, do you distinguish a trunk anole from a trunk-ground or a trunk-crown anole, or a trunk-ground from a grass-bush? Second, how can one make sure that a given species fits into a single category? Perhaps some species have a broader niche that encompasses multiple ecomodes, or perhaps a species slices up the environment in an entirely different way (e.g., a trunk-bush or twig-ground species)?

Previous workers (including me) have been able to define ecomorphs and categorize species for two reasons. First, the ecomorph categories are defined not just on the basis of habitat use, but also by reference to morphology and behavior. Indeed, the morphological differences between ecomorphs are quite clear, and they correlate strongly with habitat use and behavior. One may quibble with a few assignments (e.g., is A. opalinus a trunk-crown or trunk anole?), as I discuss in Chapter 3 of Lizards in an Evolutionary Tree, but for the most part, assignment to ecomorph category is clear-cut (including the category of “non-ecomorph” for the minority of West Indian species that fail to meet the morphology/behavior/ecology criteria of any of the ecomorph categories).

The second reason we can make these assignments is because we have quantitative data that can be statistically analyzed. By contrast, the Nicholson et al. assignments are subjective decisions based on a reading of the literature, often relying on short summaries in broad regional reviews such as Savage’s (2002) The Amphibians and Reptiles of Costa Rica and Henderson and Powell’s (2009) Natural History of West Indian Reptiles and Amphibians. Use of these summaries is problematic for two reasons. First, although some mainland species have been studied extensively and quantitatively (e.g., the work of Vitt, Fitch, and Andrews), the habitat use of many species is not well studied. As a result, evaluating some summaries can be difficult because one does not know the extent and quality of the underlying data—in some cases (not Savage or Henderson and Powell), I suspect summary statements are not based on any hard data at all, but just qualitative impressions. In addition, even when species have been studied extensively, going from an encapsulated summary of such studies to an ecomode categorization is often not straightforward. For these reasons, the Nicholson et al.’s assignments of species to specific habitat use categories in many cases may not be reliable.

West Indian Non-Ecomorph Species

I will illustrate these problems by first discussing Nicholson et al.’s treatment of West Indian non-ecomorph species. For these species, there are a number of errors resulting from trying to interpret summary information provided in overview volumes. Continue reading

How Likely Are The Dates From Nicholson et al.?

Recent posts on Anole Annals evaluated the taxonomic implications of Nicholson et al.’s [1] new systematics, yet their manuscript included similarly bold interpretations of anole biogeography and the chronology of their diversification.  Nicholson et al. claim that a single genus genus concept for anoles can stifle “scientific communication regarding evolutionary events” and used their new multi-genera taxonomy “to propose a bold hypothesis of the biogeographic history of the family within the constraints of the phylogeny inferred here, the latest known fossils, and a paleogeographic interpretation of the deep history of the West Indies, North America, Mesoamerica, and South America.”  My goal today is to address if their phylogenetic dating analysis is capable of delivering on such claims.

Anoles are characterized by a sparse and poorly understood fossil record.  Any attempt to elucidate the evolutionary history and biogeography of anoles depends on neontological data in the form of DNA sequences from extant species.  Nicholson et al. utilized molecular clock dating methods to hypothesize about the temporal history of anoles.  They calibrated their tree with two amber fossils containing lizards identifiable as anoles.  They attribute the first, Anolis dominicanus, to the clade containing A. aliniger, A. chlorocyanus, A. coelestinus, and A. singularis and assign an age of 23 million years before present (mypb) to this clade.  They use the second second fossil, A. electrum, to calibrate the split between A. limifrons and A. zeus to 28 mybp.  With this background in hand, let’s turn to evaluating their results.

For the sake of a critical evaluation, I have centered the remainder of the post around a three questions I would have asked had I been selected to review this paper during the peer review process.
Continue reading

The PhyloCode and the Names of Anole Clades

I’m posting these remarks at the request of Anole Annals founder Jonathan Losos in light of his suggestion that a proponent of the PhyloCode explain how this system works (with reference to anoles).  As one of the developers of the PhyloCode, as well as a systematic biologist who studies anoles, I guess I’m the logical person to do this.  These issues relate to the recent proposal to “split” Anolis into multiple “genera” following the rules of the Zoological Code (ICZN) in that the PhyloCode (ICPN) describes an alternative system for applying taxon names according to which the very idea of “splitting a genus” has no meaning (hence my use of quotation marks).  The reason is that unlike the Zoological Code, which is based on artificial ranks (e.g., genus, family), the PhyloCode is based on statements about phylogenetic relationships, which means that the PhyloCode ties names directly to clades (monophyletic groups), rather than tying them indirectly and loosely to clades through the intermediary of ranks, as in the case of the Zoological Code.  Clades are evolutionary groups about which scientists can make inferences (regarding properties such as composition, diagnostic characters, and age of origin); they are not things that scientists can “lump” or “split.”  In any case, some of the advantages of the PhyloCode are that names maintain more stable associations with clades, many unnecessary and disruptive name changes that occur under rank-based nomenclature can be avoided, clades can be named one at a time as the evidence permits (rather than requiring large-scale revisions to the taxonomy, many components of which may lack an adequate evidentiary basis), and much more information about phylogenetic relationships can be conveyed (because the system is not artificially constrained by ranks).  In the rest of this post, I’ll illustrate these points using examples involving anoles.

The Fundamental Difference

The fundamental difference between the Zoological Code and the PhyloCode concerns the way in which names are defined in the two systems.  Under the Zoological Code, the name Anolis is effectively defined as follows:  Anolis := [is defined as] the taxon ranked as a genus that contains the species carolinensis.  Now it turns out that no one has defined the name Anolis using the PhyloCode approach, which requires names to be defined explicitly.  The following examples are just two possible ways in which that name could have been defined prior to the proposal to “split” the “genus”:  Anolis := the least inclusive clade containing bimaculatus, lineatus, carolinensis, punctatus, and auratus (some of the species originally included by Daudin) or Anolis := the clade originating in the first ancestor of carolinensis that had adhesive toe pads synapomorphic with those in carolinensis (one of the diagnostic characters originally cited by Daudin).  Note that the PhyloCode style definitions tie the name directly to a clade, while that of the Zoological Code only ties the name to a taxon, which might or might not be a clade, and even if it is a clade, the tie is only indirect through the clade being ranked as a genus.  I also want to point out that PhyloCode methods for applying names are tree-based in that they require phylogenetic trees for determining the limits of the clades to which the names apply.  Although rank-based methods can be applied in the context of trees, they are not inherently tree-based in that first, their implementation doesn’t require trees (taxa can be “erected” however the taxonomist chooses), and second, the names are more strongly tied to artificial ranks (in this case the “genus”) than they are to any of the monophyletic groups (clades) implied by a tree.

Associations between Names and Clades

As a consequence of the indirect (and thus weaker) tie between names and clades under the Zoological Code, names governed by that code do not have stable associations with clades.  This should be obvious from the fact that the name Anolis is associated with a relatively large clade of ca. 385 (currently recognized extant) species according to the current widely accepted taxonomy, but that name is to be associated with a relatively small clade of ca. 44 species according to the proposed “split.”  By contrast, under the PhyloCode, names have more stable associations with clades.  Thus, if we were to adopt either of the phylogenetic definitions of the name Anolis described in the previous section, that name would apply to the same large clade of ca. 385 species under both the phylogeny of Poe (2004: Figs. 1–4), who treated the entire clade as a “genus,” and that of Nicholson et al. (2012: Fig. 4), who propose to “split” the “genus.”  The reason is that the name is defined as referring to a particular clade independent of arbitrary rank assignments (note that the phylogenetic definitions make no references to ranks).  In addition, any changes concerning hypothesized species composition under the PhyloCode can result only from revised phylogenetic inferences (i.e., new scientific results); they cannot result from artificial and non-scientific decisions to change ranks (whether a particular clade is a “genus” is not a scientific hypothesis).  Thus, if we were to adopt either of the phylogenetic definitions of the name Anolis described in the previous section, the phylogenies of both Poe and Nicholson et al. lead unambiguously to the conclusion that Anolis includes the species formerly referred to the “genera” Chamaeleolis, Chamaelinorops, and Phenacosaurus.  But this does not mean that those names must be “synonymized” with Anolis, as they would be under the rank-based Zoological Code.  Instead, the name Chamaeleolis can continue to be applied to the clade of giant twig anoles including Anolis chamaeleonides and it close relatives (rather than adopting the new and cumbersome name “Xiphosurus chamaeleonides species group” of Nicholson et al.).  Similarly, the name Chamaelinorops can continue to be applied to the clade of anoles with certain distinctive vertebral modifications that is currently considered to include only the single extant species Anolis barbouri (rather than applying that name to a larger clade including 8 other species that do not possess those vertebral modifications and were not previously included in Chamaelinorops, as Nicholson et al. were obligated to do by the rank-based Zoological Code when they chose to rank that clade as a “genus”).

Unnecessary and Disruptive Name Changes Continue reading

Mid-Week Roundup Of Discussion On 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. Continue reading

In Support Of The New Taxonomy

ResearchBlogging.orgIt is very clear that most people who have posted to the blog site are quite uncomfortable with any proposed change to the concept of one big happy Anolis. What shines through to me in the posts is how deeply emotional the thought of this change is for many of us. I think I understand this emotion and hope to try to persuade you to let go of it by presenting this short story. I did my dissertation on Norops humilis in Costa Rica. The emotional side of me likes to think that, when this scientific name is mentioned in the future, my name and my work will forever be associated with it. Because of that, when Gunther Köhler and Kirsten Nicholson (my very own former student!!!!) wrote a paper demonstrating that I had not performed a dissertation on N. humilis but instead had worked with N. quaggulus, I took the news quite badly. In fact, to this day I struggle with this news because I find it difficult to deal with an emotion that says my work will be lost to the scientific community because of this name change. Obviously, this is totally illogical. The scientific community has been quite resilient to such changes. Classic works on North American Natrix were not lost to careful scientists by a name change to Nerodia. Blair’s work on North American Bufo will continue to be found and cited by anyone working with evolution of Anaxyrus. In the case of my N. humilis work, the thing that has gotten me over the emotional hump is the exciting biology that becomes clear if N. humilis and N. quaggulus are distinct species. Jenn Deitloff, Kirsten Nicholson, and I have been looking for the contact zone between the species I studied at La Selva and the species in Costa Rica that I thought I was studying. We want to determine how two species can maintain separate evolutionary trajectories given that there is no obvious boundary to their dispersal and their dewlaps, at least to my eye, are virtually identical. Köhler’s work seems to indicate that anole biologists have vastly undercounted the real species richness within Norops (and probably the other genera) because some characters, like dewlap color, may operate on a much more subtle level than we have allowed ourselves to consider. If I could have forced the world to succumb to my emotions, I would have, and these anoles would still be one big happy species rather than the several smaller lineages that character data seem to indicate they are. I could cling to N. humilis by pointing to a node on the tree and argue that, because of taxonomic stability, this should continue to be that species so that my La Selva work would maintain its association with that taxon. But, I would miss out on the interesting biology that emerges from simply letting go of that concept.

I see similar advantages to breaking anoles into eight genera. My experiences have caused me to develop a completely different search image for anoles in the genus Dactyloa than I have for those in the genus Norops. In helping to generate the revised taxonomy, I think I learned something interesting about anole ecology, and that is that it may be shaped by an origin of the group in the crowns of canopy rainforest trees in South America followed by a series of biogeographic events that brought them down to the leaf litter. I don’t recall our notions of evolution of anole communities being framed in quite this way. The fossil record and the topology of the phylogenetic tree led us to that insight. Discussions among the authors of the revised classification, during which we forced ourselves to use eight generic names instead of one, helped us gain those insights. We encourage the use of our taxonomy because it helped us see things that we might not have seen and we are confident that this may happen to others. As foundational as Schoener’s studies of one- and two-species islands were (and are – this work certainly shaped my interests), we think it would have been improved had he been forced to recognize those anoles as belonging to the genera Dactyloa and Ctenonotus. We suspect he would have analyzed the sets of islands separately and might have generated discussion among ecologists about degrees of freedom in comparative studies a decade before that discussion actually emerged. We think the taxon-loop vs. character-displacement argument would have been refined had the Dactyloa islands been viewed separately from the Ctenonotus islands. The Dactyloa-islands likely would have been described as fitting most strongly with the taxon loop hypothesis (large ancestors forced to become small with the first small species being doomed to extinction by the next smallest species – or large colonists reaching these islands, leading to the same process) and the Ctenonotus islands likely would have been described as most strongly fitting the character displacement hypothesis (mid-sized ancestors with a niche focused toward the ground diverging to make room for the next mid-sized colonists). We think Losos’ analysis of evolution of ecomorphology of Puerto Rican anoles would have been improved had he been forced to use the genera Deiroptyx and Ctenonotus.

I think the real intent of this blog is expressed in Glor’s posts. In my opinion, he is clearly asking the community of anole systematists to band together as a unified voice against acceptance of the proposed new taxonomy. Obviously, the community of anole systematists has never been of one mind on this topic and I would hope that the community would recoil at the thought that we ever should be. The notion that the world recently came to accept a single large genus Anolis as the only viable concept can be rejected by the observation that some in the community of anole systematists continue to publish under names such as Dactyloa, Norops, and Ctenonotus (e.g. Savage’s book). Given what is happening with so many other large, cumbersome genera, I think it is inevitable that a revised classification of anoles will happen and those who are fighting so hard to prevent it will find their careers intact when they cross that inevitable threshold. Once there, I think they will wonder why they fought so hard against change.

KIRSTEN E. NICHOLSON, BRIAN I. CROTHER, CRAIG GUYER & JAY M. SAVAGE (2012). It is time for a new classification of anoles (Squamata: Dactyloidae) Zootaxa, 3477, 1-108

A Case For Splitting Up Anolis

To some degree, I am playing Devil’s advocate in supporting the split of Anolis – but I do think there are valid arguments that need to be considered.

There are a number of assumptions that, if proven to be false, weaken my argument:

    1. As a clade, anoles are older than the KT boundary – 65 million years. The estimates from Nicholson et al. are much older than that, but if you were to choose a date where splitting up vertebrate genera might make sense, 65 million years is not unreasonable. It is likely that coalescent methods will make the estimated age of anoles younger than the 95 million years in the paper, but I’m going to guess older than 65 million years. You may feel that clade ages are irrelevant, but I’m willing to bet that most people would have some age that they would say is too old for any genus (500 million years?)
    2. The Alfoldi et al. (2011) tree is pretty accurate and the following aspects of that tree will remain after adding taxa and more data. Starting with the Norops clade or genus (see below for a discussion of why Norops), there are 8 very well supported clades (black dots on the Supplemental figure). There are very short branches between 4 of those groups, representing a rapid radiation such that only 3 of 7 possible inter-group relationships are well supported. Anolis lucius and  A. argenteolis were left in Anolis by Nicholson et al. because A. argenteolis represents the biggest conflict between mtDNA and nuclear DNA and is placed with high confidence with the Anolis clade in Alfodi et al. – I assume that the nuclear tree represents the correct placement of that species.
    3. If Anolis is split up, the usage of the word “anole” would increase and refer to all 8 genera to a degree that would minimize workers not knowing that these 8 genera are monophyletic.

One narrative that needs to be considered (see Rich Glor’s excellent post on the history) is that the impetus to split Anolis comes from those who have primarily worked in Central and South America, where the two most disparate (by time) clades of anoles co-exist. If there are non-systematists working on anoles on the mainland it would be useful if they recognized the deep split between two clades of species now in the same genus, especially if clade names fail to be used outside of those whose focus is phylogentic trees. The problem has been that if Dactyloa and Norops are used on the mainland, then a bunch of other generic names are needed for the Caribbean species that fall between the two genera on the tree, with 8 being the minimum number of very well supported groups (again with an assumption that the nuclear DNA framework is robust).  To split Norops further might lose the great story of the reinvasion of the mainland from the Caribbean (Nicholson et al., 2005). From the perspective of those working on the mainland, 8 is a logical minimum number. Given the lack of resolution between the 8 groups, 8 clades is more information than 1 and not much is lost going to 8.

It is important to ask what workers on mainland anoles other than Nicholson et al. think about splitting Anolis. What does Laurie Vitt think, for example?

Another aspect of genera that hasn’t been touched on yet is morphological dissimilarity. Although there is no agreed upon (or necessary) level of dissimilarity needed to recognize a genus, my personal feeling is that if two species are in separate genera, it should not be difficult to tell them apart as species.  I think that this is one reason that I am opposed to the excessive splitting of Bufo and Rana that have been proposed. (To really make this a really good argument, I would need to find some specific cases where the new Frost et al. 2006 genera are difficult to tell apart as species – I’m just assuming that this is true –). In any case, Anolis is not like Bufo – the species are distinct and there is plenty of morphological variation. Long before molecular phylogenies, workers on Anolis, knew (or at least strongly suspected) that ecomorphs were not monophyletic. This does not necessitate splitting Anolis, but it distinguishes it from other cases that may be oversplit.

It seems very likely, (particularly on the mainland) that some workers will use the revised taxonomy and some will not, leading to an increase in the mixture of name usage.

Unlike others, I don’t think that this fragmentation in usage is necessarily horrible because it will force anyone who works on this clade to consider phylogenetic relationships and to be cautious about applying any methods that blindly consider genera to be equivalent in any way (this includes any meta-analyses of squamates that use genera as a unit of measure).

In conclusion, even if I’m playing devil’s advocate to some degree, I have a real concern about the best way to encourage the use of phylogenetic information outside of research that is focused solely on taxonomy and the phylogenetic history itself.

KIRSTEN E. NICHOLSON, BRIAN I. CROTHER, CRAIG GUYER & JAY M. SAVAGE (2012). It is time for a new classification of anoles (Squamata: Dactyloidae). Zootaxa, 3477, 1-108

Nicholson, K.E., Glor, R.E., Kolbe, J.J., Larson, A., Hedges, S.B. & Losos, J.B. (2005) Mainland colonization by island lizards. Journal of Biogeography, 32, 929–938.

It Is NOT Time For A New Classification Of Anoles

ResearchBlogging.orgWe’ve had a lot of great discussion about Nicholson’s et al.’s proposal to split Anolis into eight genera. To date, most of the commenters have been against the proposal; I’d like to explain why I agree with this majority view.

Anole Annals summarized the arguments for splitting Anolis several days ago. Nicholson et al. argue that the failure to divide Anolis in the past has inhibited evolutionary and systematic research:

“Systematic progress in this regard has been delayed by an extremely conservative taxonomic approach to recognizing the diversity within the group and its extraordinarily ancient historical roots.” (p.4)

“The current practice (following Poe, 2004) of treating all dactyloids as comprising a single genus underemphasizes the evolutionary diversity within the family (as currently recognized) and obfuscates major biological differences among clades. In addition, simply because of the large size of the family (nearly 400 valid species), the single genus concept can be a hindrance to scientific communication regarding evolutionary events and directions of future research.” (p.13)

These quotes suggest that research on anoles is being held back by treating the entire clade as a single genus, but where is the evidence for these claims? No examples are provided. Quite the contrary, research on anoles has flourished over the last several decades, making it a well-known group for the study of many diverse evolutionary phenomena, and much of this work has explicitly incorporated phylogenetic information. Indeed, anole evolution, considered in a phylogenetic context, has become a commonly cited textbook example of adaptive radiation, and work on anoles has become so broad and deep that one commenter at last year’s Evolution meetings noted that “I didn’t go to the Evolution meetings for three years…When I “returned” in 2011 in Norman, it was like everybody had switched to working on anoles and sticklebacks!” The Dobzhansky Prize winners at the last two Evolution meetings have conducted phylogenetically-based research on anoles, and anole workers have nabbed the Fisher Prize and four Young Investigators Prizes at the meetings in that time span. Anole research is going gang-busters, and it is hard to see how retaining the name Anolis for the entire clade has had any sort of detrimental effect. (see also comments by Eric Schaad on why taxonomic names are no longer important for conducting phylogenetically-based evolutionary studies and by Yoel Stuart on why splitting evolutionarily-interesting clades may actually impede research).

I disagree with the proposal to split Anolis into eight genera for two reasons. First, it is not possible for the Linnean classification system to fully represent phylogenetic relationships—splitting genera simply changes the information conveyed, gaining some bits of information and losing others (for more discussion on this point, see the recent post by Luke Mahler and ensuing commentary). Second, splitting Anolis will be extremely disruptive for scientific researchers and the public. Continue reading

What’s In A Name? Perhaps A Rose Is A Rose Is A Rose, But Is An Anolis A Dactyloa?

ResearchBlogging.orgA half century ago my graduate research was stimulated and influenced by the important unpublished Etheridgean thesis (Etheridge, “1959”, 1960).  As an E.E. Williams student, I was an  adopter, user, and later coiner of informal names for seemingly natural evolutionary groups in the diverse genus Anolis.  In most cases, I was building upon (sometimes tweaking) the foundation of Etheridge’s classification.  I believed then and believe now that the use of informal names for natural groups worked well for communicating evolutionary hypotheses both to specialists in our field, and to a broader audience of professional and amateur biologists who are likely not well informed about the nomenclatural history of these lizards.

Nicholson et al. (2012) believe otherwise. Here is their overview, page 13:

“The role of systematics is to advance our understanding of biological diversity in the natural world. Its practitioners are the guardians of the knowledge produced by past generations and responsible for the rational interpretation of new data and their implications. Within this framework, phylogenetic inference has consequences that we think bind its practitioners to produce a systematic classification of the studied organisms. Such a classification must be founded on the inferred evolutionary relationships and dictated by the canon of monophyly.”

I support that.

This note, then, is neither about the role of systematics, nor the  interpretation of phylogenetic analyses (the Nicholson et al. presentation is comprehensive and extremely valuable).  Rather it concerns their conclusion to the cited paragraph about the use of Anolis, as the generic name for the entire clade. They write:

“the single genus concept can be a hindrance to scientific communication regarding evolutionary events and directions of future research.”

I believe exactly the opposite. Specifically, I believe that the single genus concept enhances scientific communication and suggests directions of future research. Continue reading

Historical Perspective On Anole Genera

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 PhenacosaurusChamaelinorops 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). Continue reading

The Code Does Not Compel Anole Biologists To Accept Nicholson et al.’s New Classification

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. Continue reading

Day Geckos Eating Cheerios

Those darn faux anole day geckos are out-cuting our boys again. The title of this post is self-explanatory, but the link to anoles isn’t completely tenuous–the gene that encodes for taste receptors that are sensitive to sweet things isn’t posssessed by all animals (e.g., cats lack it), but it has been found in the anole genome and, Matthew Cobb guesses based on this video, in geckos as well.

Anolis Carolinensis Named “Invasive Species Of The Week”

The Invasive Species Specialist Group, a Species Survival Commission (SSC) of the International Union for the Conservation of Nature and Natural Resources (IUCN), recently gave the weekly top honor to our favorite greenie. We love ‘em here in the U.S., but as we’ve documented many times, they can be a problem elsewhere. A pdf of the picture above is available at the ISSG site.

How Often Do Anoles Lose Their Tails In Intraspecific Fights?

Male A. pogus fighting. Photo from http://www.lesfruitsdemer.org/wp-content/gallery/anolis-pogus-battle-03-01-2010/DSC_7573.jpg

Recently, our lab group was discussing what can be inferred from calculating tail loss rates in anole populations. It was pointed out that tail loss doesn’t necessarily result from predators and that, in fact, males may bite off the tails of other males in fights,  and the victor or vanquished may even eat the tail. Someone pointed out that the older literature certainly pointed this out with examples*, but we haven’t seen much of this in more recent literature. So, we then asked, has anyone ever actually seen a tail lost in a fight? No one had. I then got online to look for photos. I could find plenty of males fighting, usually locking jaws or sometimes biting the body or a limb, but I found no photos of an anole biting another’s tail, much less biting off a tail. So, I ask you, fair AA reader, have you ever seen this? Can you provide a photo?

*By earlier literature, we were thinking 1960’s and 1970’s, but here’s a quote from the 1870’s, referring to A. cristatellus. Can you name the author? “During the spring and early part of the summer, two adult males rarely meet without a contest. On first seeing one another, they nod their heads up and down three or four times, and at the same time expanding the frill or pouch beneath the throat; their eyes glisten with rage, and after waving their tails from side to side for a few seconds, as if to gather energy, they dart at each other furiously, rolling over and over, and holding firmly with their teeth. The conflict generally ends in one of the combatants losing his tail, which is often devoured by the victor.”


A Week Of Discussion On Anole Taxonomy, Biogeography, And Ecomode Evolution

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

Friday: Loose Ends and Discussion

What’s In A Name?, Part II

Last week, I wrote a post on how the new classification for anoles proposed by Nicholson et al. 2012 might affect long term taxonomic stability for this group. That post generated some discussion, including, most recently, commentary by Kirsten Nicholson herself, explaining some of the reasons her group decided it was time to split up the anoles. Because that conversation is quickly becoming buried in the depths of Anole Annals, I wanted to continue it here on the main page. Also, I wanted to write some more to expand on some of the thoughts that prompted me to post last week, and I hope folks will continue to weigh in (note, the rest of this post will make a lot more sense if you first read my previous post, and the ensuing commentary). I’d like to make several general points:

1 – I think we can all agree that taxonomies should reflect accurate phylogenetic knowledge (I don’t think anyone here would disagree with this – let’s take it as a given that Linnean taxa should not be paraphyletic or polyphyletic).

2 – Beyond accuracy, I’m pretty sure there aren’t any rules governing the type or level of phylogenetic information that “should” be included in a binomial classification. Whether binomial names should reflect deep phylogenetic knowledge or shallow phylogenetic knowledge is a matter of opinion – I’d propose it’s completely subjective.

3 – The amount of phylogenetic information you can communicate in a binomial classification is trivial. It’s hard enough to represent phylogenetic structure across the depths of the entire Linnean hierarchy, and there’s almost no such information in Genus+species epithets. The goal of communicating finely resolved phylogenetic information probably should not be our main concern when dealing with genus names (so long as they are not phylogenetically inaccurate).

4 – Given that no one’s to say who’s right about what the appropriate phylogenetic scale of a genus is, and that Latin binomials are ineffective at communicating much of anything about phylogenetic information anyway, issues of stability are comparatively very important. It’s no small thing to propose a change for 88.6% (n = 343) of the scientific names of a group of species studied by thousands of people.

Since I think we can all agree that Linnean names should be applied solely to monophyletic groups, I’ll start with my second point, which is that there’s no “right amount” of phylogenetic knowledge that should be expressed in binomial names. Kirsten suggested we might all agree that “our classifications should mirror our phylogenetic knowledge.” I certainly agree with this statement in general, but I suspect I might disagree on some of the details. What sort of classification, exactly, would mirror our knowledge best? Should we assign genera to the smallest phylogenetic units about which we can be reasonably certain of monophyly, and continue to split them up into additional genera as we work towards resolving the entire bifurcating history of anoles? If so, we’ll probably eventually end up with a taxonomy that’s as finely parsed as that of the non-avian dinosaurs, where the genus:species ratio is 1:2 (I’m not even kidding – check it out…)! At this point, we’d have all sorts of cool binomials, like Nicholsonolis annectans and Mahlerolis gorgonae, but the genera would be functionally equivalent to species names (as they are in dinosaurs). This sort of reasoning (taxonomy should reflect ever-improving phylogenetic knowledge) is implied in the very title of the Nicholson paper, which seems to suggest that periodically, when the progress of systematics has advanced enough, “it is time” to reclassify everything (I think this contradicts the founding purpose of Linnean classification, but that’s another point). Anyhow, if this isn’t what it means for a taxonomy to mirror phylogenetic knowledge, then what exactly does that mean? Why 8 genera, and not 60, 16, or 4?

My main point here is that it’s a matter of opinion what kind of phylogenetic knowledge should be in a Latin name. One person might think that a genus should apply to the MRCA and all descendants of any two species similar enough to be confused by an experienced herpetologist (e.g., Anolis fraseri and A. biporcatus; see Williams 1966 for details). Another person might maintain that a genus should have 20 species max, no exceptions. Both are entirely matters of opinion, and such opinions abound when it comes to systematics. But since there are no official guidelines on the matter, I don’t think that such opinions can suffice to justify a disruptive taxonomic change.

I next wanted to criticize the logic of amending genus names to reflect systematic developments. The reasons are that (a) there’s very little phylogenetic information in Latin binomials, and (b) any change in the names of genera will result in a gain of some phylogenetic information (shallower information) at the expense of other phylogenetic information (the deeper stuff).

Linnean binomials contain next to no phylogenetic information. When we look at a list of scientific names, all we know is that congeners are more closely related to one another than they are to members of other genera, and other than that, they don’t tell us anything about phylogeny. To illustrate this, I created “binomial phylogenetic trees” for the Iguanidae (or Iguania, depending on who you follow..). I included all species in “Iguania” from the Reptile Database. Here’s what the traditional classification looks like, with Anolis highlighted in red:

Binomial “phylogenetic tree” of iguanian genera, following the traditional classification.

Continue reading

A History of Head Bobs

ResearchBlogging.orgIf you were to cast lizards as characters in a remake of The Great Gatsby, anoles, of course, would have to be cast as protagonist Jay Gatsby. “What Why Gatsby?” you might ask.  Well, like Gatsby, anoles have gaudy, aggressive displays that show fitness and define territory. Also like Gatsby, (SPOILER ALERT) anoles cannot seem to escape their past (for the headbob part of their display, at least).

In a recently published paper, Terry Ord investigated whether past ancestry explains variation in Anolis diplays better than evolution by natural selection. To begin to ask this question, Terry compiled data on the average time of headbob and dewlap bouts for species for a Western Caribbean Anolis lineage (Jamaica, Cayman Islands, Cuba) and for an Eastern Caribbean lineage (Puerto Rico and Hispaniola). The data and phylogenetic relationships are shown in Figure 1. Continue reading

Species Richness Patterns in Caribbean (and Mainland) Anolis V

In our comparison of mainland and island species turnover, we sampled mainland communities by randomly superimposing each of the Caribbean islands on the mainland five times. In each of these mainland island-shaped regions, we then tallied how many species were present and then measured turnover between regions.


Oceanic islands are famous for their high endemism. We all love Darwin’s finches, Hawaiian honeycreepers, Komodo Dragons, and all those weird things on Australia. These endemic wonders suggest that islands may be home to unique processes of diversification.  However, there are many mainland regions that rival islands in their level of endemicity, especially in mountainous regions that have strong dispersal barriers and environmental gradients. Thus, you could ask, are islands truly special? Continue reading