Anole Annals

Anolis cristatellus, native to Puerto Rico but introduced to a number of areas, awakened on a leaf. Photo credit: Tom Kennedy, University of New Mexico.

Human-mediated species invasions are excellent real-time experiments to assess community assembly. These recent invasions are considered accurate analogues of ancient colonizations, which contribute to today’s natural species communities. Whether this is a correct assumption, however, had until now not been sufficiently tested.

A new paper by Steven Poe available online in the American Naturalist examines this point. His results are very exciting for many people working on anoles, and everyone interested in species invasions and community assembly. Therefore, I present a summary of his findings here.

Previous studies have shown that recently naturalized species are morphologically similar to ancient colonizers, indicating that processes shaping biotic communities could be the same in both situations. However, the unnatural (i.e., human-mediated) mode of dispersal responsible for assembling modern communities and the frequent establishment of animals in urban areas may result in unique species combinations that are not normally present in nature. Poe examined this proposition by comparing natural and nonnative two-species communities of anoles based on morphology and phylogenetic structure.

The results show that the morphological differences among the species in natural communities are not significantly lower or higher than those in naturalized species pairs. Furthermore, the anole species in natural and nonnative communities are morphologically indistinguishable; they have unusually high colonization scores and all morphological trait comparisons of species from naturalized communities versus natural communities are nonsignificant.

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Should Anolis be split into several genera, and why is this is the wrong question? The battle over anole classification is not about splitting Anolis into several genera; it is about changing the content of a well-understood taxon, by pointing the name Anolis to a different branch or node of the tree. The war, then, is about the failure to connect taxonomy to phylogeny in an evolutionarily meaningful way, which is that taxon names should be associated with evolutionary lineages (clades) and not with ranks. If one accepts this, then it is rarely necessary to change the association of a name with its taxon, as proposed by Nicholson et al. (2012) in the case of Anolis.

Below I respond to several misconceptions about taxonomy, some with reference to anoles. I am not claiming that Nicholson et al. (2012) espouse these explicitly, but they are germane to anole taxonomy.

Misconception 1. Taxonomic stability is ignorance. Put another way, stability in taxonomy is not necessary, or even desirable. In contrast, I argue that stability should be a basic characteristic of taxonomy.

Taxonomies become unstable when the association between a name and its taxon changes, i.e., when the name points to a different taxon. However, stability does not mean that taxonomies do not change at all. Stable taxonomies can change, that is, improve, by adding more information about hierarchy. That is, as new nodes are discovered, names are progressively applied to those nodes. The existing associations between names and taxa need not change.

Misconception 2. Taxonomies are primarily for systematists. Unfortunately, some systematists view taxonomy as a personal sandbox. Rather, taxonomies are reference systems that are fundamentally important to the community of non-systematists. If not conservative, taxonomies are confusing for those who need stable reference lists. Witness the controversy about Bufo, Rana, etc.

Misconception 3. Some people don’t like change.  Two types of change are at issue: (a) change in taxonomy, and (b) change in the practice of taxonomy. We who prefer a conservative taxonomy that maintains name-taxon stability are considered old-fashioned. Those who prefer taxonomy that breaks name-taxon stability, as has been proposed for anoles, are often considered progressive (see Misconception 1), under the assumption that any change is progress.

Ironically, a stable, “conservative” taxonomy requires a radical change in mindset about how taxonomy is done. Simply put, one maintains the association between name and clade, and applies new names when as needed to newly uncovered taxa. This approach reflects a growing understanding of the relationship between taxonomy and phylogeny. de Queiroz (1988) called attention more than 20 years ago to the failure of taxonomists to integrate taxonomy into the Darwinian Revolution.

A focus on ranks—arguing that eight genera of anoles are preferable to one—is inherently non-evolutionary. Thus, those who prefer to split a ranked taxon into several of equal rank are the resistors of change.

Misconception 4. Changes in stability between name and taxon are inevitable, especially in cases of paraphyly. De-stabilizing changes are not inevitable, and only result if one places primacy on rank-based taxonomy rather than taxonomy based on ancestor-descendant (evolutionary) relationships. N. B., I am not advocating that ranks should not be used, only that the emphasis on ranks is the cause of the controversy.

Elimination of paraphyly was the battle-cry of early cladists, but in reality the arguments about paraphyly were a distraction from the real issue. The Reptilia-Aves controversy was fundamentally about ranks, not paraphyly. Should Reptilia and Aves both be ranked as classes? If yes, then Reptilia is paraphyletic, because paraphyly follows from the use of ranks. The solution to the controversy was acknowledgement that Aves is nested within Reptilia, giving primacy of phylogeny over ranks. As Neil Shubin articulated, we all have an Inner Fish.

Paraphyly has consistently been a motivation for dismantling Anolis beginning with Guyer and Savage (1986). However, that the genus Norops (for example) is nested within the genus Anolis does not require splitting Anolis into several genera. One simple solution is to treat Norops as a subgenus within Anolis. The name of the species sagrei can then be written as Anolis (Norops) sagrei. The elegance of this is that Norops and Anolis, as nested taxon names, continue to refer to their traditional clades.

A second, more general solution is to use multiple levels of unranked clade names as done by Castañeda and de Queiroz (2013). They recognized as formal unranked taxa the clade Dactyloa; and within Dactyloa, clade Megaloa for the latifrons series, and clade Phenacosaurus for the heterodermus series. Because these are expicitly used as unranked names, they are not regulated by the International Code of Zoological Nomenclature (the Code).

As Cannatella and de Queiroz (1989:68) responded to Guyer and Savage (1986): “A phylogenetic taxonomy could have been effected by reorganizing sections, subsections, and series within Anolis, without generic level re-arrangements.”

Misconception 5. Subgenera are not used much in herpetology. Even if this were true, it is not a reason to reject the use of subgenera. Regardless, the data don’t support this claim; the use of subgenera is rising. They are a very useful tool, but have constraints imposed by the Code (these can be easily fixed).

Misconception 6. The most recent classification must be used as the standard. To recognize this fallacy one need only read the first Principle of the Code, which embraces taxonomic freedom. A common question from the community-at-large is, Which classification is the “correct” one? The answer is of course that there is no “correct” classification, and taxonomists who claim this do a disservice to the general community.

It is, in fact, time for a new classification of anoles, but one that truly integrates evolutionary principles with taxonomy, reflecting progress and not just change.

Acknowledgements. This essay is strongly influenced by Kevin de Queiroz, who articulated many of these ideas >25 years ago. David Wake engaged in helpful discussions.

References

Cannatella, D. C., and K. de Queiroz. 1989. Phylogenetic systematics of the anoles: is a new taxonomy warranted? Syst. Zool. 38:57-69.

de Queiroz, K. 1988. Systematics and the Darwinian revolution. Phil. Sci. 55:238-259.

del Rosario Castañeda, M., and K. de Queiroz. 2013. Phylogeny of the Dactyloa clade of Anolis lizards: New insights from combining morphological and molecular data. Bull. Mus. Comp. Zool. 160:345-398.

Guyer, C., and J. M. Savage. 1986. Cladistic relationships among anoles (Sauria: Iguanidae). Syst. Zool. 35:509-531.

Nicholson, K. E., Crother, B. I., Guyer, C., and J. M. Savage. 2012. It is time for a new classification of anoles (Squamata: Dactyloidae). Zootaxa 3477:1–108.

There’s an old saying, “life imitates art.”

The last few days have seen renewed discussion of the proposal to split Anolis into multiple genera. In their most recent paper, Nicholson et al. (2014) explain why they want to split up Anolis: “Starting with Savage (1973), we have made clear our conclusion that the beta section of Williams (1976) deserves generic status (Norops).” The reason, as they explain in the preceding paragraph: “Anyone who has caused a squamate’s tail to separate from its body, and has read Etheridge’s paper, understands immediately why we conclude that the beta condition within anoles is as important to understanding the diversity of that group as the toe lamellae of anoles is to understanding the evolution of Dactyloidae.” In other words, the caudal vertebral structure of Norops, “a derived condition of the caudal vertebrae unique among squamates,” is so notable and distinctive that Norops needs to be recognized as a genus to call attention to and emphasize this evolutionary transition.

This approach follows the rationale of Ernst Mayr’s Evolutionary Systematics Classification system, whose goal was to highlight major evolutionary transitions. This approach has generally fallen out of favor, however, because it often led to the recognition of paraphyletic groups, such as “reptiles,” when birds are elevated due to their evolutionary significance.

Nicholson et al. (2014) solve this problem, however, by recognizing the clade they consider important, Norops, but then recognizing as many other clades as necessary to render all clades monophyletic: “Therefore, the seven additional genera that we propose as replacements for the alpha section represent the minimum number of genera needed to eliminate the problem of the previous taxonomy” once Norops is elevated to generic status. Evolutionary classification meets phylogenetic systematics!

Surely if one clade of anoles is going to be recognized at the generic level because it has a funky tail, then Chamaeleolis deserves to be a genus as well.

Nicholson et al., however, are not the first to take this approach in revising anole classification. Just last year, another paper considering anole classification came to exactly the same conclusion. Dimedawter et al. (2013), writing in Nature Herpetology, propose: “This approach is implemented readily enough and entails nothing more than identifying evolutionarily important clades, recognizing them at the appropriate taxonomic level, and then revising the remaining taxonomy to ensure that all taxa are monophyletic.” Taking the approach to its logical extreme, they then illustrate it using Anolis. However, rather than Norops, Dimedawter et al. start with Chamaeleolis and Chamaelinorops, two clades so distinctive that the authors contend they should be recognized at the generic level, as they once were.

No toepads? That’s got to be its own genus.

But what constitutes evolutionary significance is in the eye of the beholder. Dimedawter et al. survey anoles and note a number of other clades that seem distinctive enough to warrant generic recognition. Among these are the padless anole of Venezuela (Tropidactylus); twig giants and dwarves of South America (Phenacosaurus); the aquatic anole of Hispaniola (A. eugenegrahami); Xiphocercus, the medium twig anole of Jamaica; Deiroptyx as originally constituted (vermiculatus and bartschi); among others. All of these anoles are cool and distinctive in their own way, and so it seems reasonable to recognize them as distinct genera. In sum, they identify 11 clades worthy of generic level designation. To maintain monophyly of all anole clades, that requires recognizing 34 more clades, for a total of 45 anole genera.

Dimedawter et al. then go one step further. Agreeing with Nicholson et al. (2012), they argue that phylogenies should be informative of phylogenetic relationships. However, they fault Nicholson et al. for not going far enough—after all, their proposal does not provide insight on the relationships among the 150 Norops, or even among the six Chamaeleolis in their own system. So, they propose a new approach, Maximally Informative Phylogenetic Clustering (MIPC), which allows one to always know the sister taxon of a species from the classification. Applying this approach to anoles, they propose the recognition of 133 anole genera.

Exciting times for anole classification!

Nicholson et al. (2014) provide two reasons that Anolis should be divided into eight genera. The first is simply that this is what modern systematists do, breaking up big groups into little groups. But this is not really a very compelling argument in its own right. As your mother used to tell you, “just because everyone else is jumping into a lake doesn’t mean you should, too.”

Their second reason is more specific. They argue that more finely divided groups are essential for understanding patterns of evolution and diversity:

“When new monophyletic structure is revealed in groups for which such structure was previously unrecognizable, taxonomy should change to incorporate that new information. This process does reveal constructs inherent to the natural world and, therefore, forces us to change the way we train future generations of biologists, design future comparative analyses, and interpret new data.”

But let’s take apart this argument. First, have Nicholson et al. revealed “new monophyletic structure” that was “previously unrecognizable”? The authors themselves point out that these groups have been found in all recent systematic studies and, indeed, the community has been well aware of them. One only needs to go back to Jackman et al. (1999) to see recognition of 17 clades, and discussion of these clades has continued ever since. Nicholson et al. would have readers believe that we thought that Anolis was one big, unstructured group of 400 species, but that is a very incorrect portrayal of the widespread understanding of anole phylogeny.

More importantly, second, has our understanding of anole evolution and diversity suffered because we have considered anoles as one genus instead of eight? This is a pretty hard argument to make. For a quarter of a century, work on anoles has been an exemplar of how to incorporate phylogenetic information into studies of evolutionary diversity. For example, anoles are now known as a model case of convergent evolution—it’s not like we’ve failed to recognize that convergence just because they’re all called “Anolis.” It’s striking in this regard that the sole paper cited by Nicholson et al. (2014) to support their contention that a single genus is problematic is nearly 30 years old! Thirty years of copious anole research shows that recognition of a single, large genus has not hindered anole research in the slightest.

Indeed, it is thought-provoking to compare the contributions made by research on anoles in the Caribbean and on the mainland. Workers on Caribbean anoles almost without exception adhere to the single genus framework, and work on Caribbean anoles has been extensive and is now well-known by the community at large. In contrast, mainland anole researchers are more divided, some favoring a single genus, others favoring multiple genera. It would be hard to compare the quantity and impact of work on Caribbean and mainland anoles and argue that recognizing multiple genera has accelerated research.

Finally, we might take a step back and ask: Is it still the case that big monophyletic groups must be broken up into little monophyletic groups to foster evolutionary research? This viewpoint may have been correct in the 1980’s when the cladistics revolution occurred, but is it really true, in this day and age, that researchers look to taxonomy to derive their evolutionary thinking? I would suggest that this is no longer true: with the huge explosion of phylogenetic thinking, modern researchers no longer look at taxonomic classifications to identify evolutionary groups; rather, they go straight to the phylogenies themselves. To see that this is true, pick up any journal and look at the evolutionary analyses. No one is basing their research on taxonomies; they are basing them on the phylogenies themselves, regardless of the binomial names appended to the terminal taxa. The argument that splitting up clades ever more finely to enhance research is old-fashioned, a hold over from the days when phylogenetic thinking was uncommon and many recognized groups were not monophyletic.

Still, Nicholson et al. are correct: it is the trend to ever more finely split up clades into smaller genera. Why should anoles be different? The answer is that there is an enormous, half-century of literature on these lizards that extends far beyond the fields of herpetology and systematics. Researchers in areas as disparate as physiology, cell biology, development and functional morphology, as well as evolution, ecology, and behavior, have conducted important work on anoles. And this work has been published using the name “Anolis.”

Nicholson et al. (2014) don’t even address the point raised by Poe and many others, that such name changes are more than disruptive, but truly damaging to scholarly research. In the herpetology course I teach, students are given a number of assignments that require them to go into the literature. And they have great trouble tracking down information on species whose names have changed. That’s not even accurate–usually they are simply unaware that there is a literature on a species under its former name. It would be nice to think that they would consult online resources that provide lists of the different names a species has had, but the students usually aren’t savvy enough (even though they are instructed to do so). In this regard, molecular biologists, physiologists and ethologists are no better than undergrads. If they read a paper on Anolis cristatellus from 1983, they will not know to connect that paper to a species now known as Ctenonotus cristatellus. Proponents of name changes tend to brush this under the rug, saying that people are adaptable and will cope, but this view is unrealistic.

Some day, all scholarly resources will be digital and species names will be automatically hyperlinked to their previous identities, but we are a long way from that point. And until that day, there are real costs to changing names, particularly for well-known groups with a long history of research. Given that research on Anolis is vibrant and phylogenetically informed, there is nothing to be gained and a lot to be lost by division into multiple genera.

Yesterday, I summarized the points made in Nicholson et al.’s recent Zootaxa rebuttal. To me, there are two main issues stemming from this paper. I’ll discuss the first today and the second tomorrow.

The first question is whether the eight proposed genera are monophyletic. There has been much criticism on this point in our pages and this was a central point in Poe’s critique. Nicholson et al.’s response strongly lays out their contention that all studies in recent times have found evidence for the same eight groups. They claim that there are very few species whose position is uncertain, not enough to worry about.

At this point, I personally don’t think it’s worth expending more effort arguing back-and-forth on this matter. Both sides have made their points. In a few years, we’ll have a lot more data on anole systematics and we’ll find out who’s right. If Nicholson et al. are correct that only a few species are in play (i.e., moved from one of their genera to another, as they have already done with A. christophei), then they’ll be vindicated. If they’re wrong and there are major upheavals to their preferred phylogeny, then their proposal will be seen as premature and misguided.

I don’t see the point in arguing this one any further.

For those of you who have been living under a rock for the last two years, here’s the short story. In 2012, Nicholson et al. published a monograph in Zootaxa on anole systematics and evolution that proposed dividing Anolis into eight genera. This paper has been much discussed and criticized in these pages (this might be a good place to start). In turn, Poe replied in Zootaxa with a critique widely considered to be overly aggressive in tone. Now, Nicholson et al. have responded to Poe in a nicely written rebuttal that for the most part clearly draws the lines on the areas of disagreement.

This Zootaxa paper is behind a pay-wall, so I thought it might be worthwhile to provide a summary of the main points of the paper in today’s post. In the next two posts, I will discuss what I see as the major issues moving forward.

I’ll summarize Nicholson et al.’s paper following their sections:

Introduction

The authors introduce the paper by citing Poe’s critique and stating: “We acknowledge that science benefits from vigorous, intellectual debate, but would have preferred his commentary to be more constructive, objective, and scientifically accurate. We therefore present this rebuttal to explain how Poe erred in characterizing our work, and missed the opportunity to present an alternative comprehensive taxonomy to replace the one against which he argues so strenuously. In this contribution we explain, and correct, Poe’s errors and misrepresentations, and argue that our taxonomy is likely to be adopted because it 1) eliminates the obvious problem that will arise if the family Dactyloidae contains only a single large genus (i.e., that a single genus obscures the evolution and diversity within the group and misrepresents or cloaks it), 2) conforms with the long historical trend of dissecting large, cumbersome groups into smaller sub-units, 3) is consistent with all recent phylogenetic studies for anoles in membership within clades we recognize as genera, and 4) aids in associating these lizards with the ancient land masses that shaped their history.”

I would only comment on this introduction by saying that criticizing Poe for not providing an alternative taxonomy seems off the mark. Poe made very clear what he thinks the preferred taxonomy is—one in which a single genus Anolis is recognized.

Monophyly and Anole Taxonomy

The paper begins by taking on the criticism that some of their eight genera are not monophyletic. They point out that for any group which has been the subject of multiple studies, there always will be some disagreements about clade membership. They review how they handled these disagreements: “We did not always follow one particular analysis or dataset (i.e., only follow the molecular data or only the Bayesian analysis) because, as systematists, we are all aware that there are always shortcomings in both the data and the analyses, especially when considering large, cumbersome groups. We integrated the available information to make these predictions, and these explanations are included in the systematic section for each group. Morphological and molecular data often disagree, and investigators are left to interpret those results.”

Character Diagnoses for Clades

This section rebuts Poe on a rather technical point about whether it is sufficient to cite diagnostic characters for a clade when those characters are identified from only one of many possible equally likely trees. Although an interesting debate, it is of minor significance compared to the bigger issues under discussion.

Recognition of Monophyletic Groups across Studies

This is the most important, and most original, part of the paper. The authors state: “Eight major clades are recovered in all studies that have broadly sampled anole taxa (Alföldi et al. 2011; Jackman et al. 1999; Nicholson et al. 2005; Poe 2004), including Pyron et al’s (2013) monumental reassessment of the Squamata. We classified these clades as separate genera because clade membership is so remarkably consistent among analyses, as is membership in 21 of 22 subgroups that we recognized within these genera (Figures 1–5). There are 12 species out of the 240 included in our combined molecular and morphological analysis that are unstable with respect to generic designation in our molecular-only tree, or other recent molecular-only phylogenies.”

Upon further examination of the 12 problematic species, the authors conclude that only “… 5 species that we placed in the genera Anolis (argenteolus, cyanopleurus, lucius, and spectrum) and Chamaelinorops (christophei) …may potentially, eventually, warrant different generic assignments than those we recommended.” Moreover, in a Note Added in Proof at the very end of the paper, the authors state “The recent analysis of several large datasets leads us now to recommend placing the species christophei into our genus Xiphosurus rather than in Chamaelinorops as we suggested in our 2012 paper.” This point refers to the recent papers by Pyron and Burbrink and Gamble et al., recently discussed in our pages (see comments). The authors conclude on this point: “Poe notes that node support for some of the eight major clades of anoles is weak, and concludes that more data are required to justify them. We continue to argue that the consistent recovery of eight dominant clades of anoles in multiple independent studies is sufficient justification for recognizing eight genera. In our view, the pattern is clear; the accumulation of additional data is going to recover these same eight genera.”

The most novel and important part of this paper is the figures 1-5, which show that, for the most part, the same eight clades have been detected time and time again. Here, for example, is the phylogeny from Jackman et al. (1999):

And here’s a comparison to Poe’s own work:

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Doc Frog (a.k.a. Cesar Barrio Amorós) has the most amazing balcony anywhere. Previously, we posted photos of Anolis biporcatus mating and A. charlesmyersi being beautiful, taken from that overlook. Now the good doctor reports photographs of anoles taken not from his balcony, but on his balcony. Specifically, two male A. limifrons in a tense encounter.

We’ve had posts in the past of other anoles sticking their tongues out in male-male encounters (e.g., A. fuscoauratus, A. stratulus). I wonder how widespread it is in the anole kingdom. I am unaware of any review of this topic, but the first place to start would be Schwenk and Mayer’s paper, “Tongue display in anoles and its evolutionary basis,” published in Anolis Newsletter IV.

Who else can report tongue use in anole displays?