Author: Jonathan Losos Page 54 of 129

Battling anoles. Image Credits: Ken King // Dixie Native

The St. Augustine Record published a very nice article two weeks ago discussing the invasion of brown anoles, A. sagrei, and how they’ve affected green anoles. But instead of the usual alarmist hysteria–green anoles being pushed to extinction–this article pretty much gets it right!

“…the invasion of the brown anoles have chased the natives into the treetops. The brown anoles, having few enemies, have taken over the former habitat of the greens, forcing them into new territories and farther from our sight.”

That’s right–the green anoles aren’t going extinct, they’re just shifting their habitat use to get away from the browns. The only quibble I would have is that this is not really “a new territory” because not only have green anoles in Florida been using high perches all along, but that’s what their ancestors in Cuba, who’ve always lived with brown anoles, have always done.  Green anoles experienced what’s called “ecological release” when they got to Florida and found it brown anole-less; now they’re simply returning to their ancestral niche.

For more on this topic, see previous AA posts [e.g., 1, 2, 3].

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?

Convergent evolution is Anolis Lizards’ middle name, and so it is with great interest that we read two brand-spanking new papers on convergent evolution. The first is by  Arbuckle et al. out of the University of Liverpool. Published in Methods in Ecology and Evolution, the paper describes a new method for quantifying the strength of convergent evolution. You’ll have to read the paper for the details, but the gist of the method is that convergence is greatest either when species are greatly different phenotypically from other species or when the convergent species are distantly related phylogenetically.

And the focal taxon used to demonstrate the method with empirical data? Why, none other than Greater Antillean ecomorphs. The paper found that in “In Anolis lizard data set, perhaps the most notable finding is that ecomorphs differ in the strength of their convergence—grass-bush and trunk-ground anoles stand out as having particularly strong convergence compared to others. Furthermore, some traits are more strongly convergent within some ecomorphs but not others. Therefore, patterns of convergence in particular traits are ecomorph specific.” Specifically, “analyses found the strongest convergence in limb length occurred in grass-bush anoles compared to the other ecomorphs, consistent with Losos’ (1990b, 2009) finding of relationships between limb length and jumping and sprinting (perhaps particularly important for grass-bush anoles). The strong convergence of lamellae number detected in trunkground anoles suggests that there is a notable degree of adaptation in this trait.”

The abstract of the paper is appended at the bottom of this post.

Meanwhile, in a non-anole example, Collar and colleagues, in a paper in the American Naturalist, looked at convergent evolution in snail-eating moray eels. The authors found that the durophagous eels evolved in generally the same direction morphologically relative to their non-snailivorous relatives, but that there was substantial variation among the shell-crackers, actually more variation than seen among their relatives.

The authors explain this “imperfect convergence” in this way:  “we show that following 10 transitions to durophagy (eating hard-shelled prey) in moray eels (Muraenidae), cranial morphology repeatedly evolved toward a novel region of morphological space indicative of enhanced feeding performance on hard prey. Disparity among the resulting 15 durophagous species, however, is greater than disparity among ancestors that fed on large evasive prey, contradicting the pattern expected under convergence. This elevated disparity is a consequence of lineage specific responses to durophagy, in which independent transitions vary in the suites of traits exhibiting the largest changes. Our results reveal a pattern of imperfect convergence, which suggests shared selection may actually promote diversification because lineages often differ in their phenotypic responses to similar selective demands.”

Such imperfect convergence is not unknown among anoles. For example, Langerhans et al. showed that despite the convergence among the ecomorphs, there were also island-specific effects that produced variation among members of an ecomorph. Moreover, a larger scale example is the comparison of mainland and Greater Antillean anoles. Is the lack of convergence due to environmental differences, or is it an example of species evolving different adaptations to living in the same environment?

Exciting times for those of us interested in convergent evolution!

The abstract of the Arbuckle et al. paper:

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And it’s a looker!

The species, described recently in Amphibian & Reptile Conservation by Fernando Ayala-Varela and colleagues, comes from the western slope of the Andes in Ecuador. In appearance, it’s most similar to A. gemmosus, which occurs to the north. Detailed examination shows it to be most phenotypically similar to that species and A. otongae, and DNA analysis indicates that A. gemmosus is its sister taxon.

Check out the paper, which has lots of lovely photos not only of the new species, but of some of the species with which it is sympatric.

Courtesy Nirvana Reptiles

Gunther Köhler has just published a paper in Zootaxa describing the many characters used in anole species descriptions. Here’s how he explains the endeavor:

“Anolis are important research organisms and many articles are published every year dealing with different aspects of the biology of these lizards. However, at this point we still lack detailed and standardized descriptions of all recognized species of Anolis. The species descriptions found in original descriptions, reviews of species groups, or faunal treatments are extremely heterogeneous in regard to content, usage of terms, semantic issues, and characters included. For example, some authors (e.g., Underwood & Williams 1959; Savage & Villa 1986; Köhler 2008) count the number of subdigital lamellae under Phalanges II–IV whereas others (e.g., Schwartz 1973; Williams 1995; Poe et al. 2012) report only the lamellae under Phalanges II and III. Even when the same characters are reported, often differences in definitions are evident with different authors scoring the same character differently, i.e., having different threshold levels for scoring qualitative characters (e.g., whether to consider a scale to be smooth, faintly, or weakly keeled, or not, slightly or distinctly enlarged relative to adjacent scales). Also, the way the data are generated can differ widely depending on the applied methodology. In 1995, Williams provided definitions for 37 morphological characters intended for usage in a computerized key for anoles. Williams’ (1995) approach aimed mostly to bring definitions and encodings of morphological characters usable in a computer program. Therefore, he was forced to simplify many of the included character states thereby masking the extent of variation actually observed in the genus Anolis. This article aims to provide definitions of external morphological characters that are useful in Anolis taxonomy with the goal of establishing a reference for future taxonomic work with these lizards. I am confident that a description containing the set of characters defined here will be reasonably complete for the majority of species. In species that show special morphological differentiations (such as the rostral appendage in A. proboscis), these special features need to be addressed of course. I have included many images illustrating the variation in the characters discussed, although I do not attempt to provide a comprehensive review of the variation in external morphology in anoles.”

A variety of morphometric characters from snout-vent length and head width to postcloacal scale width. Here’s one as an example:

Diameter of parietal scale. The longitudinal (LDP) and transverse (TDP) diameters of the parietal scale are measured. LDP and TDP both are measured at the greatest length and width, respectively. Slender projections of the parietal scale should be ignored in cases where these are beyond the normal concave or convex outline of the scale.

The heart of the paper is a description of a large number of scalation characters and their various alternative states. For example:

Condition of supraocular scales (CSO). These vary from smooth or rugose to weakly or strongly keeled; keeling can be uni- or multicarinate. Examples are given in Fig. 12.

Condition of circumorbital scales (COS). In many species of anoles, a row of small scales separates the enlarged supraocular scales from the scales of the supraorbital semicircles. Thus, this character refers basically to the scales situated medially to the enlarged supraocular scales; laterally to the enlarged supraocular scales usually numerous small scales are present without differentiated scales that can be identified as circumorbitals. Considerable intra- and interspecific variation can be observed in this character as exemplified in Anolis dunni (Fig. 13) with the circumorbital series varying from complete (one or more rows of scales) to incomplete or absent. Whenever one or more enlarged supraocular scales are in contact with scales of the supraorbital semicircles, the circumorbital series are incomplete or absent.

And one more set of examples:

Number of scales between supraorbital semicircles (IO). In most species of anoles a pair of semicircular series of enlarged scales is present in the frontal region between the supraocular discs. The minimum number of scales between the supraorbital semicircles is determined (i.e., usually at the narrowest point; Fig. 22).

Number of scales between supraorbital semicircles and interparietal plate (IP/IO). The minimum number of scales between the supraorbital semicircles and the interparietal plate is determined (Fig. 22). This character obviously is ignored in species that lack a differentiated interparietal plate (e.g., Fig. 22B).

Size of scales adjacent to interparietal plate (ScIP). The relative size of the scales surrounding the interparietal plate is noted. In some species the size of the scales anterior to the interparietal plate differs from those situated posteriorly to it. See examples in Fig. 22.

This looks to be a very useful contribution, particularly as the number of newly described anoles continues to rise.