Author: Jonathan Losos Page 57 of 133

AA‘s man in Wisconsin, Greg Mayer, filed this report:

In Ernest E. Williams’ 1969 classic on the ecology of colonization, he identified Anolis cristatellus as one of the ‘minor colonizers’– not as widespread as carolinensis and sagrei, but having close relatives on Mona, Desecheo, and the Turks and Caicos. This natural colonization has now been augmented by human introductions– including Florida, Costa Rica, and the Dominican Republic, so that it is moving up on the colonization hit parade. In many of these places (e.g. Miami, Limon, Costa Rica), they have become established in highly human modified habitats.

Another sort of invasion has been taking place within Puerto Rico, as Kristin Winchell of U. Mass., Boston, has reminded us– cristatellus is also occupying (and thriving in) urban habitats in the densely populated parts of Puerto Rico. In her talk, coauthored by Graham Reynolds, Sofia Prado-Irwin, Alberto Puente-Rolon and Liam Revell, she shows that urban habitats present many challenges to anoles. The typical urban habitat is full of man-made surfaces (wood, masonry, glass, metal, oftrn painted), there is little or no canopy, the ground is made up largely of impermeable surfaces (so water runs of quickly), all of which lead to urban habitats being hotter, drier, and quite distinctive compared to the natural forest and woodland habitats. And let’s not forget the cats–all those awful, lizard-eating cats! (Apologies to Jerry Coyne!)

Kristin and company supposed, naturally, that all these environmental differences could lead to fairly intense selection for local adaptation. In particular, they supposed that city lizards should have longer legs (because running on larger, flatter surfaces is done better with longer legs), and that they would have more toe lamellae (to deal with the slippery, texture-less artificial surfaces, where claws are less effective for grip).

They tested these predictions at 3 paired sites near San Juan, Ponce, and Mayaguez (the natural site in San Juan was labeled by a sign at the site as “Una esmeralda verde en un mar de cemento”!) They confirmed their environmental characterization of cities, and found, as expected, that lizards perched on wider surfaces, did have more lamellae, and had longer legs–a resounding success. Interestingly, they did not find a change in perch height distribution between urban and natural. My one query would be about the change in lamellae number. High lamellae number is associated with narrower perch diameters– the numerous lamellae allowing the toepad to curl round to conform to the curved shape of the narrower perch (as shown in trunk crown anoles having more lamellae than similar-sized trunk ground anoles). I’ll have to think about what exactly I would expect in a trunk ground lizard adapting to man-made surfaces.

Kristin mentioned that they are planning a common garden experiment to test whther the differences have a genetic basis, as opposed to representing phenotypic plasticity. So we can look forward to more interesting results from this project.

Alex Gunderson asked the question: What ecological axes are involved in ecological divergence during adaptive radiation, and what phenotypic traits occur along them?

Here are the specific questions he investigated:

Alex pointed out that we usually talk about the ecomorphs that have diverged to use different parts of the structural habitat (e.g., twigs, canopy, grass, etc.), but less attenion is paid to divergence along the thermal niche axis, yet since Ruibal’s work in the early 1960’s, we’ve known such divergence occurs. Morphological divergence allows species to coexist by using different structural microhabitats; does divergence in thermal physiology have the same effect?

Most of the research involved the Puerto Rican cristatellus group, in which there are four pairs of sister species that differ in thermal environment, one more in the sun, one more a shade species. Some data also included Jamaican anoles. The study focused on two aspects of physiology related to thermal niche use, the critical thermal maximum temperature (CtMax) and the optimal temperature for sprint performance (Topt).

Results: In 3 of 4 sister taxa, the species in the warmer environment had a higher CtMax. In 2 of 4, the species had a higher optimal temperature (in both cases, in the other comparisons, the species did not differ statistically).

Q2: What are the performance consequences of physiological divergence?

Alex measured temperatures in shaded and open habitats and asked what the risk was of a species overheating in each habitat. In shaded habitats, no species were at risk of overheating, but in open habitats, for three pairs of sister taxa, the species from the cooler environment was at greater risk of lethal overheating.

Q3: Does physiological divergence promote species co-occurrence?

In cases where morphologically similar species co-occur (same ecomorph), do they diverge in physiology? The answer: Invariably yes in Puerto Rico and Jamaica. When morphologically similar species co-occur, they always differ in thermal physiology. Thus, thermal physiological differentiation seems to be important for increasing local species richness.

Q4: How quickly does physiology evolve relative to morphology?

Surprisingly (at least to me), physiology evolves considerably more slowly than morphlogy.

Summarizing across this work, Alex concluded that physiological differentiation may be an important component of adaptive radiation. In many cases, workers studying adaptive radiation focus on morphology for a number of reasons, not the least of which that it is much easier to measure. But, by doing so, they may be missing an important part of the puzzle.

Liam Revell gave a talk entitled “Placing cryptic, recently extinct, or hypothesized taxa in an ultrametric phylogeny using continuous charater data: a case study.” The title pretty much says it all and is a report on an ongoing project conducted with Luke Mahler, Graham Reynolds, and Graham Slater (sorry, I failed to think of anything clever about two authors named Graham. S’mores, anyone?).

The problem being addressed: we have a phylogeny for a group and want to add a taxon for which we only have continuous data, such as leg length, etc. How can we place it on the tree?

The details are too technical for me to summarize (note: if you want to get to the good, anole stuff and don’t care about the method, skip to the next paragraph), but entails using a likelihood formula that Felsenstein developed for building trees with continuous characters (another note: you must have continuous characters for all taxa). The method works by considering all possible placements of the missing species. It computes the likelihood of the model and tree conditioned on the dataset to find the maximum likelihood tree including the taxon of interest that is consistent with the tree based on nuclear data for the other taxa (note that the tree must be ultrametric). Liam reported that even for trees with 100 or more taxa, an approximately exhaustive search for the ML position of the tip taxon is possible. Because the tree is ultrametric, all we’re interested in is where the attachment on the tree occurs, because the branch length is then determined by the ultrametricity of the tree.

Liam assured the audience that the drawing was not of co-author Graham Slater

Now for the good stuff: the method was illustrated with regard to Anolis roosevelti, the feared-extinct crown giant anole of the Puerto Rican bank. Known from only eight specimens and last collected in the 1930’s, things don’t look good for roosevelti. It has been assumed to be closely related to the Puerto Rican crown-giant, A. cuvieri, which it does look like. Moreover, Steve Poe’s morphological phylogeny supports this placement.

The analysis can reject many potential placements of roosevelti, but many others are not ruled out statistically; i.e., the likelihood surface is flat particularly close to root of tree, not surprising given the extensive morphological convergence of anoles. However, for what it’s worth, placement of roosevelti as a close relative to cuvieri is ruled out.

It will be interesting to see how this project develops and whether these results hold. More importantly, someone needs to go out and find a living roosevelti.

Travis Ingram in the field

At each of the Evolution meetings over the last few years, anole researchers have been honored with some of the major awards  (1, 2, 3) recognizing talented young scientists. That trend continued here in 2014, when Travis Ingram was named as one of the winners of the  American Society of Naturalists’ Jasper Loftus-Hills Young Investigator Prizes.

Travis made a 30-minute presentation on his work on adaptive radiation. This work has combined the development of new analytical methods along with detailed analysis of two systems, our beloved anoles as well as Pacific rockfishes. In particular, Travis spoke about research investigating two questions: the extent to which adaptive divergence occurs specifically during speciation events, and the degree to which within adaptive radiations, convergent evolution occurs to the same adaptive peaks. In considering this work, Travis also discussed the difference between what are called “alpha” niches, which refers to ecological differentiation between co-occurring species, and “beta” niches, which refers to ecological differences across a landscape or environmental gradient.

Travis first discussed the method in to determine the extent to which morphological variation among species evolved during speciation. Travis has already published work on rockfishes that shows that substantial proportions of morphological variation among species appears to have evolved during the speciation process. He then discussed new work asking the same question in anoles, which shows that variation in traditional ecomorph traits—related to differences in structural habitat use—seem to be little correlated with speciational evolution. In contrast, climatic niche evolution—the divergence that arises within ecomorph clades—seems to be largely speciational.

Travis then switched gears to discuss research on convergent evolution within adaptive radiations, for which he and colleagues have developed a new method, Surface. Application of this work to Greater Antillean anoles—published in Science last year—shows that there have been 29 peak shifts in anoles, that there are 15 separate adaptive peaks, and that eight of these peaks have been occupied convergently. Moreover, Travis pointed out that even though the method does not start out with a priori categorization of species to ecomorph, the tradition ecomorph categories are for the most part recovered in the analysis, with some exceptions.

Travis then presented new work applying the same method to rockfish radiations on both sides of the Pacific in the northern hemisphere. Again, many convergent peaks were found; however, of the nine convergent peaks, eight were occupied by multiple lineages with a lineage, and only one occupied by lineages in both regions. This work was published this year in the American Naturalist.

Travis summarized by noting the interesting differences found in the two aspects of adaptive radiation he studies. His work indicates that axes related to environmental gradients, i.e., the beta niche illustrating differences across space, are related to speciational evolution, whereas traits related to alpha niche (microhabitat partitioning) are related to convergence within radiations.

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:

Read More

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?