Evolution 2014: Survival of the Fattest? Body Condition Not Related to Fitness in Lizards

Screen Shot 2014-06-24 at 9.52.48 AM Robert Cox, from the University of Virginia, presented his work examining the relationship between fitness and body condition in Anolis sagrei from the Bahamas. Many evolutionary biologists want to understand selection in wild populations. But in order to do that we need to measure fitness. Finding out who survives to maturity, who finds more mates, and who produces the most viable offspring, however, is quite difficult. For this reason, many researchers use body condition, or the ratio of body mass to body size, as a proxy for fitness.

One of the issues with using body condition as a proxy, however, is that it varies a lot, even within the same individual! When resources are plentiful, even less fit individuals can fatten up. And, when the going gets tough, even vigorous individuals fare poorly. For his study, Bob wanted to know whether body condition was actually a good proxy for fitness. He did this by actually measuring fitness in the wild by tracking survivorship in A. sagrei from the Bahamas. Most studies examining survivorship are performed over a single season or a few seasons, but Bob managed to gather data for 41 estimates of selection over 10 years of work. The numbers are impressive: He tracked survivorship over the summer, which is the height of the reproductive season, for 4,608 adults from 7 populations.

What he found was surprising – it turns out that, in these populations of A. sagrei, fatter is not fitter. He found no evidence for selection favoring better body condition in males or in females. He did find, however, strong selection for body size, rather than body condition. He also found correlational selection on body condition and body size – Specifically, he found that body condition did matter, but only in really large males. But this effect only explained a small proportion of the residual variance. The selection on body size, he found, was much stronger.

Bob’s work emphasizes that we, as a community, need to be wary of the traits that we use as proxies for fitness. In the case of A. sagrei, it didn’t matter what condition the lizards were in, except in the case of larger lizards. However, survival is only one piece of the fitness puzzle. To know how body condition influences fitness, we would ideally also want to know whether fatter individuals gain more access to mates and produce more viable offspring (i.e., more fecund). Together, Bob’s work highlights the importance of body size in survivorship and provides new evidence that fitness proxies need to be experimentally verified before being widely applied.

Evolution 2014: Physiological Divergence and Adaptive Radiation


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.

Evolution 2014: A New Method for Placing Species of Interest that Lack DNA on a DNA-Based Phylogeny, Illustrated by Anolis roosevelti


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

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.

Evolution 2014: Cold Tolerance and Desiccation Resistance in Anolis sagrei

Mean CTmin for invasive (gray) and native range (green) populations of Anolis sagrei.

Mean CTmin for invasive (gray) and native range (green) populations of Anolis sagrei.

Most anole enthusiasts are familiar with the brown anole, Anolis sagrei, because it is a highly successful invader. Although it can be found as far away from its native Cuba (and nearby islands) as Hawaii and Taiwan, most of what we know about invasive populations of this species come from work conducted in Florida. A recent study by Jason Kolbe and colleagues demonstrated that physiological traits vary with latitude in A. sagrei from Florida. Specifically, cold tolerance (CTmin) and desiccation resistance were lowest at higher latitudes in Florida. Tamara Fetters, a graduate student in Joel McGlothlin’s lab at Virginia Tech, supplemented this work by adding data from a native population of A. sagrei found on the island of San Salvador in the Bahamas.

Box plots showing rates of evaporative water loss in invasive (gray) and native range (green) populations of Anolis sagrei.

Box plots showing rates of evaporative water loss in invasive (gray) and native range (green) populations of Anolis sagrei.

Tamara found that mean CTmin for A. sagrei from the Bahamas was close to 12°C, which was significantly higher than in Tifton, the most northerly population from Jason Kolbe’s study, but not significantly different from the lower latitude populations in Orlando and Miami. Similarly, she found that desiccation tolerance in native range A. sagrei was significantly higher than in lizards from Tifton, a result that she attributes to the lower relative humidity found at higher latitudes in Florida. Tamara’s future goals include measuring more physiological traits, such as oxygen consumption and heat tolerance (CTmax), along with morphological traits associated with desiccation resistance (scale number and scale area), for various invasive and native populations of Anolis sagrei.

Evolution 2014: Travis Ingram Receives Young Investigator Prize for Research on Adaptive Radiation

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.

Evolution 2014: Ecomorphological Analysis of Scale Number in Anoles

Hanna Wegener talks about Anolis scales at Evolution 2014.

Hanna Wegener talks about Anolis scales at Evolution 2014.

Talks are underway at Evolution 2014 and anoles are already off to a strong start! Early this morning, Hanna Wegener, a Ph.D. student at the University of Rhode Island, discussed some of her work on the diversity in scale size in Anolis lizards. The work she presented was conducted in collaboration with Gabe Gartner and Jonathan Losos from Harvard University. Hanna started by discussing the adaptive radiation of anoles in the Caribbean. As a community, she said, we know quite a bit about how certain morphological traits, namely skeletal dimensions and lamella counts (i.e., number of toe pad scales) differ among ecomorphs and among different climatic habitats. Scale number, however, remains comparatively unexplored in anoles. For her study, Hanna examined ventral and dorsal scale counts in anoles. Her sampling strategy was impressive – by mining the collections in the Museum of Comparative Zoology at Harvard University, she was able to get scale counts for well over 100 anole species, and Caribbean anoles were particularly well represented in her dataset.

She first sought to examine the relationship between scale number and climate. There are prevailing ideas regarding how scale size and number should relate to climate. Specifically, Michael Soulé and Charles Kerfoot have posited that larger scales are advantageous in hot environments because their greater surface area increases radiative efficiency. Larger scales are also thought to reduce water loss in dry environments. Thus, lizards in hot, dry environments should have fewer, larger scales than lizards in cool, wet environments. Hanna found a positive relationship between scale number (both dorsal and ventral) and precipitation, but she did not find a significant relationship between scale number and temperature.

Hanna showing the variation in scale number and size among anoles. The top two rows show dorsal scales, whereas the bottom two rows show ventral scales.

Hanna showing the variation in scale number and size among anoles. The top two rows show dorsal scales, whereas the bottom two rows show ventral scales.

Hanna then asked whether scale number relates to structural microhabitat use. Here the study became much more exploratory and exciting because, if there is little known about the relationship between climate and scale number, there is even less known about the relationship between scale number and microhabitat use. Hanna found significant differences among ecomorphs in scale number. She found that higher perching ecomorphs, such as crown-giants and trunk anoles, tended to have more, smaller scales. Lizards that perched lower and used broad surfaces, such as trunk-ground species, tended to have fewer, larger scales. Although the precise mechanism underlying this relationship remains unknown, Hanna posited that aspects of microclimate, such as temperature, might vary with structural habitat, which may in turn drive scale number patterns. She also suggested that the observed patterns of scale number variation might represent correlated evolution, such that scale number covaries with a trait that relates to differences in structural microhabitat use. Hopefully Hanna’s study leads to more research on the significance of scale number in anoles and other lizards.

Newspaper Article on Brown Anoles Affecting Green Anoles Gets It Right

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].

A Doubly Regenerated Tail and Other Morphological Oddities

I’m doing fieldwork with Anolis sagrei in Gainesville, FL, this summer. We now have about 125 lizards  measured and marked, and have come across a number of interesting morphological oddities in these lizards. Most interesting so far is this doubly regenerated tail, i.e. there appear to be two spots at which the tail has regenerated, which means a regenerated tail must have broken and regenerated again.

A doubly regenerated tail in a male Anolis sagrei in Gainesville, FL.

A doubly regenerated tail in a male Anolis sagrei in Gainesville, FL.

Approximately three minutes before we noticed this tail, my field assistant Christian Perez asked me if double regenerations were possible, and I confidently said “no.” As Jonathan Losos puts it in Lizards in an Evolutionary Tree, “when a tail regenerates, the new portion of is made of a rod of cartilage and thus lacks the intravertebral breakage planes that enable an unregenerated tail to autotomize.” So how did this double regeneration happen? Anyone seen this before?

The next oddity is this male with a mysteriously shortened upper jaw:

A shortened upper jaw in a male Anolis sagrei in Gainesville, FL.

A shortened upper jaw in a male Anolis sagrei in Gainesville, FL.

Third, we have a partially discoloured dewlap:


A discoloured dewlap in Gainesville, FL

A discoloured dewlap in Gainesville, FL

And finally, here’s an addition to our collection (1, 2) of multiply tailed lizards:

A double tail in an Anolis sagrei in Gainesville, FL.

A double tail in an Anolis sagrei in Gainesville, FL.


Which Puerto Rican Anoles Are These?

A few weeks ago I had the opportunity to visit Puerto Rico for the first time, albeit briefly. Fortunately, a lot of anoles can be found even on a brief visit. With the help of caribherp.org and other references, I could identify most of them. I was hoping to get some help from the knowledgable readers of Anole Annals on the rest. I suspect they are mostly all juvenile Anolis cristatellus cristatellus, but the appearances are varied enough that I couldn’t be sure. Any ID help is greatly appreciated!

Small brown anole at Cueva Maria de la Cruz, Puerto Rico

Unidentified Anole #1:  Cueva María de la Cruz

This small brown anole and a couple of similar-looking buddies were dashing about on a large tree trunk at the edge of a grassy clearing at Cueva María de la Cruz. This small cave is in northeast Puerto Rico, near the coast, north of the western edge of El Yunque National Forest. I saw adult Anolis cristatellus cristatellus in smaller trees nearby, so it seems likely that this is a juvenile, though its pattern looked non-standard to me.

Continue reading Which Puerto Rican Anoles Are These?

Do Communities of Introduced Anoles Differ from Natural Communities?

Anolis cristatellus awakened on a leaf. Photo credit: Tom Kennedy, University of New Mexico.

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. Continue reading Do Communities of Introduced Anoles Differ from Natural Communities?

Please Help Us Make the Sungazer the National Lizard of South Africa

Cordylus giganteus

South Africa has various national wildlife symbols:

National animal – the springbok (Antidorcas marsupialis)

National bird – the blue crane (Anthropoides paradisia)

National fish – the galjoen (Dichistius capensis)

National flower – the king protea (Protea cynaroides)

National tree – real yellowwood (Podocarpus latifolius)

Now, I would like to appeal to Anole Annals readers to help get the sungazer, Smaug giganteus (formerly Cordylus giganteus), formally recognized as South Africa’s national lizard by the Department of Arts and Culture. This would promote the conservation of this species, but by using it as an umbrella species, the conservation of their grassland habitats would also benefit various other organisms. It will only take a few minutes of your time. Just visit and sign the petition at: https://secure.avaaz.org/en/petition/Department_of_Arts_and_Culture_Make_Sungazers_South_Africas_national_lizard/.

The Swinhoe’s tree lizard (Japalura swinhonis) is a common endemic lizard species in Taiwan.

The Swinhoe’s tree lizard (Japalura swinhonis) is a common endemic lizard species in Taiwan.

Wouldn’t it be great if we could get a national lizard nominated for every country?

I nominate the Swinhoe’s tree lizard (Japalura swinhonis) for Taiwan.

Which anoles would you nominate for which countries?

The Battle over Anole Classification Ignores the War

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.


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.

Evolutionary Taxonomy Meets Phylogenetic Systematics: Maybe 8 Genera Isn’t Enough for Anoles

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!

Dewlap Plus Tail-wagging in Anolis cristatellus wileyae

Anolis cristatellus wileyae on St. Thomas wagging its tail as it shows its dewlap.

Crack that whip!

This proud Anolis cristatellus wileyae had snuck into the Butterfly Farm a few minutes’ walk from the cruise port in St. Thomas, U.S.V.I. So had a few dozen of its conspecifics, but this was the only one showing off its pretty two-toned dewlap while lashing its tail back and forth dramatically. Perhaps this is a common behavior, but it’s not one that I had seen before. Do other anole species also do this kind of double-showoff?

If It Ain’t Broke, Don’t Fix It: Why Splitting Anolis Is a Bad Idea

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.

Are the Data Sufficient to Split Anolis into Eight 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.

The Battle Over Anole Classification Continues

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:


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):

comparison to Jackman et al

And here’s a comparison to Poe’s own work: Continue reading The Battle Over Anole Classification Continues

Anoles (and Other Lizards) at SMBE 2014

SMBE2014-600x360The annual meeting of the Society for Molecular Biology and Evolution meetings start this weekend in San Juan, PR and there are a number of talks and posters to appeal to the squamatophile.

There are three presentations from AA contributors (Marc Tollis and Tony Gamble) using anole genomic data, as well as posters and talks on phylogeography of Puerto Rican Sphaerodactylus, and genome-scale studies of Sceloporus, skinks, and snakes. You can see the full list after the jump.

Continue reading Anoles (and Other Lizards) at SMBE 2014

Tongue Protrusion in Battling Male Anolis limifrons

limifrons displaying doc frogDoc 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. fuscoauratusA. 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?

limifron males combatting doc frog

New Papers on Convergent Evolution

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.

collar figure

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: Continue reading New Papers on Convergent Evolution