Category: New Research Page 47 of 67

Nicholson et al. recently undertook the bold mission of revising the taxonomy of our well-loved lizard genus, Anolis, based on the phylogenetic relationships among its many species. Not surprisingly this has struck a nerve with much of the anole community spawning a range of reactions immediately following its publication, some applauding their efforts but many expressing their concerns about the proposed change. If one of the author’s objectives was the generate discussion on this topic its clear that they have succeeded.

The Nicholson team should first be commended for their efforts to synthesize the historical literature on anole taxonomy, encompassing “387 recognized species and 112 additional nominal subspecies” with some reports dating as far back as the mid-1600s. This survey will likely serve as a benchmark for later systematic evaluations of this genus. However, the implications for their proposed revision extend well beyond the nuances of taxonomic rule or the analytical methods used to build phylogeny*. The issues arising extend into other biological disciplines and potentially undermine the rich intellectual history of anoles.

I, like many others, am a consumer of taxonomy and systematics. These are critical to the comparative analyses I perform and in communicating my findings to others in the anole community, herpetologists more generally, and other biologists more broadly still. Anolis has been a model for comparative biology for decades but is gaining increased attention by genomicists, neuroendocrinologists, and developmental biologists. Just this year, in fact, the anole community developed a system with which to share comparative molecular resources. Deconstructing Anolis into eight distinct genera could drive an intellectual wedge between the previously published literature and future studies, potentially derailing the continuity of information that is critical for academic advancement. This change could lead to unforeseen consequences that damage the broad utility of Anolis among biological disciplines that depend on the stability of anole nomenclature.

Nicholson et al. state, “the role of systematics is to advance our understanding of biological diversity.” While I agree with this statement in principle I feel that it is also important to ask if the benefits of revising this diverse taxon outweigh the risks I outlined above. The glaring disconnect between phylogenetic systematics and Linnean ranks is discussed at great length elsewhere and will be strategically avoided here. It is worth asking, however, whether the addition of new genera (specifically genera, not simply clade names) add anything new to our biological understanding of this group. Ultimately, can we more accurately communicate our findings using the revised nomenclature? While Nicholson et al. use monophyletic clades to distinguish the proposed genera  – a well respected practice – the precise breaks are biologically arbitrary. In my opinion the suggested genera do not offer greater clarity to the natural history of this clade as they do not partition Anolis based on distinct biogeographic groups, groups with distinct ecologies, or groups with distinct, readily recognizable morphological features. In this proposed taxonomic scheme the ecological and morphological convergence of Anolis ecomorphs** that is widely discussed and cited throughout ecological and evolutionary literature becomes a confusing hodgepodge of convergent lineages from different genera. In my opinion it is overwhelmingly clear that the benefits of re-classifying Anolis lizards do not outweigh the ensuing upheaval of our research community.

At face value it appears that the overall motivation for revising Anolis is its diversity, as it is undoubtedly one of the most diverse tetrapod genera. However Anolis pales in comparison to many invertebrate genera. The beetle genus Agrilus (jewel beetles) has an estimated 2886 species! Drosophila – the genus that possesses the genetic and developmental powerhouse D. melanogaster – contains approximately 2000 species***. It is clear that large, active research communities can readily work with diverse genera without problematic communication of their results. The sole argument of diversity is not strong justification for revising Anolis.

Perhaps some day taxonomy will abandon the binomial naming scheme derived from the Linnean classification hierarchy in favor of a more accurate system based solely on phylogenetic systematics. However, for practical purposes, we are simply not there yet. Anolis serves as a great example of where premature taxonomic revision could have far reaching consequences that can send biological research in multiple disciplines into severe turmoil.

Comments and discussion on the ideas I have shared above are welcomed and encouraged!

* This is not the say that critical evaluation of phylogenetic methods are not essential to the evaluation of taxonomic hypotheses. I will save evaluation of the Nicholson et al. analyses to those with greater experience working this these methods and those with an intimate knowledge of the proposed species groups.

** Beyond their proposed taxonomic revision the Nicholson team also reject the Anolis ecomorph concept. This idea will no doubt attract additional attention from the community.  Stay tuned to Anole Annals for more on this issue.

*** A similar discussion to ours recently took place in the Drosophila community and many of these same concerns were expressed. O’Grady and Markow 2009 state that “such radical taxonomic revision is not advisable…as the literature and traditions are
so well established that any such formal reassessment would not be worth the confusion engendered.” After review and comments from the community the ICZN voted that taxonomic revision of Drosophila was “premature” and wisely left this diverse genus intact.
KIRSTEN E. NICHOLSON, BRIAN I. CROTHER, CRAIG GUYER & JAY M. SAVAGE (2012). It is time for a new classification of anoles (Squamata: Dactyloidae) Zootaxa, 3477, 1-108

We’ve had a week now to let the proposed reclassification of Anolis sink it, so it’s time to start discussing it. A revolutionary new view of the scientific review process suggests that in the future, all papers will be published open access online (as this one is–thanks Nicholson et al.), the journal in which it appears (if any) will not matter, and peer review and evaluation will be conducted post-publication on internet discussion sites. Realistic? Who knows, but why not give it a try?

The paper by Nicholson et al. is undoubtedly the most important paper on anoles to be published in the last several years. Not only does it propose to split Anolis into eight genera, but it also presents provocative findings about the ecological evolution of anoles (including throwing out the ecomorph concept), anole biogeography, and the dating of evolutionary events in anole history.

Anole Annals’ goal is to be the meeting place for discussion of all things Anolis, so let’s take this post-publication review and commentary idea out for a spin. Anole Annals invites members of the anole community to post their thoughts on any aspect of the Nicholson et al. paper. We hope to get a conversation going on the merits of splitting the genus, as well as the other issues raised in the paper. In fact, this has already begun, as evidenced by the comments by Mssrs. Crother, Hillis and Duellman, among others.

To get the ball rolling, here’s a short précis of the paper:

1. Phylogenetic analysis based on previously published data of all sorts (genetic, morphological, karyological), with a smidgeon of new molecular data, reveals a phylogeny with eight strongly supported clades in a Bayesian analysis. These clades are recognized as distinct genera.

2. The ecomorph concept does not apply to mainland anoles because species similar in habitat use are not similar in morphology. Hence the term “ecomode” is coined for species similar in habitat use. Phylogenetic analysis of ecomode evolution on the phylogeny suggests that the crown-giant ecomode is ancestral for Anolis. The ecomorph concept is argued to not work for Greater Antillean anoles and should be discarded.

3. Biogeography is reconstructed on the phylogeny. Using the phylogeny, the authors argue that the eight clades differentiated about the time that the proto-antillean islands were passing between what is now North and South America. The Norops clade differentiated on several of these blocks (both island and mainland), explaining why Norops is nested within Caribbean non-Norops taxa without requiring the island-to-mainland colonization of Norops proposed by a number of previous papers.

4. Molecular clock dating reveals that anoles are surprisingly ancient, originating in South America approximately 130 million years ago.

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

An interesting paper in 2009 showed us that jumping without a tail can be a disaster for green anoles. In that paper, the authors found that the bodies of tailless individuals often underwent extensive posterior rotations in the air, resulting in very awkward landings. Moreover, tail regeneration can take months to complete, which implies that losing stability in the air may not be a short term situation. So we wondered: can green anoles quickly improve in-air stability, or do they just have to wait until they have their tails back again? To address this question, we tested in a recent study whether tailless green anoles can improve in-air stability in five week’s time and whether gaining more jumping experience facilitates the improvement.

We found that there was extensive variation in how much an individual could improve within five week’s time. By the end of our study period, some individuals showed no sign of improvement,

httpv://youtu.be/aTfui2FlC9Q

whereas others did improve their in-air stability as time went by.

httpv://youtu.be/5s86p8KMWTE

Interestingly, the acquisition of more jumping experience did not seem to matter. Lizards with more jumping experience on average did not do better than those without. It appeared that the motor coordination capacity of an individual might be the most relevant factor for locomotor recovery in tailless green anoles. Our finding suggested that the cost of tail loss might be very different among individuals in natural populations. It would be very interesting to perform a manipulative field study to see whether individuals that are unable to improve in-air stability alter their habitat use and movement patterns to a greater extent to avoid jumping.

CHI-YUN KUO, GARY B. GILLIS and DUNCAN J. IRSCHICK (2012). Take this broken tail and learn to jump: the ability to recover from reduced in-air stability in tailless green anole lizards [Anolis carolinensis (Squamata: Dactyloidae)] Biological Journal of the Linnean Society DOI: 10.1111/j.1095-8312.2012.01958.x

Here on the Anole Annals we like to talk food. Although anoles are predominantly insectivorous creatures, we have documented some of their stranger eating habits on this blog. For example, through recent research we have learned that they are more frugivorous than previously thought. They also include other vertebrates into their diets, such as frogs. Chamaeleolis anoles, we have learned, have specialized molars to aid in crunching mollusks.

Sadly, however, anoles are often also on the receiving side of predation. Anoles are important prey items for many different animals. Sometimes, even plants get their fill on anoles.

In her recently published undergraduate thesis, Dr. Yudisleidy López Ricardo from the University of La Habana, Cuba discusses the diet of the barn owl (Tyto alba furcata) in several localities in Villa Clara and Ciego de Ávila. Dr. López Ricardo examined nearly 300 owl pellets (regurgitated bits that contain food remains) and found 69 different prey types. As expected, small mammals such as the house mouse and black rat were common prey items. A novel finding of this study, however, is that large species of anoles, namely A. equestris, A. porcatus, and even Chamaeleolis sp. lizards were found in the owl pellets. Smaller anoles, including A. jubar, A. sagrei, and A. lucius were also found in the diets of the barn owl. The authors also found that a different herp, the Cuban tree frog, Osteopilus septentrionalis, was not uncommonly found in owl pellets, but this species is nocturnal.

The finding that anoles are a small, but important, component of this species’ diet is quite interesting in light of the fact that Tyto alba, like most owls, is nocturnal. The main question for me is how they are finding and catching anoles. Owls rely heavily on sensitive hearing to locate moving prey at even great distances. But anoles are predominantly diurnal creatures, and are typically asleep and quite still by nightfall. Owls also have great vision and may be spotting anoles during crepuscular hours. Or are they opportunistically feeding on anoles? Perhaps a different predator scares an anole out of its sleeping site and owls are snatching up fleeing anoles.

Any thoughts from the Anolis community on this interesting finding?

Squares are A. gaigei; circles are A. tropidogaster; triangles are locations of members of the species complex for which specimens were not examined and thus determination to species has not yet been accomplished.

Gunther Köhler’s at it again! This time with a merry band of colleagues he’s split Anolis tropidogaster, a little brownjob of an anole widespread in southern Central America and Colombia, into two species, A. tropidogaster in Colombia and eastern Panama and A. gaigei sandwiching it in western panama and the Santa Clara Mountains of Colombia.

Like a number of recently differentiated mainland anoles, the species differ markedly in the shape of their hemipenes. However, in contrast to some other cases, they also differ in dewlap color and a number of scale characters. Further, a limited genetic analysis suggests that the two forms may be substantially differentiated genetically.

The title of the paper says it all: “It is time for a new classification of anoles (Squamata: Dactyloidae).” No doubt, AA contributors will have something to say about this before long, but comments–or posts–are welcome now. The paper–by Nicholson, Crother, Guyer, and Savage–is a 108 page monograph in Zootaxa (text runs to page 69). Anolis is proposed to be split into the following genera: Dactyloa, Deiroptyx, Xiphosurus, Chamaelinorops, Audantia, Anolis, Ctenonotus, and Norops. In addition to presenting a phylogeny and a new classification, the paper also has sections on biogeography, dating, ancestor reconstruction and–most intriguingly–“Evolution of ecomodes in the family Dactyloidae.” Stay tuned!

High school students conducting anole research. Read all about it in the author’s post on the paper.

Everyone knows that anoles, like most reptiles, are not good parents. They just drop off the eggs, and that’s that. If they come across their offspring, they might even eat them! Not a paragon of parenthood. But does that mean the anole moms don’t do anything to help their kids? If nothing else, perhaps they could lay their eggs in places that would lead to maximally healthy offspring.

To test this idea, Aaron Reedy and a cast of dozens conducted an experiment in which they gave female brown anoles a choice of nest substrates varying in moisture content to see if they preferentially put eggs in some places over others. Then, they raised the eggs in the different environments to see if it matters.

The results were clearcut: females prefer to lay eggs in the soil with the highest moisture levels available. And, in turn, it matters: eggs put in such soils (the placement of eggs was randomized after the females laid them) had high hatching success, produced large offspring, and led to an overall increase in offspring survival.

These results are interesting and in agreement with a variety of studies on other reptiles. What is particularly notable about this research is that it was conducted in a low-income neighborhood city high school science classroom. The first author, Aaron Reedy, was a science teacher (he’s now in grad school at the University of Virginia), and the project was conducted by him and a large number of his high school students. Now, that’s remarkable! Reedy provides an interesting account of how the experiment came to be and what the students thought of it in a post at Scientific American’s website.

This paper also brought to our attention another paper published earlier this year that had eluded AA‘s notice.

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Figure from Leal and Powell paper showing that members of the same ecomorph category are not convergent in brain structure.

The Caribbean anole radiation is famous for its convergence. First detected in features related to habitat use and locomotion, such as limb length and toepad size, we now know that the Greater Antillean ecomorphs are convergent in many other attributes such as sexual dimorphism, territory structure and head shape. One might wonder what other features are convergent as well. For example, brains. The anole ecomorphs differ in the complexity of the environments in which they live, which might lead to selection for different brain configurations in different habitats. Brian Powell set out to examine anole brains for his just completed doctoral dissertation at Duke University, and he has now published the results. The short story: the anole ecomorphs are not convergent in brain structure! You can read more details in Chipojolab’s first-hand account of this paper, or check out the paper’s abstract here:

Read More

Dan Rabosky and co-authors have just published an important report on patterns of organismal diversity in PLOS Biology, with one of their main conclusions being that clade age does little to explain species richness.  Luke Harmon has a commentary on this article in the same issue of PLOS Biology, and I’ll refer readers there for a general summary of the work’s implications.  I wanted to give this article a shout-out here at Anole Annals because they used an anole as their icon for squamates in Fig. 3 (see above).

Inspection of their supplemental Table 2 and consultation with the authors, however, reveals that anoles were inadvertently left out of the final analyses due to a book-keeping error involving use of the timetree age for Iguanidae sensu Schulte et al. 2003 but the species richness for Iguanidae sensu Frost & Etheridge 1989. (A quick taxonomic review for the uninitiated: The family diagnosed as Iguanidae by Frost and Etheridge included only a subset of the species previously regarded as members of the much larger family Iguanidae.  Frost and Etheridge assigned Anolis and many of the other genera previously included in Iguanidae to other newly defined families.  They considered this taxonomic revision necessary because they did not recover a monophyletic Iguanidae sensu lato.  Because molecular phylogenetic analyses do tend to recover a monophyletic Iguanidae sensu lato, some subsequent authors, including Schulte et al. 2003, have advocated retention of Iguanidae sensu lato and treatment of Frost & Etheridge’s families as subfamilies [see Daza et al. 2012 for another perspective on this taxonomic debate].)

If we imagine crudely adding a circle to represent Anolis in Rabosky et al.’s figure 3 (assuming an age of ~50 mybp and species richness of ~400 for the genus), its clear that anoles would be among the youngest, yet also most species rich, of all squamate clades, providing further support for Rabosky et al.’s main conclusion that clade age has little role in explaining clade richness.

When alerted of this issue, Rabosky and his co-authors re-ran their analyses including anoles and their relatives (i.e., Polychridae/Polychrotidae of Frost and Etheridge) as well as all of the other Frost and Etheridge families that were overlooked for the same reason (e.g., Tropiduridae, Phyrnosomatidae).  Rabosky sent me a figure that illustrates the position of all these missing clades (in blue), including the clade that includes Anolis (in red) as well as the other squamate clades in the original analysis (in grey).  Because many of these clades stem from series of basal branching events within Iguanidae sensu lato and are relatively similar in age, they rather nicely illustrate the reported absence of a correlation between clade age and species richness.  Not surprisingly, Rabosky et al.’s overall conclusions about clade age and species richness are unchanged by inclusion of these additional datapoints.

At the end of the day, this discussion nicely illustrates how monkeying around with the names of formal Linnean ranks can cause chaos for anyone who is not intimately familiar with a particular name’s complete history.

Rabosky, D. L., G. J. Slater, and M. E. Alfaro (2012). Clade Age and Species Richness Are Decoupled Across the Eukaryotic Tree of Life PLOS Biology DOI: 10.1371/journal.pbio.1001381