Anole Annals

In my three previous posts [1,2,3], I have discussed Nicholson et al.’s ecomode concept and their conclusion from it that the ecomorph concept should be rejected. Here I conclude my discussion by addressing two other related points raised in Nicholson et al., whether differences in forest structure are responsible for different evolutionary patterns in the islands and on the mainland, and their critique of my 1992 paper on the sequence of ecomorph evolution.

Are Differences in Forest Structure Responsible for Different Evolutionary Patterns in Mainland and Island Anoles?

Nicholson et al. state (pp. 54-55): “In discussing differences between island and mainland anoles, Losos (2009) considered, but dismissed, forest structure as a driving factor in shaping anole assemblages, suggesting that, to anoles, a tree is a tree…[W]e are impressed with the complex nature of the moist, wet, and rain forests of Central and South America (Solé et al. 2005) that are home to the majority of anole species. The heavily fluted bark of Neotropical rainforest canopy trees such as Lecythis must require substantially different limb and toe pad shapes in anoles that use these trees than those that use the smooth bark of canopy trees such as Pterocarpus. The facts that bark texture is likely to be much more diverse in mainland than island forests, and that trees with appropriate bark texture are likely to be so much more widely dispersed in mainland than island forests, must play an important role in making morphology of mainland anoles so much less predictable than it is for island anoles. The fact that island forests are dominated by a relatively few short, smooth-barked tree species must limit the number of morphs that anoles can attain, must increase the density that anole populations can maintain, and must increase the interactions among sympatric species above that experienced by mainland anoles. Additionally, the differences in the structure of understory shrubs associated with mainland areas possessing an ancestral fauna that includes grazing mammals, compared to island areas that lacked such grazers (Dirzo and Miranda, 1990), must affect habitat available for adaptive radiation in anoles. In short, we see little evidence that the assembly rules proposed for anole communities on Caribbean islands will ever be discovered as applicable to mainland anoles, because the factors shaping vegetation structure are so different between island and mainland forests.”

And by the end of the paper (p.68), the idea has been transformed into a firm conclusion: “We note that evolution of ecomodes appears to be widely constrained within anoles and does not necessarily lead to constrained morphology within an ecomode because variation in forest structure across the geographic range of anoles is so great.”

It is certainly plausible that differences in vegetation structure between mainland and island forests are responsible for different patterns of ecomorphological evolution in the two regions. But what is the evidence for this? I have actually looked for comparisons of structure between mainland and island forests and have not found any relevant literature. The authors only cite two papers and neither documents differences between mainland and island forests: Solé et al. (2005) is about differences between canopy and understory at Barro Colorado Island, and Dirzo et al. (1990) is a comparison of mainland sites with and without large mammal herbivores (note: these references were presented by Nicholson et al. to document appropriate points about mainland forests; I am not claiming they were inappropriate citations, only that application to Caribbean forests is entirely an extrapolation of the authors). The authors may well be correct that mainland and island forests differ, but they do not provide any evidence to support this claim. Moreover, even to the extent that mainland and island forests do differ in structure, the effect such differences have had on anole evolution is entirely conjectural (e.g., perhaps different bark texture would select for differences in toepad structure, but to date, there are no data relevant to such a claim).

Indeed, one may question how likely it is that differences in tree structure actually affect anole morphological adaptation.

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After presenting the concept of “ecomodes” (equivalent to habitat specialist types) as an alternative to “ecomorphs,” Nicholson et al. argue that the ecomorph concept should be abandoned. My previous two posts have discussed the ecomode idea and what it can tell us about the evolution of habitat use in anoles (1,2). In this post, I analyze their chain of reasoning that leads to the call to discard ecomorphs.

The argumentation in Nicholson et al. undergoes a curious transformation. At the outset they note, rightly enough, that a number of workers have found that the ecomorph concept developed for Greater Antillean anoles does not apply to mainland species, but by the end of the paper, they conclude that the ecomorph concept is fatally flawed and must be discarded in its entirety. How do they make this leap?

Let’s start by defining what we mean by “ecomorph.” In his classic 1972 paper, Ernest Williams defined an ecomorph as “species with the same structural habitat/niche, similar in morphology and behavior, but not necessarily close phyletically.” This definition has been quoted repeatedly and is the essence of how the term has been used throughout the literature on ecomorphs and their evolution. Thus, the trunk-crown ecomorph is composed of those species that are similar in morphology, habitat use, and behavior; moreover, to constitute an ecomorph, a set of species must come from multiple lineages, instead of composing a single clade. (It’s worth noting that the term “ecomorph” was coined by Williams in reference to anoles and has since been widely applied to other taxa, as discussed in a previous post).

Now, let’s trace the Nicholson et al. argument:

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One of the most significant potential impacts of Nicholson et al.’s proposed classification for anoles is that it would lead to changes in the binomials applied to most anole species.  For example, Anolis cristatellus would now be Ctenonotus cristatellus and Anolis chlorocyanus would now be Deiroptyx chlorocyanus.  The fact that Nicholson et al.’s classification would change so many binomials is the main reason we’re debating their proposed revisions; because binomials are the names that are most widely-used in the literature, changes to binomials are intrinsically more significant than many other types of taxonomic revisions.  The plusses and minuses of dividing anoles among multiple genera are discussed in numerous other recent posts on Anole Annals.  This post has a somewhat different goal – namely, to explain some of the proposed binomial changes proposed in Nicholson et al.’s classification that do not involve simply swapping one generic epithet for another.

In addition to simply dividing anole species previously recognized as Anolis among a number of new genera, Nicholson et al. introduce at least 48 new binomials that involve changes in the spelling of specific or generic epithets.  My purpose is to summarize and explain these changes to the best of my abilities.  As you will see, I soon reach the limits of my knowledge of both The Code and Latin and would like to ask readers more knowledgeable readers for enlightenment.

Understanding the majority of the name changes proposed by Nicholson et al. is relatively easy, as long as you take a moment to learn a bit about one of The Code’s article’s pertaining to Latin grammar.  Indeed, Nicholson et al. are compelled to change 35 species epithets due to a controversial provision of The Code that necessitates a match between the Latin genders of generic and specific epithets.  Most of the changes necessitated by this article of the code in Nicholson et al.’s proposed revision result from moving species from a masculine genus (Anolis) to a feminine genus (Audantia, Dactyloa, and Deiroptyx), and involve changing a trailing “us” to an “a” (e.g., Anolis chlorocyanus to Deiroptyx chlorocyana). A complete list of the species epithets that are being changed to match the Latin genders of their new generic epithets is included at the bottom of this post.

While most of the changes to specific epithets are due to the Latin gender issue, other changes have different explanations.  In some cases, the reasons for these other changes are well-justified.  Anolis etheridgei, for example, is changed to Deiroptyx darlingtoni because moving this species to Deiroptyx permits use of this species’ original specific epithet that was not previously permitted because it was the same as another species of Anolis (The Code does not permit two species named Anolis darlingtoni).

Nicholson et al.’s reasons for changing the fifteen remaining generic or specific epithets are less clear (at least to someone like me with no knowledge of Latin).  From the table below comparing the species epithets in Nicholson et al. to those in the Reptile Database, one generalization one might make is that most of the proposed changes involve vowels.  Some specific types of changes are applied more than once (e.g., a “u” is changed to an “i” in the names of both pumilus/pumilis and nubilus/nubilis) but other changes are unique (changing an “o” to an “io” in anfiloquioi/anfilioquioi).  I’ve checked the spellings in all of the original species descriptions that I have on hand and found that they tend to match the species names in the reptile database.  I believe the names in the original species descriptions are what The Code characterizes as the “correct original spelling.”  Based on my crude understanding of The Code, I have the impression that these “correct original spellings” cannot be changed to correct spelling or other grammatical errors that the author may have made either intentionally or unintentionally (only those changes that were not the authors fault, such as type-setting or printing errors can be corrected subsequently).  In one case the change might be  permissible because it involves an error in the original related to number of people being honored.  In one case, an “ii” is changed to an “i” seemingly against the letter of the code.  When I asked Nicholson about these changes, she told me that they were all made in accord with “the rules of Latin usage combined with ICZN rules for how you apply name changes.”

Can others out there assist me in interpreting the justification for these proposed name changes?

NOTE: I’m reluctant to even suggest the possibility that some new binomials are the result of typos, but this possibility must be considered in a few cases.  Nicholson et al. refer to A. macilentus (Garrido and Hedges 1992) throughout their manuscript, but refer t0 this species as A. maclientus in Appendix IV.   The fossil anole from Dominican amber is mentioned only a single time in the body of the paper, where it is referred to as domincanus rather than dominicanus (de Queiroz et al. 1998).  Similarly, a new genus name – Norpos – appears in Appendix III and again in Appendix IV when referring to the species parvicirculatus.  Tables of the changes to binomial names in Nicholson et al. are below the fold.

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Although we’ve been focusing a lot of attention on Nicholson et al.’s new classification for anoles, Daniel Scantlebury recently called attention to the fact that this monograph also contains “a bold hypothesis of the biogeographic history of” anoles.  I’m going to focus here on only one aspect of Nicholson et al.’s biogeographic analyses – namely, their use of two remarkable amber fossils to calibrate a Bayesian relaxed clock analysis supporting the hypothesis that anole diversification dates back to the Cretaceous.

Nicholson et al.’s hypothesis that anoles first appeared more than 90 million years ago and that most major clades of anoles originated prior to 70 mybp is likely to be one of the most controversial aspects their hypothesized biogeographic scenario.  These extremely old ages are significant because they make anole diversification compatible with a scenario that has long attracted the attention of vicariance biogeographers (Rosen 1975, Savage 1982, Crother and Guyer 1996).  Under this scenario, anoles occupied an ancient volcanic arc that originated in the Pacific ~120 mybp and formed a landbridge between North and South America in the Late Cretaceous (75-70 mybp) before moving on to form the present day West Indian islands.

I have characterized the ages for anole diversification in Nicholson et al.’s biogeographic reconstruction as “controversial” and “extremely old” because they are older than the age estimates obtained by most other studies.  Hedges et al. (1992) were among the first to use molecular methods to estimate ages for terrestrial vertebrate fauna of the West Indies, and reported ages for anoles and other taxa that were far too young to be compatible with Cretaceous vicariant events and the hypothesized Greater Antillean Landbridge between North and South America.  Hedges et al. (1992) suggested instead that anoles arrived in the West Indies via over-water dispersal.  Although Crother and Guyer (1996) criticized Hedges et al.’s use of immunological data and their resulting conclusions about over-water dispersal, more recent work has tended to support Hedges et al.’s conclusions by recovering ages for anoles and other terrestrial West Indian vertebrates that are too young to be compatible with the vicariant scenario hypothesized by Savage (1982), Crother and Guyer (1996) and Nicholson et al. (2012).

Daza et al.’s (2012) cladistic analysis of fossil data, for example, includes an update of the time calibrated tree generated by Conrad (2008) from available fossil material; this tree suggests that the Polychrotidae (the possibly non-monophyletic clade that includes anoles and other putative relatives like Polychrus) split from the Hoplocercidae sometime in the Eocene (~50 mybp).   Townsend et al.’s (2011) analysis of a multi-locus molecular phylogenetic dataset for iguanian lizards that used a BEAST analysis with 18 fossil calibrations suggests a split between Anolis carolinensis and the Corytophanidae at 50-70 mybp.  Most recently, Mulcahy et al.’s (In press) analysis of a multi-locus phylogenetic dataset for squamates in BEAST that relies on 14 fossil calibrations suggests that Anolis carolinensis split from Enyalioides laticeps 25-75 mybp (penalized likelihood analyses conducted by Mucahy et al. suggest a considerably older split between these two species that dates to around 80 mybp).

Recently published trees with estimates for the age of Anolis from Daza et al. 2012, Townsend et al. 2011, and Mulcahy et al. in press.

Why is there a discrepancy between the ages for anoles reported by Nicholson et al. and other studies?  

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Anole Annals dedicated all of last week to a detailed discussion of Nicholson et al.’s new monograph on anole classification, biogeography and ecomode evolution.  Because we had so many interesting posts, our discussion has spilled over into another week.  Some of the previously scheduled posts on biogeography and ecomode will be posted later today or tomorrow.  Check back later today for more discussion of Nicholson et al.’s hypothesized biogeographic scenario and stay tuned throughout the week as we wrap up our discussion of Nicholson et al.’s important monograph.  Remember also that Anole Annals welcomes posts and comments from anyone in the anole biology community about Nicholson et al.’s monograph, or any other topics to anole research.

Below the fold I provide an updated directory of the 18 previous Anole Annals posts pertaining to the Nicholson et al. monograph.

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Nicholson et al. conclude that the ancestral ecomode for anoles was a crown-giant anole, and that anole evolution was characterized by a general movement from up in the trees down toward the ground (e.g., from more arboreal to more terrestrial ecomodes). Unfortunately, even accepting ecomode assignments at face value, methodological flaws render this conclusion unreliable (my previous post discusses problems with the manner in which Nicholson et al. assign species to ecomode categories; for the purposes of this post, I accept the ecomode designations they provided). Two main problems plague the analysis. First, Nicholson et al. fail to estimate uncertainty in their ancestral state reconstructions, now a standard and expected method. Had they done so, they would have found that most nodes deep in the tree cannot be reconstructed confidently as a particular ecomode. Moreover, second, independent of this problem, had  ecomode state of outgroup taxa been correctly categorized, the ancestral ecomode of the anole radiation would not be unambiguously reconstructed as an arboreal species.

Problems with Ancestor Character State Estimation

The field of comparative biology has advanced greatly in the last 20 years, and it is no longer acceptable to simply reconstruct character states using parsimony. The reason is that such reconstructions provide no indication of how much confidence we may place in these reconstructions; indeed, as methods have been developed to estimate error bars around ancestral reconstructions, we have found that in many cases, the uncertainty is enormous, so great that we cannot state with any confidence that the most parsimonious reconstruction is better supported than other possible ancestral character states (see figure below for an example). The reason this occurs is that when we are dealing with traits that are very labile evolutionarily—i.e., that have evolved back-and-forth many times—there is little phylogenetic consistency in those traits, and thus the underlying assumption of ancestral reconstruction, that close relatives are likely to be similar in character state, does not hold.

An example of the uncertainty in ancestor reconstruction. The black dot represents the reconstruction of an ancestral ecomorph on Puerto Rico, inferred by parsimony. This species was inferred to be a generalist, lying between the ecomorphs in morphological space determined by principal component scores. However, when error bars are calculated for the esimtate, it can be seen that the ancestor could have been almost any of the ecomorphs. Figure from Lizards in an Evolutionary Tree, adapted from Schluter et al., (Evolution, 1997).

I discuss this issue at length in Chapter 5 of Lizards in an Evolutionary Tree, which I have excerpted here. Consider this: the most parsimonious reconstruction of ecomorph evolution in Greater Antillean anoles indicates that 19 transitions have occurred from one ecomorph to another. But, can we really strongly prefer a scenario implying 19 transitions from another scenario implying 20, especially if the 20-transition scenario yields very different reconstructions of ancestral states? Although those of a particular philosophical bent may disagree, I would argue that it’s hard to say with a confidence that reconstructions from a 19-transition scenario are much more reliable than reconstructions requiring 20 transitions.

The figure below estimates the likelihood of different ancestor character reconstructions of ecomorph of anoles—you’ll see that when all descendants of a node are the same ecomorph type, then we can have high confidence that the ancestor was that same ecomorph (the pie chart at a node is all one color); however, for most nodes, particularly further down the tree, this is not the case, and multiple ancestral character states are approximately equally likely.

Ancestor reconstruction of ecomorph state for Greater Antillean anoles from Lizards in an Evolutionary Tree. The likelihood that an ancestral node was a particular ecomorph type is represented by the proportion of the circle that is filled by that ecomorph’s color. None of the deeper nodes in the phylogeny can be confidently assigned to a single ecomorph category.

In others words, we can have little confidence in our reconstructions of the ecomorph/ecomode state of early ancestral species (Nicholson et al.’s ecomode designations are the same as previous ecomorph categorizations). Note in particular that not only is the base of the Caribbean anole radiation ambiguous, but that ambiguity results because there is some likelihood that the ancestral species could be trunk-ground, grass-bush or twig, but not trunk-crown or crown-giant. It thus seems extremely unlikely that the the ancestral ecomode node would have been reconstructed unambiguously as a crown-giant.

And, indeed, the Nicholson et al. analysis does not find unequivocal support that the ancestor of the Caribbean radiation was a crown-giant anole. Nicholson et al. state (p.54): “Our analysis indicates multiple equally parsimonious reconstructions of the ecomode of this northern ancestor. However, this uncertainty is derived from a transition from the crown giant ecomode for the ancestor of all anoles to a grass-bush common ancestor of Chamaelinorops, Audantia, Anolis, Ctenonotus, and Norops (hereafter derived anoles; Fig. 29). This transition represents a third major revision of the anole niche from one focused towards the canopy to one focused towards the ground and this transition makes the crown giant and grass-bush ecomodes equally parsimonious reconstructions of the northern ancestor as well as the ancestors of Deiroptyx and Xiphosurus. Because the majority of species of Deiroptyx (53%) and Xiphosurus (67%) included in our analysis have their habitat focused towards the canopy (crown giant, trunk crown, or trunk ecomorph), we suspect that the ancestors of both lineages, as well as the northern ancestor, were crown giants and not grass-bush anoles.”

But this argument is misguided.

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Anolis lividus. Trunk anole? Trunk-ground? Trunk-crown? Photo by Jonathan Losos

Mainland anoles exhibit a great diversity in habitat use and morphology, a topic we have discussed previously on AA. For this reason, an analysis of patterns of evolution in habitat use across all anoles, not just mainland species, would be very welcome. Nicholson et al. step into the breach by presenting habitat categorizations for a large number of mainland species, as well as for most West Indian species, and then analyzing habitat evolution on their preferred phylogeny. Along the way, they coin a new term, “ecomode,” argue that the ecomorph concept is fatally flawed and should be discarded, and present a scenario for patterns of ecological diversification in both mainland and island anoles. Although I applaud the effort to understand ecological evolution in mainland anoles and welcome the attention this paper brings to an important and little-studied question, I find the conclusions unconvincing. In this post, I discuss whether the data are sufficient to create categories of habitat use and confidently assign species to them; in subsequent points I will discuss the analysis of habitat use evolution and Nicholson et al.’s critique of the ecomorph concept.

What is an “ecomode”? The term is not explicitly defined in Nicholson et al., but it appears to refer to different categories of habitat use. The problem with creating such categories and assigning species to them is two-fold. First, most anole species use a variety of different habitats. I like to say that you can find almost any anole anywhere sometimes. More specifically, most anole species use the trunks of trees, often at different heights, and most can be found on the ground occasionally. How, then, do you distinguish a trunk anole from a trunk-ground or a trunk-crown anole, or a trunk-ground from a grass-bush? Second, how can one make sure that a given species fits into a single category? Perhaps some species have a broader niche that encompasses multiple ecomodes, or perhaps a species slices up the environment in an entirely different way (e.g., a trunk-bush or twig-ground species)?

Previous workers (including me) have been able to define ecomorphs and categorize species for two reasons. First, the ecomorph categories are defined not just on the basis of habitat use, but also by reference to morphology and behavior. Indeed, the morphological differences between ecomorphs are quite clear, and they correlate strongly with habitat use and behavior. One may quibble with a few assignments (e.g., is A. opalinus a trunk-crown or trunk anole?), as I discuss in Chapter 3 of Lizards in an Evolutionary Tree, but for the most part, assignment to ecomorph category is clear-cut (including the category of “non-ecomorph” for the minority of West Indian species that fail to meet the morphology/behavior/ecology criteria of any of the ecomorph categories).

The second reason we can make these assignments is because we have quantitative data that can be statistically analyzed. By contrast, the Nicholson et al. assignments are subjective decisions based on a reading of the literature, often relying on short summaries in broad regional reviews such as Savage’s (2002) The Amphibians and Reptiles of Costa Rica and Henderson and Powell’s (2009) Natural History of West Indian Reptiles and Amphibians. Use of these summaries is problematic for two reasons. First, although some mainland species have been studied extensively and quantitatively (e.g., the work of Vitt, Fitch, and Andrews), the habitat use of many species is not well studied. As a result, evaluating some summaries can be difficult because one does not know the extent and quality of the underlying data—in some cases (not Savage or Henderson and Powell), I suspect summary statements are not based on any hard data at all, but just qualitative impressions. In addition, even when species have been studied extensively, going from an encapsulated summary of such studies to an ecomode categorization is often not straightforward. For these reasons, the Nicholson et al.’s assignments of species to specific habitat use categories in many cases may not be reliable.

West Indian Non-Ecomorph Species

I will illustrate these problems by first discussing Nicholson et al.’s treatment of West Indian non-ecomorph species. For these species, there are a number of errors resulting from trying to interpret summary information provided in overview volumes.

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Recent posts on Anole Annals evaluated the taxonomic implications of Nicholson et al.’s [1] new systematics, yet their manuscript included similarly bold interpretations of anole biogeography and the chronology of their diversification.  Nicholson et al. claim that a single genus genus concept for anoles can stifle “scientific communication regarding evolutionary events” and used their new multi-genera taxonomy “to propose a bold hypothesis of the biogeographic history of the family within the constraints of the phylogeny inferred here, the latest known fossils, and a paleogeographic interpretation of the deep history of the West Indies, North America, Mesoamerica, and South America.”  My goal today is to address if their phylogenetic dating analysis is capable of delivering on such claims.

Anoles are characterized by a sparse and poorly understood fossil record.  Any attempt to elucidate the evolutionary history and biogeography of anoles depends on neontological data in the form of DNA sequences from extant species.  Nicholson et al. utilized molecular clock dating methods to hypothesize about the temporal history of anoles.  They calibrated their tree with two amber fossils containing lizards identifiable as anoles.  They attribute the first, Anolis dominicanus, to the clade containing A. aliniger, A. chlorocyanus, A. coelestinus, and A. singularis and assign an age of 23 million years before present (mypb) to this clade.  They use the second second fossil, A. electrum, to calibrate the split between A. limifrons and A. zeus to 28 mybp.  With this background in hand, let’s turn to evaluating their results.

For the sake of a critical evaluation, I have centered the remainder of the post around a three questions I would have asked had I been selected to review this paper during the peer review process.

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