Author: Jonathan Losos Page 89 of 130

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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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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We’ve had a lot of great discussion about Nicholson’s et al.’s proposal to split Anolis into eight genera. To date, most of the commenters have been against the proposal; I’d like to explain why I agree with this majority view.

Anole Annals summarized the arguments for splitting Anolis several days ago. Nicholson et al. argue that the failure to divide Anolis in the past has inhibited evolutionary and systematic research:

“Systematic progress in this regard has been delayed by an extremely conservative taxonomic approach to recognizing the diversity within the group and its extraordinarily ancient historical roots.” (p.4)

“The current practice (following Poe, 2004) of treating all dactyloids as comprising a single genus underemphasizes the evolutionary diversity within the family (as currently recognized) and obfuscates major biological differences among clades. In addition, simply because of the large size of the family (nearly 400 valid species), the single genus concept can be a hindrance to scientific communication regarding evolutionary events and directions of future research.” (p.13)

These quotes suggest that research on anoles is being held back by treating the entire clade as a single genus, but where is the evidence for these claims? No examples are provided. Quite the contrary, research on anoles has flourished over the last several decades, making it a well-known group for the study of many diverse evolutionary phenomena, and much of this work has explicitly incorporated phylogenetic information. Indeed, anole evolution, considered in a phylogenetic context, has become a commonly cited textbook example of adaptive radiation, and work on anoles has become so broad and deep that one commenter at last year’s Evolution meetings noted that “I didn’t go to the Evolution meetings for three years…When I “returned” in 2011 in Norman, it was like everybody had switched to working on anoles and sticklebacks!” The Dobzhansky Prize winners at the last two Evolution meetings have conducted phylogenetically-based research on anoles, and anole workers have nabbed the Fisher Prize and four Young Investigators Prizes at the meetings in that time span. Anole research is going gang-busters, and it is hard to see how retaining the name Anolis for the entire clade has had any sort of detrimental effect. (see also comments by Eric Schaad on why taxonomic names are no longer important for conducting phylogenetically-based evolutionary studies and by Yoel Stuart on why splitting evolutionarily-interesting clades may actually impede research).

I disagree with the proposal to split Anolis into eight genera for two reasons. First, it is not possible for the Linnean classification system to fully represent phylogenetic relationships—splitting genera simply changes the information conveyed, gaining some bits of information and losing others (for more discussion on this point, see the recent post by Luke Mahler and ensuing commentary). Second, splitting Anolis will be extremely disruptive for scientific researchers and the public.

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