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.
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.
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. Ancestor reconstruction with parsimony is based on the the phylogenetic arrangement of taxa with different character states; not the number of species exhibiting a character state. That is, whether a clade with a particular character state contains two species or 20 is irrelevant. The parsimony analysis clearly indicates that one cannot distinguish on the basis of parsimony between a grass-bush and crown-giant ancestor for the Caribbean anole clade—the reasoning employed by Nicholson et al. violates a basic tenet of parsimony analysis. The conclusion of this analysis is straightforward: if the ancestor of this clade cannot be assigned unambiguously, then the argument that the Caribbean radiation progressed from in the crown to more terrestrial cannot be supported. The Nicholson et al. analysis does not support that conclusion, and had uncertainty in character reconstructions been calculated, the lack of clarity would have been even more apparent.
Is the story for mainland anole ecomodes likely to be different? No. Check out the willy-nilly assortment of ecomode types across the phylogeny of mainland Norops. If anything, ecomode evolution seems more evolutionarily labile in this clade than in the West Indian species. My eyeball estimate is that minimally somewhere around 20 evolutionary transitions are required in this part of the tree. If the degree of uncertainty had been calculated for ancestral character states in this part of the tree, I have no doubt that the reconstructions for most of the deeper Norops nodes would have been as ambiguous as they are for the Caribbean ecomorphs.
What about for the Dactyloa clade? There things are slightly better, in that only eight character state transitions are required if one accepts that crown-giant is the ancestral ecomode state. Because these transitions are to five different states (including “polymorphic” as a character state, which probably isn’t appropriate procedurally because polymorphic is both a combination of multiple other states and a different combination of ecomodes in different species), the ancestral state of most nodes (other than for the phenacosaurs, which are the green and red species) may be fairly strongly supported as crown giant. Moreover, if one were to forget about body size and combine crown-giant (dashed blue lines) and trunk-crown (solid blue) into one “crown” ecomode (see next section), then this ecomode would probably be very strongly supported as the ancestral state throughout the clade.
Some might argue that phylogenetic inference of ancestral states is always about putting forth the best estimate as a hypothesis for further testing, and in this light, one might consider the most parsimonious reconstruction of ancestral states to be that best hypothesis. That may well be so, but what this sort of analysis indicates is that even the best hypothesis may not be very strongly supported, and thus not suitable for drawing strong conclusions about evolutionary patterns.
Problems with the Outgroup Character State
It is odd that Nicholson et al. distinguish between trunk-crown and crown-giant anoles given that ecomode categorization is explicitly based on habitat use and not on morphology (Nicholson et al.’s justification for this is a tad ironic given their taxonomic proposal to split Anolis: “We retain a category for canopy giant despite the obvious drawback that this category retains a feature of morphology by referring to body size. We do this because of the wide use of this category in past literature.” p.50).
This procedure seems mostly harmless in that it appears to have only been used to distinguish trunk-crown vs. crown-giant anoles in most cases; i.e., a species wasn’t classified as a crown-giant due to its body size if its habitat use wasn’t in the crown. With one big exception. The analysis includes two outgroups that form a polytomy with anoles, and one of them is Basiliscus, representing the Corytophanidae (see Dactyloa phylogeny figure above). Everyone knows that basilisks run across streams, not canopies, and yet it is coded as a crown-giant, presumably because of its size (from what is known, neither of the two other corytophanids–Corytophanes or Laemanctus–is a crown animal, either, at least from what is known of their natural history).
Would changing the ecomode character state of the Basiliscus clade to something more terrestrial—trunk-ground is perhaps the closest anole analogue—have made a difference? Absolutely. Given the huge heterogeneity in character states in the sister group to Dactyloa (incidentally, we need a name for this clade; perhaps Caribanolis recognizing that six of the seven major clades are exclusively Caribbean in geography?), crown-giant would no longer be the clear reconstruction for the ecomode of the ancestral anole. One possibility would still be that crown-giant was the ancestral character state, as exhibited by Polychrus and retained in anoles, with a more terrestrial state in both Basiliscus and Caribanolis being derived. But a plausible alternative would be that being terrestrial is the ancestral state, as exhibited by Basiliscus and, potentially, by Caribanolis, and that the crown-giant character state was independently derived in Polychrus and the ancestor of Dactyloa. More generally, re-casting corytophanids as some other ecomode would most likely have led to an ambiguous reconstruction for the ancestral node if uncertainty were calculated.
Bottom line: If appropriate outgroup characterizations and methods for estimating uncertainty in ancestor character states were used, the results of this analysis would be highly uncertain. of the major ancestral nodes in the phylogeny, probably only the ancestor of Dactyloa would be reconstructed with high certainty. Because ecomode has evolved back-and-forth so many times, phylogenetic approaches simply cannot provide a clear view of the history habitat use evolution. The conclusion that anole history documents a directional trend from a highly arboreal ancestor to more terrestrial descendants is premature.