Three weeks ago, I initiated discussion of Nicholson et al.’s recent monograph by noting that it is the most important paper on anoles published in recent years. We’ve had a lot of interesting discussion of many aspects of the paper since then, but we should keep in mind, even in the light of this discussion, that regardless of what one thinks about the various issues debated on our pages, this paper certainly represents a comprehensive compendium of knowledge about anole taxonomy, systematics, biogeography and ecology, and as such will remain an important resource for years to come.
Having said that, I wanted to use this last post of mine to synthesize what I see as the conclusions of the past three weeks’ discussion concerning the “bold hypothesis” of anole biogeography and evolution presented by Nicholson et al. Their hypothesis can be boiled down to three main points: Anolis is much older than previously recognized; divergence into eight major clades of anoles (which this paper raises to generic status) occurred when the geological blocks that now form the Caribbean islands separated from their previous, connected position where they had served as a landbridge connecting North and South America (and, hence, anole biogeography is primarily the result of vicariance, rather than dispersal); and the history of anole habitat use is primarily one of change from a large, crown-inhabiting species to smaller species found on or near the ground. How does this scenario stand up in light of discussion on AA?
Anolis Is Much Older Than Previously Recognized
Nicholson et al. conclude that the ancestor of anoles diverged from their nearest relative 95 million years ago (mya) and that diversification to produce the eight major clades occurred 72-87 mya. These dates are far older than other estimates; three recent studies have pegged the split between Anolis and its sister taxa as occurring 25-80 mya.
Nicholson et al. molecular phylogeny with their dates of divergence and with dates corrected assuming a younger date for the Mexican amber anole, A. electrum in parentheses. The arrow points to the phylogenetic position where A. electrum was placed by Nicholson et al.
This proposed antiquity of anoles is surprising, but is almost surely mistaken. The crux of the problem is the use of the Mexican amber anole, A. electrum, as one of only two points to calibrate the molecular dating. Nicholson et al. assigned A. electrum to be the sister taxon to the very young clade composed of A.limifrons and A. zeus (see figure ab0ve). Given the youthful position of this clade, one can easily see how an age of 28 million years would ramify throughout the tree, leading to the very old estimates for deeper nodes of the tree. Unfortunately, 28 million years is an overestimate, and more recent dating places the fossil at 15-20 million years. Given the key role this fossil must play in determining the age estimates (the other fossil is younger and in an older clade, and thus does not constrain age estimates), as a first approximation, reducing the age of this fossil to 71% of its stated value (20 vs 28 my) is likely to correspondingly reduce all of the age estimates of deeper nodes by a similar amount. This alone would reduce the age of Anolis to 68 mya and divergence of the eight subclades to 51-62 mya (of course, appropriate analyses will have to be conducted to verify these results, as well as to put error bars around the estimates). In itself, this change would render the divergence date of Anolis right in the middle of all of the previous estimates.
However, there is a bigger problem with the analysis. The description of Anolis electrum provides no synapomorphic characters that link A. electrum with the limifrons-zeus clade, nor even with any other clade within Anolis–in other words, all we can really say is that it’s an anole. Even in the description of the species, Lazell said that, based on phenetic grounds, the lizard could be either a Dactyloa or a Norops clade anole. At best, one might place the fossil within Norops on the grounds that Norops is the only anole clade present today in Mexico. However, even this conclusion is questionable: the biogeographic fossil history of Anolis, as detailed by Nicholson, puts anoles in non-tropical North America in the Paleocene, as well as sister taxa corytophanids and polychrotids, now entirely Neotropical, in Europe in earlier days. Clearly, anoles and their kin get around, and just because a clade is absent from Mexico today doesn’t mean that it wasn’t there 20 million years ago. In any case, even if we grant that electrum is a Norops, doing so would only have the effect of dating the divergence of Norops at minimally 20 or 28 million years, in turn putting the minimal age of origin of Anolis at only about 50 million old.
The bottom line here is that, correcting for the problems with dating and placement of A. electrum, Nicholson et al.’s analysis is unlikely to produce an older age for Anolis than that already in the literature.
Divergence of the Eight Major Anole Clades Occurred By Vicariance When The Greater Antillean Archipelago Landbridge Fragmented
In the Nicholson et al. scenario, the geological blocks that ultimately became the Greater Antilles formed a landbridge connecting North and South America from 75-70 mya.
The Nicholson et al. scenario is that the ancestors of today’s clades were already present and had started to diversify when the precursors to today’s Greater Antilles formed a landbridge connecting North and South America (see figure to left). When the proto-islands moved eastward and fragmented, the clades became isolated, going their own evolutionary ways, and leaving two clades still on the mainland, Dactyloa and the mainland Norops clade (whose sister taxon, Caribbean Norops, floated away on what eventually became Jamaica).
According to Nicholson et al., the Greater Antillean geological blocks began to separate from the mainland 70 mya. This figure shows the situation 60 mya. Caribbean anole clades diverged only after the islands had separated from the mainland, making a vicariance explanation impossible for the origin of Caribbean anoles.
Unfortunately, this scenario is not compatible with the revised dates for divergence of the eight subclades, as presented above. As discussed above, even if A. electrum has been placed in the correct place in the phylogeny, most anole subclades had not yet originated before the proto-Greater Antillean blocks began to fragment 70 mya. As a result, vicariance cannot explain the biogeographic distribution of anoles in the Greater Antilles–the islands had already floated away before Caribbean anoles diverged from mainland Dactyloa. Similarly, the divergence between mainland and island Norops also occurred after the islands had separated from the mainland, and so again, vicariance cannot be the explanation. Clearly, the explanation for the occurrence of anoles in the Greater Antilles, as well as the presence of Norops on the mainland, must be the result of dispersal events.
Nicholson et al. conclude their paper by stating: “We accept the argument that vicariance (and accretion) is the appropriate null hypothesis, and that dispersal is the ad hoc explanation invoked for exceptional cases (Nelson, 1974). We continue to be concerned that overexposure of data that document recent dispersal has diverted attention from extensive data that are consistent with vicariant (and accretion) events in anole evolution (Crother and Guyer, 1996).”
But Williams (1969) long ago noted the dispersal ability of anoles to colonize far distant islands. That these events were the result of dispersal is clear because many of these islands were underwater at the last sea-level maximum, about 120,000 years ago. Note how far some of these dispersal events are, from Cuba to mainland Central America and other far-distant islands. Given this proven ability of anoles to disperse, and the incompatibility of the geological and phylogenetic histories, dispersal is the obvious explanation for how anoles got out to the islands, and how Norops returned to the mainland.
Overwater colonization by A. carolinensis and A. sagrei. From Williams (1969). Arrows were placed in the center of Cuba only for artistic purposes.
The history of anole habitat use
Nicholson et al. proposed that being a crown-giant anole was the ancestral condition for anoles, and that the history of anole evolution has been one of decreasing body size and movement down toward the ground. I have previously discussed difficulties with this analysis, concluding that little could be said with confidence either about the ancestral habitat use of anoles, or of the ancestral condition for Caribbean anoles. Probably the only result that is likely to be strongly supported is that crown-giant anole is the ancestral condition for the Dactyloa clade.
One factor that may be relevant is that, at least among extant anoles—there are no crown giants that have a record of ever colonizing across water. All else equal, that would suggest the ancestral anole in the Caribbean probably wasn’t a crown giant. One of the best colonizers is A. carolinensis, a trunk-crown anole, so it is certainly possible that a crown-dwelling anole could have been the ancestral colonist, just not a big one.
Summary
Nicholson et al. provide a comprehensive and detailed analysis, bringing together a lot of information on disparate aspects of anole evolution, ecology and systematics, and thus will be valuable for years to come. Nonetheless, I find none of their bold claims on dating, vicariance vs. dispersal, or evolution of habitat use to be compelling.
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Ivan Prates
I personally agree with the need of a taxonomic restructuring for the anoles, but I was really concerned about the dating performed by Nicholson et al. and all the conclusions drawn from it. I’m glad to read Jonathan’s criticism and I would add the following: using a single marker from the mitochondrial genome for dating at this phylogenetic level will likely mislead divergence date estimation; mitochondrial genes are known to produce dramatic overestimation of split dates due to substitution saturation – up to 3 to 10-fold (Zheng et al 2011 Mol. Biol. Evol. 28(9):2521–2535). Testing for saturation is so often neglected!