Of Ecomodes And Ecomorphs: IV. Are Differences In Forest Structure Responsible For Different Patterns of Anole Evolution On Islands And Mainland, And Have Anole Radiations Occurred In The Same Sequence Across Islands?

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. I addressed this point in Lizards in an Evolutionary Tree: “Given that much of the ecomorphological work on anoles has focused on how differences in morphology have evolved to exploit different parts of a tree, vegetation structure would seem to be an important determinant of anole evolution. However, even within a Greater Antillean island, great variety exists in vegetation, from xeric scrub through dry forest to rainforest and cloud forest, yet the same basic ecomorph types occur widely throughout each island. Although certainly some differences in the structure of habitats occur between mainland and West Indian islands, it is not obvious that these differences matter to anoles. That is, anoles use the same variety of structures—e.g., tree trunks, twigs, leaves—in both areas. Even if the mainland in general had taller or broader trees or more lianas, how this would drive anole evolution in significantly different directions is not obvious. Nonetheless, these thoughts represent just my intuition, and detailed study of how vegetation structure affects anole behavior, ecology, and morphology (e.g., Johnson et al., 2006), both within and between regions, would be instructive.”

I conclude now as I did three years ago: the hypothesis that structural and vegetational differences between island and mainland forests drives differences between island and mainland anole faunas is worth investigating, but given the complete lack of relevant data, I think that Nicholson et al. overstate their case.

Critique of Losos’ 1992 Systematic Biology Paper

In 1992, I published a paper in which I reconstructed ancestral character states for the Jamaican and Puerto Rican radiations using parsimony methods much like Nicholson et al. do in their analysis (though I used quantitative morphological variables, rather than ecomorph categories). I concluded that the sequence of ecomorph evolution was very similar for the two islands.

Parsimony reconstruction of ecomorphology of ancestral anoles for Jamaica (left) and Puerto Rico, from Losos (1992). The reconstructions suggested that the assemblages evolved through a very similar sequence of ancestral stages.

On pp. 410-411 of that paper, I stated: “caveats to the reconstruction of ecomorph types must be stated. First, the Anolis of Puerto Rico are not actually monophyletic; they probably represent three separate lineages: the ancestors of occultus, cuvieri, and the other seven taxa (the cristatellus series). Although the phylogenetic affinities of the first two groups are uncertain, it is likely that they are the result of relatively early divergence events in anole radiation. Consequently, the temporal patterns inferred below are probably not greatly mistaken. Until their close relatives are identified, it will not be possible to determine to what extent their morphology reflects their ancestry and to what extent it reflects coevolutionary change subsequent to their arrival on Puerto Rico. For the purposes of this analysis, Puerto Rican anoles are treated as a monophyletic group, with the understanding that a reanalysis may be warranted when anole phylogeny is more fully understood.”

Here’s what Nicholson et al. had to say about the paper (p.50): “Unfortunately, only Jamaica appears to have been colonized by a single species that then diverged to the four sympatric ecomorphs that characterize the current Jamaican anole fauna. Analysis of the only other fauna included in Losos (1992b), the Puerto Rican anoles, suffered from pruning of the phylogeny to include only those taxa present on Puerto Rico. This process generated a misinformative pattern that appeared similar to the pattern for Jamaica only because contradictory evidence from the entire tree had been eliminated via the pruning process.”

Nicholson et al. provide no substantiation for their bold claims. In what way are the results “misinformative”? What is the “contradictory evidence from the entire tree”? It would be one thing to say that we should not have confidence in the results from an analysis that treated a non-monophyletic group as if it were monophyletic, but the authors’ statement implies that the conclusions are positively misleading, assertions that they fail to substantiate in any way.

Indeed, I think I may be forgiven for having taken the approach that I did with the Puerto Rican anoles two decades ago, when analytic methods for testing macroevolutionary hypotheses on a phylogeny were in their infancy and when molecular phylogenies for all Anolis did not exist (the reason that I limited the study to Jamaica and Puerto Rico was because some sort of molecular phylogenies had been published for the anoles on these two islands). But, 20 years later, neither the absence of analytic methods nor the incomplete sampling of the anole tree are issues. If Nicholson et al. (or anyone else) wish to dispute my conclusions, the best way to do so is by conducting the appropriate analyses, rather than merely through strongly-worded but unsubstantiated assertions. Without doing the proper reanalyses, all the authors should have done is re-state the caveats I presented 20 years ago.

Because Nicholson et al. failed to seriously engage with topic, I will provide a qualitative appraisal of how results might differ if information from the phylogeny we now have available for all Anolis were used to conduct a similar analysis. The short answer is that the results likely would be little changed.

Molecular phylogenies confirm that A. occultus is the only species on a long branch that comes out near the base of the anole tree, and its sister taxa, which occur on other islands, are not twig anoles (nor are twig anoles likely to be the ancestral ecomorph type), so it seems likely that this species evolved to become a twig anole on Puerto Rico. On the other hand, A. cuvieri is now known to be reasonably closely related (though not sister taxon) to the Hispaniolan crown-giants, as Williams surmised 30+ years ago. As a result, it is possible that cuvieri possessed its crown-giant morphology before becoming a member of the Puerto Rican fauna. The cristatellus series is still the youngest of the three clades on Puerto Rico and three ecomorph types have emerged from within this clade (trunk-crown, trunk-ground, and grass-bush). Consequently, my guess is that a parsimony analysis done today would show that the sequence of ecomorph evolution in Puerto Rico was pretty similar to what I concluded in 1992, with the major difference being whether at the two species stage, it was a twig anole and a generalist, as I concluded then; a twig anole and a crown-giant; or something else.

It turns out, however, that Nicholson et al.’s critique is irrelevant because it is directed toward a hypothesis long-discarded. In 1998 in Losos et al., a number of colleagues and I showed that the pattern of ecomorph relationships on the other two islands did not mirror what was seen on Jamaica and Puerto Rico and, moreover, that our understanding of phylogenetic relationships on Jamaica had changed, altering the ancestor reconstruction on that island as well. As a result, the idea that ecomorphs evolve in the same sequence across all islands is long dead. Furthermore, as I argued in a previous post, ancestor reconstructions based on parsimony are often very ambiguous, as is the case for the evolution of the ecomorphs, so this entire approach is not very reliable.

For these reasons, there is no longer support for the hypothesis that ecomorphs evolved in the same sequence on different islands and, in fact, even if they had, our methods probably would not be able to detect it. Nonetheless, contrary to Nicholson et al., this conclusion has no bearing on whether the Greater Antillean  ecomorph concept is valid. Phylogenetic analysis, combined with data on morphology, ecology, and behavior, clearly indicate that similar sets of ecomorphs have evolved independently on the four islands of the Greater Antilles.

Jonathan Losos

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7 Comments

  1. On the diversity of bark in mainland versus Caribbean forests:

    I thought I might provide the perspective of a field botanist on the mechanism proposed relating bark and Anolis diversity. As someone that has spent considerable time staring at anoles during lunch breaks in between measuring thousands of trees in Puerto Rico, this conversation interests. One of the many striking features of tropical tree assemblages is the general low degree of bark (specifically outer bark) diversity. Indeed the vast majority of species and individuals have smooth and unremarkable outer bark. This is true for the mainland and the islands. This lack of diversity often unnerves temperate tree researchers introducing themselves to the tropics because they are accustomed to using outer bark during species identification in the field. The inner bark, on the other hand, can be quite diverse and is frequently used to identify species, but of course this is not something anoles care about as far as I know.

    Though there are some interesting species that do have furrowed and/or flaky outer bark and so I thought I might discuss this topic. Nicholson et al. rightly state a lack of the furrowed species of Lecythis (family Lecythidaceae) in the West Indies. In general, the Lecythidaceae are not common in the West Indies aside from a handful of exotics and one native species and they are also less diverse in Meso-America when compared to the large number of species in South America. Despite the general rarity of this family in the West Indies it is not difficult to name a number of important/common species and genera that are shared between the mainland and the West Indies that have deeply furrowed or complex outer bark. Here is a quick/condensed list: Alibertia edulis; Andira inermis; Calycophyllum candidissimum; Cedrela odorata; Ceiba pentandra; Lysiloma; Exostema; Trichilia glabra. Many of these species are primarily found in dry forests. This is not surprising given that outer bark morphology, from my perspective, is much more diverse in dry forests than wet forests (which raises the question of whether Anolis should be more diverse in dry forests given the mechanism proposed). Of course these are just a few examples, the West Indies flora contains over 13,000 species of plants and there have been no formal comprehensive studies of outer bark diversity that I am aware of in tropical forests aside from recent work by Tim Paine and colleagues on bark thickness in French Guiana. I should also point out that while Pterocarpus does have smooth bark, it also has large thin buttresses at maturity that can be fairly close together making the tree appear as if it is folding longitudinally or fluted. This can be readily seen in the large individuals of Pterocarpus officinalis located at the Anolis hotspot of El Verde Field Station in Puerto Rico.

    In sum, from a fair bit of field work on the mainland and in the Caribbean I do not perceive any fundamental difference in the diversity of outer bark morphology or frequency of complex morphologies between the two locations and I do not see a reason why it should be assumed from the start. I also feel that given the general lack of outer bark morphological complexity on the mainland and the islands it seems to me that the encounter rate of an Anolis with a complex bark morphology would be sufficiently small for it to not have a large impact on anole diversification/diversity. If anything I might expect selection for a suite of traits across species useful for gripping and maneuvering on smooth outer bark.

    Those are my two cents.

  2. cybokat

    Actually, when Kris Crandell accompanied me on a field trip in the Dominican Republic, she tested the clinging force of a single species of Anolis to different structures (pine bark, rock, glass) and as far as I can remember did not find a difference between bark and rock, so perch texture did not seem to be the reason for different perch choice.
    Jonathan, I think we should convince her to write these results up for Breviora, given the paucity of overall data.

    • cybokat

      to the botanist: The bark was from Pinus caribeensis and occidentalis

  3. I’ve also had a really hard time following some of the logic in the Nicholson et al. report. I have the impression that they may have simply misunderstood what an ecomorph is and how anole biologists have previously investigated ecomorph evolution. How else could they end up dismissing prior work on ecomorph evolution and formulating their ecomode idea based partly on an unsubstantiated and irrelevant critique of a 20 year old paper that nobody views as central to our current understanding of ecomorph evolution? One of the first things I learned about anole evolution when I was a graduate student in the late 1990s and early 2000s was that the conclusions about shared patterns of ecomorph evolution reported by Losos 1992 were no longer supported by the data.

  4. Peter Tolson

    After spending a lot of time time working in subtropical dry forest here in the Cuzco Hills of Cuba, I agree that there is a lot of tree bark diversity in dry forest. Here in the GTMO forest we have several quite common species of trees with very shaggy bark such as Lysiloma latisiliqua, Guazuma ulmifolia, Psuedosaminea cubana, Brya ebenus, etc. etc., along with smooth-barked species such as Ficus and Acacia, yet our forest anole species diversity is pretty low: homolechis, porcatus, sagrei, argillaceous.

  5. Don Lyman

    A tangential tree thought: I’ve often wondered why anoles that are mangrove specialists haven’t evolved. Mangroves seem like a very distinct ecosystem that might lend themselves, at least from a human perspective, to the evolution of anoles that just inhabit magrove swamps.

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