Anole Annals

Anolis cybotes sitting on a rock. Image from Discover Life.

Martha Muñoz presented data on how shifts in behavior constrain evolution of thermophysiology and drive morphological differentiation in the Anolis cybotes complex. The A. cybotes complex occurs across a large altitudinal range on the Caribbean island of Hispaniola and Martha was interested in whether and how lizards are adapted to thermal differences at different elevations. Martha tested whether body temperatures differ between lizards found in the different thermal habitats. Sampling more than 400 individuals, Martha did not find differences in body temperature between the populations. This is surprising because ambient temperature differed by more than 10 degrees Celsius between the low and high elevation localities.

So, if temperatures differ so dramatically among the different altitudinal habitats, how do lizards maintain similar body temperatures? Habitat use data from the two populations show that the high elevation lizards use rocky substrates more often than low elevation lizards, which are mostly found on tree trunks and other types of vegetation. Data obtained by using copper models that measure temperature as a lizard would experience it in a given habitat show that rock habitats are too hot at lower altitudes, but ideal at higher ones. This suggests that lizards keep their body temperatures stable by shifting from arboreal habitat type to rocks in higher elevations.

Martha then asked whether similarity in body temperature was matched with similarity in underlying thermal physiology. In ectotherms such as lizards, the ability to perform a task is dependent on temperature such that is optimized over a narrow range and then drops at lower and higher temperatures until the animal is immobilized. She found that lizards from all populations have similar preferred temperatures, and so their underlying physiologies do not appear to be evolving.

While thermoregulation keeps thermal physiology stable, the shift in structural habitat affects morphology. Martha measured morphological characters such as head shape, limb proportions, and lamella number to test whether habitat use has driven morphological change. Martha found that lizards in high elevations have wider and flatter heads and shorter limbs than populations in lower habitats. Thus, she found that a thermoregulatory behavior impedes physiological evolution while simultaneously driving morphological evolution.

AA‘s man in Wisconsin, Greg Mayer, filed this report:

In Ernest E. Williams’ 1969 classic on the ecology of colonization, he identified Anolis cristatellus as one of the ‘minor colonizers’– not as widespread as carolinensis and sagrei, but having close relatives on Mona, Desecheo, and the Turks and Caicos. This natural colonization has now been augmented by human introductions– including Florida, Costa Rica, and the Dominican Republic, so that it is moving up on the colonization hit parade. In many of these places (e.g. Miami, Limon, Costa Rica), they have become established in highly human modified habitats.

Another sort of invasion has been taking place within Puerto Rico, as Kristin Winchell of U. Mass., Boston, has reminded us– cristatellus is also occupying (and thriving in) urban habitats in the densely populated parts of Puerto Rico. In her talk, coauthored by Graham Reynolds, Sofia Prado-Irwin, Alberto Puente-Rolon and Liam Revell, she shows that urban habitats present many challenges to anoles. The typical urban habitat is full of man-made surfaces (wood, masonry, glass, metal, oftrn painted), there is little or no canopy, the ground is made up largely of impermeable surfaces (so water runs of quickly), all of which lead to urban habitats being hotter, drier, and quite distinctive compared to the natural forest and woodland habitats. And let’s not forget the cats–all those awful, lizard-eating cats! (Apologies to Jerry Coyne!)

Kristin and company supposed, naturally, that all these environmental differences could lead to fairly intense selection for local adaptation. In particular, they supposed that city lizards should have longer legs (because running on larger, flatter surfaces is done better with longer legs), and that they would have more toe lamellae (to deal with the slippery, texture-less artificial surfaces, where claws are less effective for grip).

They tested these predictions at 3 paired sites near San Juan, Ponce, and Mayaguez (the natural site in San Juan was labeled by a sign at the site as “Una esmeralda verde en un mar de cemento”!) They confirmed their environmental characterization of cities, and found, as expected, that lizards perched on wider surfaces, did have more lamellae, and had longer legs–a resounding success. Interestingly, they did not find a change in perch height distribution between urban and natural. My one query would be about the change in lamellae number. High lamellae number is associated with narrower perch diameters– the numerous lamellae allowing the toepad to curl round to conform to the curved shape of the narrower perch (as shown in trunk crown anoles having more lamellae than similar-sized trunk ground anoles). I’ll have to think about what exactly I would expect in a trunk ground lizard adapting to man-made surfaces.

Kristin mentioned that they are planning a common garden experiment to test whther the differences have a genetic basis, as opposed to representing phenotypic plasticity. So we can look forward to more interesting results from this project.

Alex Gunderson asked the question: What ecological axes are involved in ecological divergence during adaptive radiation, and what phenotypic traits occur along them?

Here are the specific questions he investigated:

Alex pointed out that we usually talk about the ecomorphs that have diverged to use different parts of the structural habitat (e.g., twigs, canopy, grass, etc.), but less attenion is paid to divergence along the thermal niche axis, yet since Ruibal’s work in the early 1960’s, we’ve known such divergence occurs. Morphological divergence allows species to coexist by using different structural microhabitats; does divergence in thermal physiology have the same effect?

Most of the research involved the Puerto Rican cristatellus group, in which there are four pairs of sister species that differ in thermal environment, one more in the sun, one more a shade species. Some data also included Jamaican anoles. The study focused on two aspects of physiology related to thermal niche use, the critical thermal maximum temperature (CtMax) and the optimal temperature for sprint performance (Topt).

Results: In 3 of 4 sister taxa, the species in the warmer environment had a higher CtMax. In 2 of 4, the species had a higher optimal temperature (in both cases, in the other comparisons, the species did not differ statistically).

Q2: What are the performance consequences of physiological divergence?

Alex measured temperatures in shaded and open habitats and asked what the risk was of a species overheating in each habitat. In shaded habitats, no species were at risk of overheating, but in open habitats, for three pairs of sister taxa, the species from the cooler environment was at greater risk of lethal overheating.

Q3: Does physiological divergence promote species co-occurrence?

In cases where morphologically similar species co-occur (same ecomorph), do they diverge in physiology? The answer: Invariably yes in Puerto Rico and Jamaica. When morphologically similar species co-occur, they always differ in thermal physiology. Thus, thermal physiological differentiation seems to be important for increasing local species richness.

Q4: How quickly does physiology evolve relative to morphology?

Surprisingly (at least to me), physiology evolves considerably more slowly than morphlogy.

Summarizing across this work, Alex concluded that physiological differentiation may be an important component of adaptive radiation. In many cases, workers studying adaptive radiation focus on morphology for a number of reasons, not the least of which that it is much easier to measure. But, by doing so, they may be missing an important part of the puzzle.

Liam Revell gave a talk entitled “Placing cryptic, recently extinct, or hypothesized taxa in an ultrametric phylogeny using continuous charater data: a case study.” The title pretty much says it all and is a report on an ongoing project conducted with Luke Mahler, Graham Reynolds, and Graham Slater (sorry, I failed to think of anything clever about two authors named Graham. S’mores, anyone?).

The problem being addressed: we have a phylogeny for a group and want to add a taxon for which we only have continuous data, such as leg length, etc. How can we place it on the tree?

The details are too technical for me to summarize (note: if you want to get to the good, anole stuff and don’t care about the method, skip to the next paragraph), but entails using a likelihood formula that Felsenstein developed for building trees with continuous characters (another note: you must have continuous characters for all taxa). The method works by considering all possible placements of the missing species. It computes the likelihood of the model and tree conditioned on the dataset to find the maximum likelihood tree including the taxon of interest that is consistent with the tree based on nuclear data for the other taxa (note that the tree must be ultrametric). Liam reported that even for trees with 100 or more taxa, an approximately exhaustive search for the ML position of the tip taxon is possible. Because the tree is ultrametric, all we’re interested in is where the attachment on the tree occurs, because the branch length is then determined by the ultrametricity of the tree.

Liam assured the audience that the drawing was not of co-author Graham Slater

Now for the good stuff: the method was illustrated with regard to Anolis roosevelti, the feared-extinct crown giant anole of the Puerto Rican bank. Known from only eight specimens and last collected in the 1930’s, things don’t look good for roosevelti. It has been assumed to be closely related to the Puerto Rican crown-giant, A. cuvieri, which it does look like. Moreover, Steve Poe’s morphological phylogeny supports this placement.

The analysis can reject many potential placements of roosevelti, but many others are not ruled out statistically; i.e., the likelihood surface is flat particularly close to root of tree, not surprising given the extensive morphological convergence of anoles. However, for what it’s worth, placement of roosevelti as a close relative to cuvieri is ruled out.

It will be interesting to see how this project develops and whether these results hold. More importantly, someone needs to go out and find a living roosevelti.

Travis Ingram in the field

At each of the Evolution meetings over the last few years, anole researchers have been honored with some of the major awards  (1, 2, 3) recognizing talented young scientists. That trend continued here in 2014, when Travis Ingram was named as one of the winners of the  American Society of Naturalists’ Jasper Loftus-Hills Young Investigator Prizes.

Travis made a 30-minute presentation on his work on adaptive radiation. This work has combined the development of new analytical methods along with detailed analysis of two systems, our beloved anoles as well as Pacific rockfishes. In particular, Travis spoke about research investigating two questions: the extent to which adaptive divergence occurs specifically during speciation events, and the degree to which within adaptive radiations, convergent evolution occurs to the same adaptive peaks. In considering this work, Travis also discussed the difference between what are called “alpha” niches, which refers to ecological differentiation between co-occurring species, and “beta” niches, which refers to ecological differences across a landscape or environmental gradient.

Travis first discussed the method in to determine the extent to which morphological variation among species evolved during speciation. Travis has already published work on rockfishes that shows that substantial proportions of morphological variation among species appears to have evolved during the speciation process. He then discussed new work asking the same question in anoles, which shows that variation in traditional ecomorph traits—related to differences in structural habitat use—seem to be little correlated with speciational evolution. In contrast, climatic niche evolution—the divergence that arises within ecomorph clades—seems to be largely speciational.

Travis then switched gears to discuss research on convergent evolution within adaptive radiations, for which he and colleagues have developed a new method, Surface. Application of this work to Greater Antillean anoles—published in Science last year—shows that there have been 29 peak shifts in anoles, that there are 15 separate adaptive peaks, and that eight of these peaks have been occupied convergently. Moreover, Travis pointed out that even though the method does not start out with a priori categorization of species to ecomorph, the tradition ecomorph categories are for the most part recovered in the analysis, with some exceptions.

Travis then presented new work applying the same method to rockfish radiations on both sides of the Pacific in the northern hemisphere. Again, many convergent peaks were found; however, of the nine convergent peaks, eight were occupied by multiple lineages with a lineage, and only one occupied by lineages in both regions. This work was published this year in the American Naturalist.

Travis summarized by noting the interesting differences found in the two aspects of adaptive radiation he studies. His work indicates that axes related to environmental gradients, i.e., the beta niche illustrating differences across space, are related to speciational evolution, whereas traits related to alpha niche (microhabitat partitioning) are related to convergence within radiations.

Battling anoles. Image Credits: Ken King // Dixie Native

The St. Augustine Record published a very nice article two weeks ago discussing the invasion of brown anoles, A. sagrei, and how they’ve affected green anoles. But instead of the usual alarmist hysteria–green anoles being pushed to extinction–this article pretty much gets it right!

“…the invasion of the brown anoles have chased the natives into the treetops. The brown anoles, having few enemies, have taken over the former habitat of the greens, forcing them into new territories and farther from our sight.”

That’s right–the green anoles aren’t going extinct, they’re just shifting their habitat use to get away from the browns. The only quibble I would have is that this is not really “a new territory” because not only have green anoles in Florida been using high perches all along, but that’s what their ancestors in Cuba, who’ve always lived with brown anoles, have always done.  Green anoles experienced what’s called “ecological release” when they got to Florida and found it brown anole-less; now they’re simply returning to their ancestral niche.

For more on this topic, see previous AA posts [e.g., 1, 2, 3].