Category: New Research Page 11 of 66

Kiyomi Johnson (L) and Marina Carbi (R) presenting their poster, “Speciation and Phylogeography of Anolis opalinus on Jamaica,” at JMIH 2018.

Caribbean anoles have been studied extensively, with researchers examining their evolution, ecology, physiology, morphology, and behavior in many different contexts. In some respects, they are one of the best known groups of organisms in the world. But are there still unique species “hidden” within the diversity of anoles we already know? Some papers suggest just that. In 2002, Jackman et al. examined the mitochondrial DNA of Jamaican anoles and found evidence that several species contained deeply diverged clades, indicating the potential presence of cryptic species.

Enter Marina Carbi and Kiyomi Johnson, two public high school students with a drive to dig into the biological sciences and a budding curiosity about all things Anolis. Ms. Carbi, a recent high school graduate, and Ms. Johnson, a rising senior at Fiorello H. LaGuardia public high school, began an internship specifically for high school students at the American Museum of Natural History. Working with Dr. Ed Myers, they set out to investigate the phylogenetic diversity in A. opalinus, the Bluefields anole, by sequencing a combination of mitochondrial and nuclear DNA from a series of 22 specimens of Jamaican anoles.

Mss. Carbi and Johnson found that both the mitochondrial data and combined species tree support the existence of a cryptic species within what is currently considered A. opalinus. Populations of the Bluefields anole found in the Blue Mountains area are monophyletic and sister to A. valencienni, indicating a potentially deep divergence from A. opalinus. Todd Jackman, whose initial work inspired this research, dropped by to check out Kiyomi and Marina’s follow up to his paper and was impressed. “Hopefully, they can go to Jamaica themselves,” Todd remarked, before adding as an aside, “I’m glad that their results match ours.”

The authors presented strong evidence that A. opalinus contains a cryptic species. Pic via Twitter.

Looking forward, Ms. Carbi has plans to attend Cornell University in the future, while Ms. Johnson is completing her high school degree. Both expressed interest in continuing to work in biology, with Ms. Carbi noting that she was excited to have had the opportunity to interact with researchers from Cornell at JMIH. The Society for the Study of Amphibians and Reptiles provided support for Mss. Johnson and Carbi to attend the meeting. More extensive sequencing is ongoing in order to further elucidate the phylogeography of what is currently known as Anolis opalinus. Stay tuned!

Three in The Bed: a Curious Case of a Shared Sleeping Perch in a Neotropical Anole

By Tom Brown

On July 8, 2018

In Anole Photographs, Natural History Observations, New Research, Notes from the Field

Opposite views of a communal sleeping event (1 male, 2 females) of Anolis cusuco at Parque Nacional Cusuco, Departamento Cortes, Honduras (Brown & Arrivillaga, 2018)

Let’s be honest: anoles are fascinating! These charismatic and well-adapted lizards are always a pleasure to watch and document. Better yet, no matter how well you think you know a species, they’re still always full of surprises.

The sleeping behavior of anoline lizards is a fascinating aspect of their natural history, and a growing amount of literature has detailed species-specific sleeping activities. Typically, anoles are considered solitary sleepers owing to their territorial nature, but ‘behind closed doors,’ this may not always be the case!

For those curious, a recent ‘behavioral oddity’ published in Mesoamerican Herpetology by Brown & Arrivillaga (2018), reported an example of three individual Anolis (Norops) cusuco sleeping together on a perch! The individuals were so close that portions of their bodies overlapped! Strange, indeed; this observation contrasts the typical view of anole sleeping ecology, territoriality and indeed that what is known for this species (Clause & Brown, 2017). In over 5 years of visiting Cusuco NP (observing countless solitary sleeping A. cusuco), imagine the surprise in finding these anoles having a sneaky snuggle!!

As we wrote: “Although a conclusive explanation is not available, we suggest that because the sleeping group consisted of one male and two females, that the shared perch might have been breeding-related. This situation might be associated with the overlap of male and female territories, or by the anoles awakening close to necessary resources. Conceivably, however, courtship might have been interrupted by nightfall, and the orientation of the sleeping male ensured that courting would continue the following morning.”

Anole Outpost: The Cay Sal Bank, Part III

By Graham Reynolds

On June 28, 2018

In New Research, Notes from the Field

This is the final of a three-part post on our work on the anoles of Cay Sal Bank, Bahamas. In this post, I will visit the Brown Anoles (Anolis sagrei). Like many, many places in the Caribbean, Anolis sagrei occurs across the Cay Sal Bank. This species has the widest range of any Caribbean anole, having colonized a huge range of regions from ancestral origins in Cuba- from the northern Bahamas, throughout the northern Caribbean, all the way to the Atlantic versant of Mesoamerica.

(Mostly) native range of Anolis sagrei.

Our ongoing work on this species has resolved the evolutionary history of A. sagrei across this great range, but one hole that had lingered was the status of the populations on the Cay Sal Bank. Prior to our cruise to the region in 2015, A. sagrei was known from the following islands: Cay Sal Island, the Anguilla Cays (including Cotton Cay), and Elbow Cay (Buckner et al. 2012). Further, these populations were considered to be the subspecies A. sagrei ordinatus, or, the Bahamian Brown Anole (Buden and Schwartz 1968; Buckner et al. 2012). This subspecies was originally described owing to having supraorbital scales in contact and a different dewlap color. We know now that dewlaps are highly variable both among and within populations of brown anoles on the Bahamas banks (e.g., Vanhooydonck et l. 2008). Populations proximal to the Cay Sal Bank- that is- populations on the Bimini islands, have a very distinct dewlap comprised of a light orange background streaked with dark red. Brown anoles on Cay Sal do not share this dewlap color; instead, they have a more classic sagrei pattern of darker red with a light distal border. This is not a smoking gun for considering Cay Sal anoles something other than A. s. ordinatus, of course, given the range of dewlaps we see to the east.

Cay Sal (left), South Bimini (right). Photos by R. Graham Reynolds.

If Cay Sal browns were indeed A. s. ordinatus, that would imply a (likely) westward colonization across the Santaren Channel–not an implausible scenario. During periods of lower sea level, the Cay Sal Bank would have been a big ‘ol target for lizards involuntarily leaving the Great Bahamas Bank. Of course, an alternative would be the reverse: an initial colonization of Cay Sal, followed by dispersal to the east across the Channel. Of relevance, during the course of the work I’m presently describing, we also found a snake: Tropidophis. We determined, using the same molecular phylogenetic techniques, that this snake is most likely T. curtus, and thus a population conspecific with Tropidophis over on the Great Bahamas Bank, evidence for a likely westward colonization.

Map of the Cay Sal Bank, from Reynolds et al. (2018). Note that Cotton Cay is part of the Anguilla Cays.

Of course, Cay Sal browns could also be Cuban in the sense that they might have colonized the bank directly from Cuba across the Nicholas Channel. To parse these alternative origin stories, we collected samples of the species from across the Cay Sal Bank and generated a coalescent gene tree paired with all our sampling from other brown anole populations across the region. We find that Cay Sal A. sagrei are actually much more closely related to western Cuba A. sagrei, rather than Bahamas A. s. ordinatus. Combining this finding with our analysis of A. fairchildi, we find that this particular Anole Outpost was colonized from Western Cuba by at least two species–and likely at different times.

Phylogeny of A. sagrei, showing Cay Sal Bank lineagers in blue (and a Cay Sal specimen in the inset). From Reynolds et al. 2018.

New Records

In addition to these findings, we also documented some novel populations of A. sagrei on the Cay Sal Bank. We added East Doubled Headed Shot Cay, Elephant Rocks, Great Dog Rock to the list of known populations on the bank. What is particularly interesting about these new records is the range of habitat types that they support. Cay Sal Island and the Anguilla Cays are by far the most lush, with lots of vegetation. To the north, the cays become increasingly xeric and barren. East Double Headed Shot Cay is the most vegetated of the northern islands, and has a thick, but low, covering of coastal shrub plant community. Anolis sagrei is not abundant on this island, and we only saw a few dozen during several hours of searching.

East Doubled Headed Shot Cay. Photo by R. Graham Reynolds.

In stark contrast, the Elephant Rocks to the west are tall, jagged, steep, and rocky islets with almost no vegetation at all. We had low expectations as we jumped into the sea from the dingy to start our ascent of these islands at dawn. But, to our surprise, we found some anoles happily living among the rocks. Not at high densities, but here they were, a saxicolous population of A. sagrei.

Elephant Rocks, Cay Sal Bank. Photo by R. Graham Reynolds.

Naturally, Alberto and I would love to follow up on some of this, but Cay Sal is a tough place to work. Maybe someday we’ll get back there, in the meantime, we can reflect on what a special opportunity we had to visit this Anole Outpost.

Sunrise on the Cay Sal Bank. Photo by R. Graham Reynolds.

References

Buckner, S. D., R. Franz, and R. G. Reynolds. 2011. Bahama Islands and Turks & Caicos Islands. In R. Powell and R. W. Henderson, editors. Island Lists of West Indian Amphibians and Reptiles. Bulletin of the Florida Museum of Natural History 51: 85–166.

Buden, D. W., and A. Schwartz. 1968. Reptiles and birds of the Cay Sal Bank, Bahama Islands. Quarterly Journal of the Florida Academy of Sciences 31: 290–320.

Vanhooydonck, B., A. Herrel, J. J. Meyers, and D. J. Irschick. 2009. What determines dewlap diversity in Anolis lizards? An among-island comparison. Journal of Evolutionary Biology 22: 293–305.

What’s New in Anole Literature?

By Jessica Pita Aquino

On June 26, 2018

In New Research

Anolis biporcatus. Photo by Jessica Pita Aquino.

Anole biologists and enthusiasts, stay updated on the latest anole research and find out about these fascinating creatures as scientists continue to make amazing discoveries! Here’s what’s been published in the last year and a half (2017-2018): nearly 150 papers in just a year and a half!

Anole Annals welcomes posts on new anole literature. Our goal is to try to keep the anole community up-to-date with regard to new publications, but we need help! So, if you’d like to try your hand at some science communication (or need something to list as a Broader Impact), please consider writing a post summarizing or discussing a recent paper.

And authors: there’s nothing more interesting than to get the insider’s view of a recent paper. Tell us the backstory: how a paper came to be and why you conducted the study in the first place. Provide the fascinating details that you can’t find in a published paper. It’s a great way to disseminate your work, and looks good on grant proposals.

We invite anyone interested to write posts! If you’d like to be a contributor, please write anoleannals@gmail.com.

2017

Alibardi, L. 2017. Review: Biological and Molecular Differences between Tail Regeneration and Limb Scarring in Lizard: An Inspiring Model Addressing Limb Regeneration in Amniotes. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 328:493–514.

Armstead, J. V., F. Ayala-Varela, O. Torres-Carvajal, M. J. Ryan, and S. Poe. 2017. Systematics and Ecology of Anolis biporcatus (Squamata: Iguanidae). Salamandra 53:285–293.

Birke, L. L., A. M. Cespedes, E. R. Schachner, and S. P. Lailvaux. 2017. Cystic Calculus in a Laboratory-housed Green Anole (Anolis carolinensis). Comparative Medicine 67:112–115.

Bochaton, C., S. Bailon, A. Herrel, S. Grouard, I. Ineich, A. Tresset, and R. Cornette. 2017. Human Impacts Reduce Morphological Diversity in an Insular Species of Lizard. Proceedings of the Royal Society B: Biological Sciences 284.

Bonneaud, C., I. Sepil, L. Wilfert, and R. Calsbeek. 2017. Plasmodium Infections in Natural Populations of Anolis sagrei Reflect Tolerance Rather Than Susceptibility. Integrative and Comparative Biology 57:352–361.

Boyer, J. F. F., and L. Swierk. 2017. Rapid Body Color Brightening is Associated with Exposure to a Stressor in an Anolis Lizard. Canadian Journal of Zoology 95:213–219.

Anole Outpost: The Cay Sal Bank, Part I

By Graham Reynolds

On June 20, 2018

In All Posts, New Research, Notes from the Field

What determines species composition on remote Caribbean islands? Geographic proximity to source populations? The vicissitudes of dispersal and colonization? Propagule pressure and prevailing biotic and abiotic environmental conditions? The study of biogeography addresses such questions, and is concerned with understanding the geography of biodiversity- where do species occur and why?

We perhaps often think of species groups accumulating from colonists arriving from the same place, that is, we identify a likely natal source for island colonists. But might species groups be chimeric, in that they contain groups of diasporic species from different natal lands? This is certainly a plausible scenario and could potentially lead to some interesting evolutionary outcomes.

The Cay Sal Bank is a remote island bank, or shallow carbonate platform, on which rests a line of small islands strung out along its margins. This region, as well as our recent expedition, has been mentioned in a previous AA post. Here I am returning to discuss the anoles and the results from our recently published work describing the evolutionary relationships of the terrestrial squamate fauna. Fundamentally, we ask a question that has circulated for the better part of a century: where do the anoles on Cay Sal come from?

Six terrestrial squamates are found on this bank:
Anolis fairchildi (endemic)
Anolis sagrei
Tropidophis curtus
Sphaerodactylus nigropunctatus
Cubophis cantherigerus
Typhlops biminiensis

Dispersal hypotheses for terrestrial squamates found on Cay Sal Bank, from Reynolds et al. 2018

Of these, all but Anolis fairchildi and the recently discovered population of Cubophis were thought to have Bahamian evolutionary affinities. The endemic A. fairchildi has been of particular interest, owing to its status as the product of one of the ex situ speciation events occurring in the green anoles as they dispersed from Cuba (Williams 1969). But a previous AA post (1) reminded us that the origins of Anolis fairchildi had not been resolved- did they come directly from Cuba or are they derived from Bahamian A. smaragdinus (among other alternatives?). Here we tackle this question, using a basic mitochondrial dataset and lots of taxon sampling from previous study of the group (more on A. fairchildi in a future post). We constructed a coalescent gene tree of all “carolinensis-clade” Cuban green anole species, including our samples obtained from Cay Sal Island in 2015. We find unequivocally that A. fairchildi is a recent colonist from western Cuba- nested within the western Anolis porcatus lineage. Thus we see both ancient and recent emigration (divergence) events leading to what we recognize as species in the carolinensis clade of green anoles, setting up a really nice opportunity to examine the accumulation of variation in diasporic populations over different time periods.

Phylogeny of “carolinensis clade” green anoles from Reynolds et al. 2018, with A. fairchildi highlighted in green and shown in the inset photo

Drivers and Constraints of Within-Species Diversity in Dewlap Design

By Simon Baeckens

On June 6, 2018

In New Research

Sampling locations of the populations of study across the Caribbean. (1) Soroa (Cuba), population 1; (2) Soroa (Cuba) population 2; (3) Grand Cayman; (4) Santa Clara (Cuba); (5) South Bimini; (6) Chub Cay; (7) Andros; (8) Crooked Island; (9) Acklins; (10) San Salvador; (11) Staniel Cay; (12) Pidgeon Cay; (13) Grand Bahama; (14) South Abaco; (15) Cayman Brac; (16) Little Cayman; (17) Jamaica.

The dewlap is arguably one of most fascinating features of anoles. For me, it is the baffling diversity in dewlap size, coloration, and use —both among and within species— that makes it so interesting. However, understanding the origin and evolution of dewlap diversity in Anolis has proven a daunting task (Nicholson et al. 2007; Vanhooydonck et al. 2009). In an attempt to make (a little more) sense of the drivers and constraints of anole dewlap variation, a team of Belgian researchers from the University of Antwerp, led by evolutionary ecologist Tess Driessens, decided to look at dewlap diversity in Anolis sagrei. They surveyed 17 island populations of A. sagrei across the Caribbean and quantified dewlap design (color, size) and dewlap display behavior of both males and females.

Last year, Driessens and colleagues published their findings on how variation in abiotic factors (such as precipitation, temperature and other climatic variables) could explain much of the observed inter-island variation in dewlap design and use in A. sagrei (‘signal efficacy’ hypothesis). In a paper that came out last week, the team reports on the role of the biotic environment in driving dewlap diversity in the brown anole. Inspired by the wonderful study of Vanhooydonck et al. (2009), the researchers tested whether among-population dewlap variation could be (at least partially) assigned to variation in predation pressure (estimated by island size, tail break frequency, presence/absence of the predatory curly-tailed lizards, clay model attack rate), sexual selection (using sexual size dimorphism), and/or species recognition (number of syntopic Anolis species). Overall, they found only limited support for the idea that the extensive interpopulational variability in dewlap design and use in A. sagrei is mediated by variation in their biotic environment. Although they did find that males from larger islands show higher dewlap display intensities than males from smaller islands, and that males are more likely to have a ‘spotted’ dewlap pattern when co-occurring with a high number of syntopic Anolis species, the direct connection with predation pressure and species recognition remains ambiguous and demands further investigation.

In another recent paper, focusing only on the size of the male dewlap and their maximum bite capacity, the Belgian researchers asked a different question: does dewlap size signal fighting capacity (estimated by bite force) in A. sagrei, and is this true for all 17 sampled populations? And, does the level of signal honesty (that is, the steepness of the dewlap size-bite force relationship within a population) vary among populations, and is it linked with the strength of intrasexual selection? Their results showed that absolute dewlap size is an excellent predictor of bite force in all A. sagrei populations. However, relative dewlap size was only an honest signal of bite performance in 4 out of the 17 populations. Surprisingly, the level of signal honesty did not correlate with the strength of intrasexual selection.

Male brown anole biting on a purpose-built force plate. Photo by Tess Driessens

While the work of Tess Driessens and her team sheds new light on the drivers and constraints of dewlap diversity in A. sagrei, there is still plenty of study material left for future dewlap fanatics.

Can Evolution in Brown Anoles Keep Pace with Climate Change?

By Michael Logan

On June 2, 2018

In New Research

A male brown anole from the island of Great Exuma in The Bahamas.

Human-caused climate change is rapidly changing the thermal environments experienced by many species. Most ectotherms, like many of our beloved anoles, maintain small home ranges and are therefore assumed to lack the ability to disperse over long distances. If they can’t migrate to thermally suitable areas, how will anole populations deal with climate change? A major theme emerging in the literature is that evolutionary adaptation may be one of the primary ways that anoles compensate for rapid environmental change.

In close collaboration with many other people, my recent work has focused on thermal adaptation in the brown anole (Anolis sagrei) from The Bahamas. Our early findings suggested that this species may be able to rapidly adapt to changing thermal environments. For example, we found that the thermal optimum for running speed (the “thermal performance curve”) was locally adapted in populations living on a series of thermally variable cays in The Bahamas. Populations were locally adapted despite high levels of gene flow across the archipelago, suggesting that selection is constantly weeding out maladapted genotypes as they arrive and favoring individuals whose thermal biology matched local conditions. We also tested this idea experimentally by transplanting brown anoles from a cool, forested environment to a sun-baked peninsula and tracking (through mark-recapture) which individuals survived and which perished. The peninsula was much warmer and more thermally variable than the ancestral environment, and we were able to show that strong selection favored individuals with higher thermal optima and broader thermal tolerances on the peninsula. While these studies suggested that there is potential for evolutionary adaptation to future climate change, a major question was left unanswered: is there sufficient genetic variation underlying thermal traits such that populations could evolve rapidly? If a trait is not heritable, it will not evolve, and surprisingly few studies have measured the additive genetic basis of physiological traits in lizards.

To answer this question, we captured adult brown anoles from the same two populations involved in our previous transplant experiment (lizards from the islands of Eleuthera and Great Exuma in The Bahamas), brought them back to Bob Cox’s lab at the University of Virginia, and conducted a common-garden breeding experiment. First, Bob raised hundreds of offspring from these two populations, which were native to environments that differed dramatically in their thermal properties. The environment on Eleuthera was much warmer and more thermally variable than the environment on Exuma, so if genetic adaptation had occurred, the offspring of these populations should differ in their thermal physiology when raised in an identical environment, and the differences should be congruent with our previous estimates of natural selection. Interestingly, we found that these populations differed in every aspect of thermal physiology that we measured, but only some of these differences matched our predictions. For example, Eleuthera offspring had higher thermal optima for running speed (predicted to occur based on the warm environment they came from), but lower performance breadths (the opposite of what we predicted because the site on Eleuthera is more thermally variable).

Next, to understand the potential for rapid adaptation to future climate change, we used the pedigrees of the breeding colonies to estimate the additive genetic basis (i.e. heritability) of both the thermal sensitivity of running speed and several aspects of thermoregulatory behavior. For the latter, Don Miles introduced hundreds of Great Exuma individuals to a thermal gradient and measured how they behaved in the gradient. Though the results were somewhat variable, the bottom line is that we found very low heritability in most aspects of thermal physiology and thermoregulatory behavior.

The thermal sensitivity of running speed differed between brown anole populations from the cooler island of Exuma and the hotter island of Eleuthera, even when we raised hatchlings in an identical environment, suggesting that the populations have genetically diverged. Peak running speed for Eleuthera lizards occured at warmer body temperatures, and Exuma individuals ran faster at all body temperatures measured other than the lowest. This figure is copied from Logan et al. (2018).

In general, our results suggest that these populations have adapted to divergent thermal environments in the past, but lack the capacity to evolve rapidly into the future. This could be because strong selection has reduced genetic variation in thermal traits by fixing locally adapted alleles in each environment. Or in the case of the thermal performance curves, it is possible that precise thermoregulatory behavior has removed the need for alleles that confer broad thermal tolerance, leading to mutational decay of those genes. Whatever the cause, we now have evidence to suggest that some thermal traits in brown anoles lack the capacity to evolve rapidly.

There are a number of caveats that go along with our study. First, our sample sizes (Great Exuma = 289, Eleuthera = 119) are modest as quantitative genetic studies go. That fact combined with the difficulty of getting precise estimates of physiological and behavioral traits means that our study should not be considered the final word on the evolutionary potential of thermal performance curves or thermoregulatory behavior in brown anoles or any other species. Second, brown anoles are one of the most successful species on the planet. Indeed, they are extremely common in their native range and have invaded much of the Western Hemisphere. This is not a species that appears to have trouble conquering novel thermal environments, so in no way are we suggesting that they are particularly vulnerable to climate change. In fact, our data suggests that they are likely using behavioral adjustments or phenotypic plasticity to adapt to novel environments, and if anything testifies to the fact that within-generation physiological adjustments can be an extremely powerful tool for mitigating the effects of climate change. Lastly, there are a number of traits we did not measure. What about the critical thermal limits? What about the thermal sensitivity of other performance traits like digestive efficiency, endurance, and bite force? What about thermoconforming species that live deep in forests and have different thermoregulatory strategies and physiological tendencies? There is a lot of work left to be done before we know the full evolutionary potential of anoles under rapid climate change.

The work I’ve discussed here resulted from the efforts of a number of hard-working scientists, including Ryan Calsbeek, Bob Cox, Joel McGlothlin, Don Miles, Katie Duryea, John David Curlis, Anthony Gilbert, Albert Chung, Orsolya Molnar, and Benji Kessler.

Behavioral and TRPA1 Heat Sensitivities in Three Sympatric Cuban Anolis Lizards

By Masakado Kawata

On April 1, 2018

In New Research

I would like to introduce our recently published paper on Comparison of Behavioral and TRPA1 heat sensitivities in Cuban Anolis lizards. In Cuba, three sympatric species of Anolis lizards (Anolis allogus, A. homolechis, and A. sagrei) inhabit different thermal microhabitats (above). Different thermal habitats, that is shade, edges of forests and cleared forests, are occupied by A. allogus, A. homolechis and A. sagrei, respectively. Anolis allogus is non-heliothermic, while A. homolechis and A. sagrei are heliothermic species. Our previous study found that these species showed distinct gene expression patterns in response to temperature stimuli, suggesting the genetically distinct thermal physiology among species (Akashi et al. 2016. Mol.Ecol.).

For lizards, heat avoidance behavior is crucial for limiting their body temperatures within thermally safe margins. We predict that the temperature that elicits heat avoidance behavior would differ between these three Anolis species, and the differences might be related to different heat sensors among the species. Organisms perceive various temperatures via biological temperature sensors, such as thermosensitive transient receptor potential ion channels (thermo-TRPs). Among known thermo-TRPs, transient receptor potential ion channel ankyrin 1 (TRPA1) in non-mammalian species has been reportedly heat sensitive (Saito et al. 2012).

In our paper, we first conducted behavioral experiments to analyze the temperatures at which the three Anolis species escape from heat source (i.e., hotplate; Fig. 1) to examine whether the Anolis species inhabiting locally distinct thermal habitats diverge their thermal tolerances.

Then, for each of the three species, we isolated cDNA encoding of TRPA1, and performed electrophysiological analysis to quantify activation temperature of Anolis TRPA1. We found that temperatures triggering behavioral and TRPA1 responses were significantly lower for the shade-dwelling, non-heliothermic species (A. allogus) than for sun-dwelling heliothermic species (A. homolechis and A. sagrei).

The ambient temperature of shade habitats where A. allogus occurs stays relatively cool compared to that of open habitats where A. homolechis and A. sagrei occur and bask. The high temperature thresholds of A. homolechis and A. sagrei may reflect their heat tolerances that would benefit these species to inhabit the open habitats.

Akashi, H., S. Saito, A. Cádiz , T. Makino, M .Tominaga, M. Kawata. (2018) Comparisons of behavioral and TRPA1 heat sensitivities in three sympatric Cuban Anolis lizards. Molecular Ecology https://doi.org/10.1111/mec.14572

Anoles versus Geckos: The Ultimate Showdown

By Travis Hagey

On March 26, 2018

In Ask the Experts, Introduced Anoles, New Research, Notes from the Field, Research Methods

Two green lizards in Miami, one of each variety.

History is rich with great rivalries; David versus Goliath, Red Sox versus Yankees, Alien versus Predator, but one of the greatest match ups of our time is anole lizards versus gecko lizards. For readers of this blog that are unfamiliar, for which I assume there are few, geckos and anoles are well matched competitors because of their morphological and ecological similarities. Geckos (infraorder Gekkota) are the earliest branch on the squamate tree (sister to all other lizards and snakes) with over 1500 species around the globe, whereas anoles (genus Anolis) appeared roughly 150 million year after the origin of geckos (nested within the Iguania infraorder). The roughly 400 species of anoles can be found primarily in Central and South America. Geckos and anoles both independently evolved very similar hairy adhesive toe pads that help them adhere to and navigate vertical and inverted surfaces. While anoles can likely trace their toe pads to a single origin (and one loss in A. onca), toe pads likely arose and were lost multiple times within Gekkota, although we are still sorting out the exact details (Gamble et al., 2017). Nearly all anoles are arboreal and diurnal, with only a handful of terrestrial or rock dwelling species. Conversely, geckos can be found thriving in arboreal as well as rocky and terrestrial microhabitats day and night.

While anoles tend to get all of the attention from evolutionary ecologists, with decades of amazing research quantifying their habitat use in the Caribbean, geckos are actually older, with more ecological and morphological diversity. As my prior PhD advisor Luke Harmon can surely confirm, I have been interested in knowing how or if insights from Caribbean anole ecomorphology can be applied to geckos. How similar is the evolution and diversification of geckos and anoles? Do geckos partition their habitat along similar dimensions as Caribbean anoles?

In this post, I’d like to share some of my previous work comparing and contrasting gecko and anole diversification and habitat use and then solicit information and opinions from the anole community for an upcoming field trip in which we will be looking at habitat use of sympatric introduced geckos and anoles.

Fig 1. Our reconstruction of gecko (blue) and anole (green) ancestral toe pad performance based on our best fitting weak OU model of trait evolution. Horizontal bars below the X-axis represent the region in which we constrained the origin of toe pads for each clade. Detachment angle (y-axis) represents our measure toe pad performance (the maximum ratio of adhesion and friction a species can generate). The generation of more adhesion for a given amount of friction results in a higher detachment angle. Shaded bands represent our estimated OU optimum value for each clade. Figure modified from Hagey et al. (2017b).

In 2017, we had two great papers come out investigating the diversification of toe pad adhesive performance in geckos and anoles, and the ecomorphology of Queensland geckos. In our diversification paper (Hagey et al., 2017b), we found that while geckos are an older and larger group than anoles, their toe pad performance does not appear to be evolving towards a single evolutionary optimum. Instead, we found that Brownian motion with a trend (or a very weak Ornstein-Uhlenbeck model) best modeled our data, suggesting geckos have been slowly evolving more and more diverse performance capabilities since their origin approximately 200 million years ago (Fig 1). These results assume a single evolutionary origin of Gekkota toe pads, which was supported by our ancestral state reconstructions, but ancestral state reconstructions are far from a perfect way to infer the history of a trait. And so for now, the true history of the gecko toe pad’s origin(s) remains a ‘sticky’ issue. Conversely, adhesive performance in anoles appears to be pinned to a single optima in which anoles quickly reached after their split from their padless sister group (i.e. a strong Ornstein-Uhlenbeck model, Fig 1).

Given these results and the fact that geckos are such a morphologically diverse group, living on multiple continents in many different microhabitats, our results suggest the adhesive performance of geckos may be tracking multiple optima, and when pad-bearing geckos are considered together as a single large group, could produce the general drifting pattern we observed when we assume their ancestor started without little to very poor adhesive capabilities. On the flip side, we can imagine multiple reasons why anoles appear to be limited in their toe pad performance. Perhaps anoles lack the genetic diversity to produce more variable toe pads or they are mechanically or developmentally constrained to a limited area of performance space. Alternatively, since anoles are nearly all arboreal and diurnal in new world tropical environments, it is possible that they are all succeeding in the same adaptive zone and there isn’t the evolutionary pressure or opportunity to evolve more diverse performance capabilities. Closer studies of the adhesive performance capabilities of the few anoles species that have branched out from arboreal microhabitats, such as the rock dwelling aquatic species would be really interesting!

Fig 2. Our gecko and anole residual limb length calculations suggest geckos (grey triangles) generally have shorter limbs then anoles (black circles). Figure modified from Hagey et al. (2017a).

In our second paper from 2017 (Hagey et al., 2017a), we quantified microhabitat use and limb lengths of geckos across Queensland, Australia and compared these patterns to those known from Caribbean anoles. We found some interesting differences and similarities. Our first result arose as we tried to calculate residual limb lengths and realized that geckos, as a group, have shorter limbs than anoles, which resulted in us calculating residual limb lengths for geckos and anoles separately (Fig 2). We then compared microhabitat use and limb length patterns and found that Strophurus geckos may be similar to grass-bush anoles. Both groups have long limbs for their body lengths and use narrow perches close to the ground. We also found other general similarities such as large bodied canopy dwelling crown-giant anoles and large bodied canopy dwelling Pseudothecadactylus geckos. Unfortunately, we didn’t focus on sympatric Australian geckos and so we couldn’t make direct habitat partitioning comparisons to anoles. We hope to fix that in our next project and would really love to hear from you, the anole community.

Later this spring, I am planning a fieldtrip with John Phillips and Eben Gering, both fellow researchers here at Michigan State University, to Hawai’i (Kaua’i and O’ahu) to investigate habitat partitioning of invasive geckos and anoles, specifically A. carolinensis, A. sagrei, and Phelsuma laticauda. Jonathan Losos one claimed that Phelsuma are honorary anoles! These three species are all diurnal, arboreal, have adhesive toe pads, and are commonly seen in Hawai’i and so we expect them to be competing for perch space. This has been on some of the greatest anole minds since at least 2011 with Jonathan wondering which group would win when the two clades collide in the Pacific. Previous studies of anole ecomorphs across the Greater Antilles and invasive A. sageri in the southeastern US give us a good expectation of how the trunk-crown A. carolinensis and the trunk dwelling A. sagrei should interact and partition their arboreal microhabitat, with A. sagrei pushing A. carolinensis up the trunk. The wild card is P. laticauda. There hasn’t been much microhabitat use work done with Malagasy geckos, and definitely nothing compared to the extensive work with Caribbean anoles. As a result, I don’t know much about exactly what part of the arboreal environment P. laticauda uses in its natural range or how it will fit in with its new pad-bearing brethren in Hawai’i. The best information we have to my knowledge is a study of other arboreal Phelsuma by Luke Harmon in Mauritius (Harmon et al., 2007). He found that while the Phelsuma geckos of Mauritius also partition their arboreal habitat by perch height and somewhat by diameter, they also partition by palm-like or non-palm-like perches. I’m not aware of any anole observations suggesting a palm/non-palm axis of partitioning and so this may be a novel axis that P. laticauda is using in Hawai’i to live in amongst the anoles.