Anoles are also models for urban evolution. Why? Anoles are found abundantly across the Caribbean in urban and forest environments where they specialize in divergent microenvironments characterized by shifts in climate and physical structure. Urban habitats tend to be warmer, drier, more open, and dominated by buildings and impervious surfaces instead of vegetation — providing the perfect opportunity for repeated adaptation to a novel combination of environmental conditions. In other words, Caribbean cities provide a replicated natural laboratory to study adaptation as it happens when these lizards colonize and thrive in urbanizing areas. And there is no shortage of urban-tolerant and urbanophilic anole species to choose from!
Species of Anolis lizards are found in urban environments across the Caribbean (photos CC-BY K. Winchell; Earth at night by NASA).
So I’ve been reading a lot of anole papers, aside from the ones I normally read for fun (can’t believe I read papers for fun now), and I found an anole that’s pretty similar to two anoles I’ve looked at before but also still unusual.
Welcome back by the way. Nice to have to you here again.
This week is a third little cave anole, Anolis alvarezdeltoroi, or the Mexican cave anole. Mexican cave anoles live in a similar karst limestone habitat like Anolis bartschi and Anolis lucius and are often found deep inside caves, occasionally sleeping from the roof it. They may also perch from vegetation in or around the caves, particularly as juveniles.
Like the other two anoles, the Mexican cave anole has a similar short body/long hindleg morphology. In a paper redescribing the species, the average SVL of the male anoles they measured was 53.3-74.0 mm, and 49.6-66.5 mm in females.
They seem to rely heavily on the karst habitat with healthy populations being found in areas with diminished forest but intact limestone/cave areas.
Male Mexican cave anoles have dark red dewlaps with white lateral rows of scales, while females have smaller black dewlaps with a similar pattern.
Please read the paper redescribing this anole here! For a while there was only a specimen available of it and not much info, but they worked on it and you should check it out. I wouldn’t have been able to write this if it wasn’t for them.
Turns out grad school eats up a lot of your time some weeks. Who knew!
So here is a pretty cool Caribbean anole this week. Anolis acutus, the Sharp Anole is endemic to St. Croix. These anoles are tan to olive in colour. Their dewlaps are white with a large yellow-orange blotch closer to the body. Males have an average SVL of 67mm and females, about 49mm.
They are territorial and maintain hierarchies within their habitats. If an individual is removed, they become slightly agitated until the territory is taken over by a new anole or the individual returns (Ruibal & Philibosian, 1974). The adults also tend to be sedentary and have a perch height hierarchy, but exclude juveniles from occupied trees leaving them to find and occupy empty ones or live on the ground (Ruibal & Philibosian, 1974).
St Croix anoles appear to be eurythermal, meaning they have a broad temperature range (McManus & Nellis, 1973).
Cities are hot. Because of the urban heat island effect, urban environments tend to be significantly warmer than nearby non-urban environments. For ectothermic organisms, like lizards and insects, elevated urban temperatures create thermally stressful conditions. It might be unsurprising then that researchers have documented an increase in thermal tolerance in urban animals (e.g., City Ants Adapt to Hotter Environment). These studies point to the ability to cope with elevated urban temperatures as a critical aspect of persisting in urban environments.
Although there is evidence that the urban environment shapes adaptive thermal tolerance in Anolis lizards at the genomic level, it is also possible that anole species that thrive in hot urban environments have an innate ability to do so due to local adaptation in their ancestral habitat (i.e., forests). In fact, an analysis of patterns of urban tolerance across Caribbean anoles found that species that experience hotter and drier temperatures in their native ranges and those that maintain higher field body temperatures tended to be the ones that do well in urban environments (Winchell et al. 2020). And when researchers looked at genomic variation in Cuban species not found in urban areas, they identified genes associated with thermal sensitivity (Akashi et al. 2016), suggesting tolerance of different thermal environments may be encoded at the genomic level. But does this mean that some anoles are predisposed to tolerate hot urban temperatures based on the climate of their ancestral forest homes?
Kanamori et al. (2021) — “Detection of genes positively selected in Cuban Anolis lizards that naturally inhabit hot and open areas and currently thrive in urban areas” — set out to answer this question by examining the transcriptome of nine species of Cuban anoles that occupy different thermal microhabitats. Cuba is home to the largest number of anole species, with species diversifying to occupy distinct thermal and structural microhabitats. In their study, the researchers attempted to identify genomic signatures of selection in non-urban populations of species that thrive in urban environments in order to understand if there was something unique about the genetic background related to thermal tolerance in these species that enables urban colonization.
Of the nine species Kanamori and colleagues studied, three are found in naturally hot and open environments: A. allisoni, A. porcatus, and A. sagrei, representing two different branches of the Cuban anole radiation. These three species (and several of their close relatives) also thrive in urban environments both in Cuba (e.g., Havana) and in their non-native range (e.g., Miami, Florida).
Anolis porcatus, Photo by James Telford iNaturalist
Anolis allisoni, Photo by Juan Rafael Rodríguez iNaturalist
Five other species are found in cool and deeply shaded forests: A. alutaceus, A. isolepis, A. garridoi, A. allogus, and A. mestrei. The last species, A. homolechis, is common in the shaded areas of forest margins.
Anolis homolechis, Photo by Alex Alfil iNaturalist
Kanamori and colleagues examined a total of 5,962 genes and found genomic signatures of selection in 21 genes in the two main branches of species that contain urbanophilic species (A. porcatus & A. allisoni, and A. sagrei), but did not identify selection in the same genes across the two lineages. In other words, these closely related species have found unique genomic pathways to deal with the hot and dry forest environments in which they thrive. This finding suggests that the predisposition to tolerate hot urban environments is determined by different genes in different anole species, and raises the possibility that further local adaptation to urban thermal environments may also be lineage specific.
When the researchers looked at the functional associations of the genes under selection in each species, they found that they were related to stress responses, epidermal tolerance to desiccation, and cardiac function. All three of these biological functions are implicated in maintaining appropriate acclimation responses to thermal stress in anoles. These findings implicate ancestral selection on stress responses, perhaps in response to thermal or ultraviolet radiation, as potential factors influencing tolerance of anoles in urban environments. Further exploring the importance of these functions will shed light on their role in the initial tolerance of urban environments upon urban colonization and adaptive modification as urban lineages persist.
Evolution has long thought to be a slow process, taking thousands if not millions of years. Recently, there has been a paradigm shift in how scientists think about evolution. We now know that we can observe evolution on a contemporary timescale, observable to the human eye. Dan Nicholson, a Ph.D. Candidate at Queen Mary University of London in Rob Knell’s lab, is working with Mike Logan and others to observe the effects of habitat change on the evolutionary ecology of Anolis apletophallus.
Dan and his team transplanted anoles from the mainland of Panama to several islands around Barro Colorado Island in July of 2017. Before release, they recorded the anoles’ morphological characteristics, including hindlimb and forelimb length, toe pad size, and head depth, and well as characteristics of their perch location, including height and width. Tracking changes in these characteristics can detect natural selection at work. At SICB 2019, Dan reported the results of the first generation of island anoles.
At SICB 2020, Dan included the trends of the second generation of island anoles. The preliminary results indicate the island anoles have continued to use wider perches than the mainland anoles. However, the majority of the island anole morphological traits now align with the mainland anoles. The exception is that hindlimb length of the island anoles decreased, while the mainland anoles hindlimb length has increased.
Some potential causes of these results, Dan speculates, include genetic drift due to the small population size. The islands started with a robust number of anoles, but over the two years of this study, their numbers have rapidly dwindled. Another possibility is the island anoles are aligning with the mainland anoles morphologically due to gene flow. In the future, Dan wants to further analyze the preliminary results from a population angle, looking at changes in groups of traits instead of individual traits.
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.
Anoles, geckos, and Hawai’i have come up repeatedly here on Anole Annals
and so we know folks have been thinking about these species and specifically this invasive set of species for a while. We are especially excited to see Amber Wright’s research suggesting P. laticauda was perching above A. carolinensis in her enclosures. We want to know what the anole community has to say. We also don’t want to duplicate or intrude on any projects that are already under way.. If this is something you’ve already started, or started to wonder about… let us know! We would love to collaborate, partitioning interesting questions, if there are already labs working in this arena. We would also be grateful for suggestions, field site recommendations, or relevant publications we may have missed.
Urbanization, the creation and spread of urban habitats, is increasing across the world. Species that live in these urban habitats are subject to many alterations in their environment, including changes in food, predators, noise, and light among others. One of the most well-known changes associated with cities is the “Urban Heat Island” effect, where city habitats are hotter than surrounding areas due to increases in pavement and other heat-absorbing materials. For lizards such as anoles, living in this hotter environment could be challenging, as increased heat could reduce time available for foraging for food or defending territories, or, in more serious cases, might even lead to death. Shane Campbell-Staton, a postdoctoral researcher at the University of Illinois and the University of Montana, decided to test if anoles were adapting to these hot urban environments, and, if so, what mechanisms were driving this adaptation.
Cities are hotter than the surrounding landscape.
Shane worked with crested anoles (Anolis cristatellus) from four different areas of Puerto Rico that had both urban and nearby natural environments. He and Kristin Winchell, his coauthor, verified that anoles in these urban habitats did indeed experience hotter conditions, and that, as a result, their body temperatures were also higher than anoles from nearby natural areas. In the lab, Shane found that these city anoles were capable of tolerating higher temperatures than their counterparts from natural areas as well. However, after 8 weeks in the lab, anoles from both types of habitats had similar temperature tolerances. Shane also raised offspring from these anoles under common conditions in the lab and found that these offspring had similar temperature tolerances (thermal limits), regardless of whether they came from urban or natural environments. These results show that anoles can have a plastic response to the thermal conditions in their environment, meaning that the differences Shane and Kristin saw in Puerto Rico are induced by an anole’s exposure to temperatures and are not completely determined by their genes.
Crested anoles (Anolis cristatellus) make use of many human-altered habitats. Photo by Andrew Battles.
Shane, however, continued to explore this question: he wanted to know if the ability, or plasticity, of an anole to alter its thermal tolerance in response to exposure to high urban temperatures was due to changes in its genetic structure. In essence, he wanted to know if anoles had evolved a higher responsiveness (or plasticity) in response to inhabiting hotter, city habitats. To get at this, Shane exposed anoles to both hot and normal temperatures in the lab and looked at their levels of gene expression. Using a transcriptomics approach, Shane could see which genes were activated differently when lizards were exposed to temperatures indicative of city and natural habitats. Shane observed differences in variation in the genes in use at these temperatures. He also found higher levels of differentiation between genes involved in thermal adaptation between lizards from city and natural environments. These exciting results show that living in hotter city environments has selected for lizards which are more able to respond to these hot temperatures when they experience them. Shane is continuing to dig deeper into these data to determine which specific genes may have been altered to understand the mechanisms by which lizards are able to alter their heat tolerances. We’re looking forward to seeing these results at a future conference!
On a side note, Shane will be setting up his own lab at UCLA this year, and he’ll be looking for talented graduate students interested in physiology, adaptation, and genomics. Don’t hesitate to look him up!
Maintaining an already-impressive 2016 conference tour de force which included presentations at both JMIH and Evolution, Kristin Winchell presented a broad summary of her urban anole research in an invite-only Urban Ecology session at ESA 2016.
This presentation provided a synthesis of two large research projects both independently reviewed on Anole Annals (1,2), and so I will provide only a brief summary here. Kristin began by presenting an over-arching question in modern ecology: how is urbanisation going to affect biodiversity? While many may intuitively think of the process negatively, there is a large (and growing) body of research suggesting that many species are able to behaviourally respond to these novel environments and persist. So what about anoles? Kristin focuses her research on two Puerto Rican species: the crested anole (Anolis cristatellus) and the barred anole (A. stratulus).
To do this, Kristin and her team employed multiple methods to explore if a) these two species have differences in their ecology in urban vs. natural areas, b) if differences in ecology are observed, does this lead to differences in morphology, and c) if differences in morphology are observed, is this related to performance? Firstly, niche partitioning between these two species in natural vs. urban areas was investigated (more details here).
This niche partitioning research is new and will be the main body of a manuscript currently in prep so I will keep discussions brief. One species, A. cristatellus, was observed to significantly shift its microhabitat use, which resulted in adaptive shifts in morphology. This research was documented in Winchell et al.’s recent Evolution paper and reviewed previously on AA (1,2,3). Specifically, urban lizards have longer limbs and stickier toepads (higher number of subdigital lamellae) in response to perching on broader, slippier substrates.
This research has now developed on to the next stage of performance-related investigations. Kristin is asking the question of whether these observed morphological shifts lead to better performance (and therefore, presumably, higher fitness). Kristin presented some preliminary results, but keep your eye out for more developments!
Lizard in an Evolutionary Tree's reworking of Williams' classic figure. Note that A. gundlachi is a trunk-ground anole, not, as indicated, a trunk-crown anole.
In this famous figure, Ernest Williams sketched out his view of how anole diversification occurred on the Greater Antilles, using Puerto Rico as an example. First, species diverge to use different structural habitat, producing the different ecomorphs. Subsequently, within-ecomorph divergence produces species that use the same structural habitat, but which occupy different climatic micro-climates, ranging from cool and moist rainforest to blazing hot and dry semi-desert. This two-stage pattern of evolution is displayed not only on Puerto Rico, but also on Cuba and Hispaniola (Jamaica, the most species deprived island, has little within ecomorph diversity).
In contrast to the plenitude of research in recent years on the adaptive basis of morphological differences among the ecomorphs, relatively little work has focused on the extent to which closely related species—members of the same ecomorph class—have adapted to occupying different microclimates.
Species of Anolis lizards are found in urban environments across the Caribbean (photos CC-BY K. Winchell; Earth at night by NASA).
