It’s been a while since we’ve looked at an anole from South America, so why not go all the way over to an an anole that is probably at the highest elevation an anole species has ever been found: Anolis heterodermus, the Flat Andes anole!
Anolis heterodermus lizards are arboreal and can be found on montane elevations in Colombia and Ecuador at about 2,600 m (8,530 ft). As you can guess, living at an such an elevation should be too cold for a lizard, but the Flat Andes anole is ok with this. They have been found to have wider preferred and body temperature ranges than expected for anoles and have adapted to take advantage of the limited hours of sun that the area gets (Méndez-Galeano & Calderón-Espinosa, 2017).
These anoles are large rich green to olive lizards with males being slightly larger than females at 85.4mm and 85mm respectively. They have wide banding on their bodies and both males and females have a patch on their tails that have been observed to change from red to blue throughout the day. This patch is larger in males (Beltrán, 2019) and is another sign of sexual dimorphism in this species. Their dewlaps are pink striped.
More on Anolis heterodermus from the pages of Anole Annalshere.
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 isolepis, Photo by Yasel U. Alfonso iNaturalist
Anolis alutaceus, Photo by Yasel U. Alfonso iNaturalist
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.
Méndez-Galeano, Paternina-Cruz, and Calderón-Espinosa
Abstract
Vertebrate ectotherms may deal with changes of environmental temperatures by behavioral and/or physiological mechanisms. Reptiles inhabiting tropical highlands face extreme fluctuating daily temperatures, and extreme values and intervals of fluctuations vary with altitude. Anolis heterodermus occurs between 1800 m to 3750 m elevation in the tropical Andes, and is the Anolis species found at the highest altitude known. We evaluated which strategies populations from elevations of 2200 m, 2650 m and 3400 m use to cope with environmental temperatures. We measured body, preferred, critical maximum and minimum temperatures, and sprint speed at different body temperatures of individuals, as well as operative temperatures. Anolis heterodermus exhibits behavioral adjustments in response to changes in environmental temperatures across altitudes. Likewise, physiological traits exhibit intrapopulation variations, but they are similar among populations, tended to the “static” side of the evolution of thermal traits spectrum. The thermoregulatory behavioral strategy in this species is extremely plastic, and lizards adjust even to fluctuating environmental conditions from day to day. Unlike other Anolis species, at low thermal quality of the habitat, lizards are thermoconformers, particularly at the highest altitudes, where cloudy days can intensify this strategy even more. Our study reveals that the pattern of strategies for dealing with thermal ambient variations and their relation to extinction risks in the tropics that are caused by global warming is perhaps more complex for lizards than previously thought.
Hot off the press — the latest anole journal cover!In this issue of Nature Ecology & Evolution, Shane Campbell-Staton and I led a team of researchers to explore the effects of urban heat islands on anoles. We found that not only can urban Anolis cristatellus tolerate higher temperatures than their forest counterparts, but also identified genomic regions associated with divergent thermal tolerance. Check out a summary of this work at the urban evolution blog I co-edit, Life in the City: Anoles Adapt to Beat the Urban Heat.
Campbell-Staton, Winchell, Rochette, Fredette, Maayan, Schweizer, and Catchen
Abstract
Only recently have we begun to understand the ecological and evolutionary effects of urbanization on species, with studies revealing drastic impacts on community composition, gene flow, behaviour, morphology and physiology. However, our understanding of how adaptive evolution allows species to persist, and even thrive, in urban landscapes is still nascent. Here, we examine phenotypic, genomic and regulatory impacts of urbanization on a widespread lizard, the Puerto Rican crested anole (Anolis cristatellus). We find that urban lizards endure higher environmental temperatures and display greater heat tolerance than their forest counterparts. A single non-synonymous polymorphism within a protein synthesis gene (RARS) is associated with heat tolerance plasticity within urban heat islands and displays parallel signatures of selection in cities. Additionally, we identify groups of differentially expressed genes between habitats showing elevated genetic divergence in multiple urban–forest comparisons. These genes display evidence of adaptive regulatory evolution within cities and disproportionately cluster within regulatory modules associated with heat tolerance. This study provides evidence of temperature-mediated selection in urban heat islands with repeatable impacts on physiological evolution at multiple levels of biological hierarchy.
Extreme heat events are becoming more common as a result of anthropogenic global change. Developmental plasticity in physiological thermal limits could help mitigate the consequences of thermal extremes, but data on the effects of early temperature exposure on thermal limits later in life are rare, especially for vertebrate ectotherms. We conducted an experiment that to our knowledge is the first to isolate the effect of egg (i.e. embryonic) thermal conditions on adult heat tolerance in a reptile. Eggs of the lizard Anolis sagrei were incubated under one of three fluctuating thermal regimes that mimicked natural nest environments and differed in mean and maximum temperatures. After emergence, all hatchlings were raised under common garden conditions until reproductive maturity, at which point heat tolerance was measured. Egg mortality was highest in the warmest treatment, and hatchlings from the warmest treatment tended to have greater mortality than those from the cooler treatments. Despite evidence that incubation temperatures were stressful, we found no evidence that incubation treatment influenced adult heat tolerance. Our results are consistent with a low capacity for organisms to increase their physiological heat tolerance via plasticity, and emphasize the importance of behavioural and evolutionary processes as mechanisms of resilience to extreme heat.
Another SICB, another great presentation from Sylvia Nunez from Thom Sanger’s lab investigating how the interaction between heat and oxygen availability affects development in the brown anole (Anolis sagrei). Last year, Sylvia presented a poster showing that above 33°C, embryonic survival was greatly reduced and many embryos developed craniofacial malformations. With some potential nesting sites for anoles now exceeding 40°C, understanding mechanisms leading to decreased survival is critical.
Low oxygen at sublethal temperatures can recapitulate negative effects on craniofacial development at high temperatures.
As a follow up to this study, Sylvia set out to understand exactly how it is that heat and oxygen can interact to lead to craniofacial deformities. She posited several hypotheses and was able to eloquently test each one, including the neural degeneration hypothesis and the oxygen limitation hypothesis. Specifically, Sylvia noted that disruption in sonic hedgehog has been linked to facial development and that oxygen demand can often exceed oxygen supply at high temperatures.
First, Sylvia tested the oxygen limitation hypothesis by examining whether low oxygen coupled with sublethal (elevated) temperature conditions recapitulate the effects of craniofacial malformation under thermal stress. Previous work in the lab induced craniofacial malformation at 36°C; Sylvia showed you could mimic this effect using 33°C with low oxygen, with a greater rate of malformation than in 27°C (the standard control temperature) with atmospheric oxygen, 27°C with low oxygen, or 33°C with atmospheric oxygen. She then tested whether an increase in oxygen can rescue embryonic survival at high temperatures. To do so, she split eggs among two treatment conditions: 27°C with high oxygen and a hot nest site temperature with high oxygen. She found further support for the oxygen limitation hypothesis – when oxygen availability was increased above atmospheric conditions there were no differences in embryonic survival. Wow! Further, there were no craniofacial malformations in the high temperature treatment when oxygen conditions were high.
To follow up on this finding, she examined if oxidative stress could be the link between temperature and craniofacial malformations using superoxide dismutase (SOD), an enzyme that helps turn the superoxide radical (O2–) into oxygen (O2) or hydrogen peroxide (H2O2), as a marker for oxidative stress in the telencephalon. Indeed, within mere minutes of a temperature increase, SOD becomes upregulated, suggesting that thermal stress contributes to oxidative stress. But Sylvia didn’t stop there. She then treated some embryos with an SOD inhibitor to show that when SOD is absent craniofacial malformations appear.
Overall, Sylvia has very eloquently shown that increased temperature leads to craniofacial malformations via thermal effects on oxidative stress. I cannot wait to see what she presents next year!
We all know that the anoles of the Caribbean partition the habitat based on structural environment and microclimate, leading to patterns of correlated morphology and habitat use within these ecomorphs. While we know a substantial amount about the morphological aspect of the ecomorph concept, many questions remain concerning the patterns of physiological trait evolution across Caribbean anoles and how this relates to habitat use and ecomorphology.
Brooke Bodensteiner, a PhD student in the Muñoz lab at Virginia Tech, is digging into this topic for her doctoral research. In her presentation at Evolution 2019, Brooke told us about two key questions she is attempting to address in her research: (1) Do ecomorphs overlap in physiological trait space or do they neatly differentiate into distinct groups as they do with morphology? and (2) Do thermal traits evolutionarily respond to the same microhabitat predictors?
Brooke measured thermal physiology of anoles in the Dominican Republic, including Anolis cybotes, shown here.
Brooke is investigating these questions in Hispaniolan anoles and has so far sampled 28 of the 41 species found in the Dominican Republic with representatives from all 6 ecomorphs! The Hispaniolan anoles are particularly good for this research topic since there are representatives of each ecomorph in very diverse habitats islandwide, providing many opportunities for physiological diversification. Building on a large dataset of morphological traits, Brooke collected thermal physiology data from all 28 of these species including critical thermal minimum and maximum and preferred temperature, to try to understand the patterns of physiological diversification and how they are correlated with morphological diversification.
Brooke’s results were fascinating, but more complex and nuanced than expected. Consequently, we will only tell you that her findings are intriguing and will give us a lot to ponder regarding patterns of correlated trait evolution and environmental factors driving physiological evolution. I look forward to seeing the finalized results published soon!
Climate change on earth is accelerating. These changes will have important impacts on all species, but some types of organisms are predicted to be affected more strongly than others. One such group is ectotherms which use the temperatures available in surrounding habitats to regulate their body temperatures. Another such group is mountaintop endemics. These species are restricted to one or several mountain peaks by climate and/or competition with other organisms. As such, they cannot easily disperse to other areas if climate makes their current habitat unsuitable!
Mountaintop endemic species may be particularly vulnerable to climate change (Chand Alli, CC BY SA).
Hispaniola contains several high elevation areas home to mountaintop endemic species, including anoles (NASA).
Many studies use correlative modeling approaches (often termed ecological niche models [ENMs] or species distribution models [SDMs]) to assess a species’ current distribution and predict its future distribution by projecting it into simulated future climate scenarios. This approach has some advantages including ease of implementation across many species. However, it has at least two potential drawbacks: the environmental data used in building such models are often measured at a fairly coarse scale that does not represent how many organisms use their environments, and the models do not explicitly include biological processes such as physiology and behavior.
Anolis armouri in a montane rock meadow (Reptile Database).
Vincent Farallo, a post doc at Virginia Tech, and his advisor, Martha Muñoz (both moving to Yale in a few weeks!), investigated whether incorporating physiology and behavior into modelling might affect predictions of climate change impacts on two mountaintop endemic anoles of Hispaniola, Anolis armouri and Anolis shrevei. Correlative SDMs (via BioMod2) predicted both species would lose much or all of their suitable habitat under climate change, perhaps leading to extinction. However, when Vincent constructed mechanistic niche models (via NicheMapR) that included knowledge about the thermal physiology and habitat use behavior of these species to predict activity time, they showed that habitat would increase in suitability under climate change, the opposite result! Interestingly, these models also predicted increased suitability for a widespread anole, A. cybotes. This result suggests that while climatic changes may not be a direct threat to these mountaintop anoles, increased competition with another anole, an indirect impact of climate change, may be.
Activity time of Anolis shrevei is predicted to increase across its range in Hispaniola with climate change (Farallo and Munoz).
As a whole, Vincent and Martha’s work shows that incorporating more mechanistic knowledge into models, including physiology and behavior, may be critical to predicting the impacts of climate change on organisms and making sound conservation decisions.
Brown anoles are invasive throughout the southeastern United States and are often transported via the nursery trade.
As invasive species expand across landscapes, they may engage in new interactions including with native competitors and prey as well as encountering novel environmental conditions such as different temperatures or patterns of rainfall. It is often difficult to observe the process of how invasive species which are dispersing across landscapes are affected by these novel conditions, because it may be difficult to find edge populations of invaders, and those extralimital populations which do not survive may have disappeared before scientists can observe them.
In southern Florida, many anole species have been introduced and are expanding their ranges, perhaps none more prolifically so than the brown anole (Anolis sagrei). In the past 75 years or so, brown anoles have occupied all of peninsular Florida, the eastern seaboard of Georgia, and Gulf Coast habitats through Louisiana. Many of these expansions are thought to occur via hitchhikers on cars or via the nursery trade, in which potted plants with adults or eggs are transported to new areas. These introductions may fail for many reasons (e.g., inhospitable environments, low numbers of colonizers, intentional extirpation by humans), but these processes of dispersal, establishment, and extirpation are difficult to study. Dan Warner, a professor at Auburn University, took advantage of a known extralimital population of brown anoles in a greenhouse in central Alabama to study the survival of a population created through this type of dispersal.
This population of anoles existed well north of its continuous invasive range in the United States and was exposed to much colder winter conditions than other studied populations. It was present at the greenhouse from at least 2006, and so survived for at least 10 generations, long enough for adaptation to these novel thermal conditions to potentially occur. Working with a team of undergraduates, graduate students, and post-docs, Dan assessed the thermal conditions in the greenhouse environment, conducted mark-recapture studies of the population, and measured thermal tolerances of lizards.
Dr. Amélie Fargevieille and Jenna Pruett representing the Warner Lab at SICB 2019.
At SICB 2019, Dr. Amélie Fargevieille and Jenna Pruett presented results from the study, showing that the greenhouse population included all life stages of lizards and reached a total size of >1000 individuals. While one might expect that these northern lizards would have altered critical thermal limits, the Warner lab showed that both the upper and lower thermal limits of these lizards (the temperatures at which their movements became uncoordinated), were the same as those found in lizards from warmer, southern populations. These results indicate that existence in a colder northern climate for >10 years did not lead to adaptive changes in thermal limits, perhaps due to the population occupying a thermally-buffered habitat, i.e., the greenhouse.
While hurricanes have facilitated several fascinating studies of anole adaptation (e.g., Schoener et al., 2017, Donihue et al., 2018), they may also take these opportunities away. In the case of this population, Hurricane Irma blew off the greenhouse roof in 2017 (which remained unrepaired), exposing this population to the rigors of a central Alabama winter. Multiple surveys in 2018 confirmed that there were no survivors of this previously robust population. Dataloggers confirmed that, even in the most sheltered microhabitats that remained, temperatures dropped below the critical thermal minima of brown anoles, presumably extirpating the entire population.
Recent Extinction of a Viable Tropical Lizard Population from a Temperate AreaWARNER, DA*; HALL, JM; HULBERT, A; TIATRAGUL, S; PRUETT, J; MITCHELL, TS; Auburn University.
Hot off the press — the latest anole journal cover! In this issue of 
