HerpHighlights Podcast: an Assortment of Anoles

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On June 10, 2018

In All Posts

HerpHighlights is a Podcast run by Tom Major and Ben Marshall in which they discuss recent advances and interesting news on reptile and amphibian behavior, ecology, and conservation.

This podcast is now live and you can listen to it by clicking the link below:

https://herphighlights.podbean.com/e/026-assortment-of-anoles/

In this episode, Tom and Ben discuss many interesting research topics – both new and old – involving anoles. Notably touching on Kamath & Losos’ recent commentary on the mating systems of brown anoles (A. sagrei) in Florida, as well as Medina et al.’s review of the evolution of dorsal patterning across Caribbean anoles.

Check it out!

Kamath, A, and JB Losos. 2018. “Estimating Encounter Rates as the First Step of Sexual Selection in the Lizard Anolis Sagrei.” Proceedings of the Royal Society B: Biological Sciences 285 (1873): 20172244.

Medina, I, JB Losos, and DL Mahler. 2016. “Evolution of Dorsal Pattern Variation in Greater Antillean Anolis Lizards.” Biological Journal of the Linnean Society 120 (2): 427–35.

 

Drivers and Constraints of Within-Species Diversity in Dewlap Design

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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.

Sometimes Knights Eat Dragons (Dragonflies, That Is!)

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On June 4, 2018

In Introduced Anoles, Natural History Observations

One of the loudest anole meals I’ve witnessed.

During one recent afternoon’s field work, I heard an unusual noise in the botanical garden I was working in: a sound like someone crunching and crinkling a foil potato chip bag. Tracing the sound from about 20 feet away, I did not find a snacking plant enthusiast, but rather a young Knight Anole (Anolis equestris) in survey posture who had apparently just snagged a large dragonfly out of mid-air. The anole chowed down on its prey while keeping a weather eye on me and conducting a few half-hearted displays to let me know it was aware of my presence. As the anole continued to masticate its rather large afternoon meal, it moved to a higher perch away from the prying eyes of this anolologist.

The dragonfly, a Regal Darner (Coryphaeschna ingens), is a common species in the southeastern United States and an accomplished aerial predator. It was also more than a mouthful for this young knight, which had to chew with its mouth open for over four minutes (and still wasn’t finished when it escaped my view); quite the prey handling time! And yet more evidence that this largest of anole species is willing to take a chance on any prey item that might fit into its maw even if it takes a little work.

An impressive snag for such a young anole.

Can Evolution in Brown Anoles Keep Pace with Climate Change?

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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.

Anole Dewlapping at Bird? Part of the Fauna “Visiting” Camera Traps

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On May 31, 2018

In All Posts

Camera traps have been placed in front of some karst solution holes in the dry-transition forest of the southern slopes of the Sierra de Bahoruco, in the Pedernales province, Dominican Republic.

The holes hold water after rains, making it one of the very few spots where water is available in that forest (no surface rivers or marshes around). These holes are visited by a variety of animals, which include herps like whiptails, curlytails, racers, iguanas, and other rarities like the solenodon, and many birds.

I wanted to share this photo, since in it is the first anole recorded, an Anolis strahmi, which seems to be displaying at a nearby bird (Ovenbird, placed at extreme right of the frame).

Insular Lizards and Urban Lizards: How Brave Are They When it Comes To Foraging?

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On May 28, 2018

In All Posts

This particular lizard did not show much fear towards our plastic snake. Photo credit: Bjorn Briesen

And now for something completely different … lacertid lizards. It almost feels like I am releasing an invasive species within Anole Annals, but dr. Jonathan Losos nevertheless kindly asked me to write something about our recent paper on the effect of insularity and urbanization on the foraging decisions of the Dalmatian Wall lizard (Podarcis melisellensis), stating that “Lacertids are honorary Anoles.”

The Functional Morphology Lab of the University of Antwerp has a long-standing tradition of research on the Croatian islands. Once a year, several members of our team travel to Croatia, accompanied by a bunch of students in the context of a course on Island Biology. In fact, four out of six collaborators on our paper (including me) were still undergraduate students when conducting the fieldwork. We soon came up with the idea to compare risk-taking and reaction to novelty of wall lizards during foraging in both urban and insular environments. Strange choice? Not at all. Both urban and insular habitats are characterized by reduced levels of predation, but also a lack of resources (e.g. lower abundance and diversity of arthropod prey). Such conditions should prompt both insular and urban lizards to behave bolder during foraging, and act less neophobic, since the risk of predation is low, but the value of the food reward is high. Fortunately, the Croatian islands are perfect to test these kind of hypotheses. Sampling both rural and urban areas on the larger island of Vis was a piece of cake, especially since wall lizards can easily be found in the harbour of Vis.

Believe it or not, wall lizards can easily be found in the harbour of vis. Photo credit: Gilles De Meester

Vis itself is surrounded by many small islets, most of them inhabited by dense populations of lizards. Some of these islets, like Biševo and Veli Budikovac, are (semi-)inhabited. Others, like Brusnik, are completely devoid of any human activity. So, small islets? Check. Urban and rural areas? Check. What else was needed? A predator model to test risk-taking, and a novel object to test neophobia. After a few pilot trails in which we compared the response of lizards to a plastic snake model and a stuffed rook (Corvus frugilegus), it was clear that lizards showed more fear of the snake. Our novel object was randomly chosen to be a flashy red drinking bottle.

Lizards from smaller islets did indeed take more risks while foraging compared to lizards from the main island. Islet lizards were more likely to leave a safe refuge in order to get a tasty mealworm, despite the presence of the snake model, and also on average left their refuges faster to do so. In fact, on multiple occasions, lizards did completely ignore the snake model, even running over it to get to the petri dish with food.

Another example of a very bold lizard. Photo credit: Bjorn Briesen.

But even on the main island of Vis, lizards behaved very boldly. In fact, between observations, we were often capable of hand-feeding some wild individuals. On the island of Brusnik, a few lizards showed absolutely no fear at all of humans, even licking and biting our hands when we came close to remove the petri dish at the end of a trail. This is, of course, a very nice illustration of  the phenomenon known as “island tameness.” Due to a lower number of predators on islands and islets, insular species often lack normal antipredator behaviour, something that even Darwin already reported after his famous voyage on the Beagle. Unfortunately, this tameness is the main reason for the historical decline and extinction of many insular species, especially after humans started bringing new predators (rats and cats) to these islands.

Maybe he was just thirsty? Photo credit: Gilles De Meester

Neophobia, whether the lizards were willing to feed in front of a novel object, did not differ between main island and small islets, despite the assumption that islet lizards should behave less neophobically as they will benefit more from exploiting new resources. In fairness, lizards overall seemed to lack a neophobic reaction towards the novel object, as they did not differ in feeding latencies from the control group. Interestingly, however, in Brusnik, lizards behaved very neophilically towards the drinking bottle. Some individuals even completely ignored the offered food in favour of this novel object.

Surprisingly, lizard behaviour did not differ between urban and rural environments. While numerous papers have proven that urban birds and mammals  behave more boldly and less neophobically compared to their rural conspecifics, the few studies on reptiles have yielded mixed results. In fact, it is still unclear whether lizards do indeed experience lower predation risk in urban areas. While natural predators might be rare, they are often replaced by dogs, rats or cats (and we all know that cats are the killing machines of nature). We did indeed observe predation on wall lizards in the harbour of Vis, not by a cat, but  by a hooded crow (Corvus cornix). A strong argument can be made that urban habitats are more open, leaving foraging lizards at greater risk of being seen by predators.

More detailed studies of behaviour of urban lizards, together with estimations of resource availability and predation pressure, could help us understand why lizards seemingly adapt different to urban environments compared to mammals or birds.

More detailed interpretation of our results, complete with nice graphs and interesting p-values, can be found in our published paper.

Variation in Cold Tolerance across the Geographic Range of the Green Anole: How Do More Northern Populations Withstand Colder Temperatures?

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On May 10, 2018

In All Posts

From Card et al. 2018

Shane Campbell-Staton and colleagues have just published a paper in Molecular Ecology on the physiological and regulatory basis of variation in cold tolerance across the range of Anolis carolinensis. In the same issue, Daren Card and colleagues have written a very nice, freely available, summary of that article. Here’s the abstract from Card et al.’s review:

How does climate variation limit the range of species and what does it take for species to colonize new regions? In this issue of Molecular Ecology, Campbell-Staton et al. (2018) address these broad questions by investigating cold tolerance adaptation in the green anole lizard (Anolis carolinensis) across a latitudinal transect. By integrating physiological data, gene expression data and acclimation experiments, the authors disentangle the mechanisms underlying cold adaptation. They first establish that cold tolerance adaptation in Anolis lizards follows the predictions of the oxygen- and capacity-limited thermal tolerance hypothesis, which states that organisms are limited by temperature thresholds at which oxygen supply cannot meet demand. They then explore the drivers of cold tolerance at a finer scale, finding evidence that northern populations are adapted to cooler thermal regimes and that both phenotypic plasticity and heritable genetic variation contribute to cold tolerance. The integration of physiological and gene expression data further highlights the varied mechanisms that drive cold tolerance adaptation in Anolis lizards, including both supply-side and demand-side adaptations that improve oxygen economy. Altogether, their work provides new insight into the physiological and genetic mechanisms underlying adaptation to new climatic niches and demonstrates that cold tolerance in northern lizard populations is achieved through the synergy of physiological plasticity and local genetic adaptation for thermal performance.

Do Dead Green Anoles Turn Blue?

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On May 8, 2018

In All Posts

Photo by Dee Simpson

AA reader Dee Simpson reports:

I recently found a deceased Green (Carolina) Anole near my home in central Florida. What struck me is that it was blue. At first, I thought just looked blue because it was desiccated, but on further examining the picture, I realized that one leg was green – if it was just the decaying process, I would expect the whole thing to be the same color/state. I came across the entry on your Anole Annals page regarding blue Carolina Anoles in Florida and was wonder if this could be one of those? Or is it just at a stage of decomposition where the color is weird?

Another Three-Legged Anole…but with a Plot Twist

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On May 6, 2018

In All Posts

Anyone who has spent a considerable amount of time catching anoles in the field has seen their fair share of injured animals. Many species we commonly study (e.g. brown anoles) are just the perfect size to be a snack for any hungry predator (and even humans! see this). Several previous posts have documented adult anoles that have sustained severe injuries (limb loss – see my previous post) and survived. But can these animals thrive with such injuries or do they just limp along through life?

Here I add to this string of anecdotes with a unique datum. This female Puerto Rican crested anole was caught by none other than James Stroud and Chris Thawley at Fairchild Botanical Gardens just this week. She is missing the rear right foot (not an unusual injury). What is new here is that I dissected this female as part of a study conducted by James, Chris, and myself, and I can report that this female, despite her handicap, is not only alive but seems to be thriving. Compared to a cohort of females captured at the same time and place (n= 13), she has greater body condition and fat mass than most of her cohort (Figure 1) and is reproductive at stage 4 (Gorman & Licht 1974). For those unfamiliar, stage 4 means that she has two developing eggs (1 in each oviduct). The mean stage for the cohort is 2.92, and, thus, her reproductive stage is more advanced than the majority of the cohort (only 2 of 13 individuals at stage 4).

Figure 1. Fat mass and residual body condition (log(mass) x log(SVL)) for the entire cohort (gray circles) and the injured female (black circle). There was no relationship between SVL and fat mass for females in this cohort so fat mass is not corrected for body size.

Cox and Calsbeek (2010) demonstrated that gravid anoles have reduced locomotor performance and lower survival than non-reproductive females. However, this female, despite the use of only 3 good limbs, has clearly been able to procure sufficient resources to  fuel reproduction and retain a level of fat reserves above most individuals in her population.  For this reason, we denote her ‘supermom’ and concede the possibility that missing a foot or limb may not severely reduce fitness for some individuals.

Cox, R.M. and Calsbeek, R., 2010. SEVERE COSTS OF REPRODUCTION PERSIST IN ANOLIS LIZARDS DESPITE THE EVOLUTION OF A SINGLE‐EGG CLUTCH. Evolution, 64(5), pp.1321-1330.

Gorman, G.C. and Licht, P., 1974. Seasonality in ovarian cycles among tropical Anolis lizards. Ecology, 55(2), pp.360-369.

 

Replicated Physiological Diversification in Lizard Adaptive Radiation

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On May 4, 2018

In All Posts

Anolis gundlachi prefers to perch in the shade near the ground — according to a new study, these microclimate differences drove some of the later diversification of anoles.
Credit: Manueal Leal, MU Division of Biological Sciences
 Report of a new study from the webpages of ScienceDaily, produced initially by the University of Missouri:

The islands of Puerto Rico, Cuba, Hispaniola, and Jamaica — collectively known as the Greater Antilles — are home to more than 100 species of Anolis lizards. The success of this colorful group of reptiles is often attributed to the evolution of distinct body shapes and behaviors that allow species to occupy different ecological niches. A new study from an international team of biologists including from the University of Missouri reports that the evolution of physiological differences that allow these lizards to take advantage of different microclimates (e.g., sun vs. shade) may have been just as important as these physical differences. The study, which was published recently in The Proceedings of the Royal Society B, has implications for predicting how well these lizards will cope with climate change.

“Why are there so many species of anoles? That’s the big question,” says Manuel Leal, an associate professor of biological sciences at MU and one of the authors of the report. “The notion that morphological differences alone drove the amazing diversity of anoles is missing an important part of the puzzle.”

For scientists, the Greater Antillean anoles represent a classic example of an evolutionary process known as adaptive radiation. After appearing on each of the four islands about 50 million years ago, the colorful lizards quickly diversified to exploit different niches on the island’s trees, including the canopy, trunk near the ground, mid-trunk, and other twigs. Each new species developed its own distinct body type, called an ecomorph, adapted to the niche where it lived. According to Leal, this focus on differences in appearance leaves some important questions unanswered.

“How can similar species coexist without outcompeting one another? One of the tenants of evolutionary ecology is that when a structural niche is filled, species diversification should either slow or come to an end due to competition. There must be some other way they are sharing that habitat to avoid competition,” he said.

The researchers hypothesized that the evolution of physiological traits related to temperature tolerance also facilitated the maintenance of biological diversity by providing an additional axis of co-existence.

Working with Alex Gunderson with the University of California at Berkeley and D. Luke Mahler with the University of Toronto, Leal set out to test this hypothesis. The team caught and collected thermal physiological data on over 300 anoles. Most of the anoles belonged to the Puerto Rican cristatellus group, which includes four pairs of sister species, each of which occupies a different thermal niche. They also included data on Jamaican anoles. The researchers measured two aspects of thermal physiology: maximum thermal tolerance and optimal temperature for sprint performance, which they used as a measure of fitness. They asked if a species heat tolerance correlated with its optimal sprint performance. They expected that sister species would diverge in one or both of these physiological traits.

They found that all Puerto Rican species pairs diverged in at least one of the two physiological traits. In three of the four pairs, the species that preferred the warmer environment had a higher thermal maximum temperature. In two cases, the species that preferred the warmer environment also had had a higher optimal temperature. They found a similar pattern among the Jamaican anoles.

“These findings show that when morphologically similar species co-occur in Puerto Rico and Jamaica, they differ in thermal physiology. We can say that thermal physiological differentiation is important for increasing local species richness,” said Leal.

An additional insight was that thermal physiology evolved slower than morphology. This evolutionary interplay, Leal said, has real-world implications when one considers the rate at which the world’s climate is warming.

“This is not good news for the ability of anoles to adapt to climate change,” said Leal. “The data suggest that the rate at which physiology changes in anoles is not fast enough to cope with how fast temperatures are rising.”

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