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Despite being on opposite sides of the world and separated by millions of years of evolution, Draco and Anolis lizards have converged on many common adaptive solutions.

It has long been suspected that the Draco lizards of Southeast Asia were ecological analogues of the Anolis lizards in the Caribbean. But it has only been recently that we’ve started to truly figure out just how similar these two groups actually are. Especially exciting has been the discovery of how lizards in both groups have converged on remarkably similar adaptations: natural selection appears to repeat itself, time and time again.

The classic textbook scenario in anoles is adaptive convergence in ecomorphology, which reflects where lizards tend to hang out in the environment. This is particularly obvious  in the adaptation of Anolis limb morphology to different types of perches. I’m not sure we can say whether Draco exhibit the same ecomorphs as Caribbean anoles just yet, but Draco do exhibit the same adaptive changes in limb morphology as the anoles of the Caribbean.

Then there’s the obvious case of the dewlap, which has evolved separately in both Anolis and Draco as a key component of their territorial and courtship displays.

Most Anolis and Draco lizards also rely heavily on elaborate sequences of head-bobs in these displays as well.

This in itself isn’t unusual. Many lizards head-bob and push-up over territory and mates. Up to now, however, Caribbean Anolis lizards were the only ones known to tailor their display movements to ensure detection. For any visually communicating animal, visual “noise” from windblown vegetation and poor ambient light make it difficult to see visual signals. Anolis lizards were exceptional because they actively monitored environmental conditions and exaggerated their body movements when it was visually noisy (e.g., on windy days) or extended the duration of their displays when light levels diminished (e.g., on cloudy days or deep inside a forest).

There are a countless ways lizards might produce a conspicuous signal. Many Australian and Chinese lizards add arm-waves or elaborate tail-flicks or simply rely on colourful ornamentation that stands out well in the environment. Many North American lizards rely on performing lots of head-bobs or positioning themselves to accentuate a colourful badge on their throat or sides. But anoles seemed unique in both the complexity of their visual displays and their capacity to modify their behaviour to the prevailing conditions in the environment.

But after years of studying Anolis on Jamaica and Puerto Rico, and then even more years studying Draco in the Philippines, Borneo and Malaysia, we have now discovered more astonishing parallels between the two lizard groups that extends beyond just morphology.

Southeast Asian Draco lizards exhibit virtually identical strategies for coping with visually difficult environments as do the Caribbean Anolis lizards. Draco use the dewlap in the same way as the anoles, and change the speed (or exaggeration of movements) and the duration of displays in the same way as anoles, and this capacity to tailor displays to the conditions of the environment has also tended to precede what seems to have been adaptive divergences in display behaviour among species.

To discover all this, we had to study many different species of Draco and Anolis (11 and 12 species respectively), including hundreds and hundreds of lizards (727 to be precise), and then conduct thousands and thousands of hours of video analysis (13,310 hours – !!).

To be perfectly honest, what I was hoping to document from all this work was how differences in evolutionary history between the Anolis and Draco had shaped the trajectory of display evolution. Sure, Draco had evolved a dewlap like Anolis, but how that dewlap has been morphologically constructed was quite different between the two groups. I had become quite interested in these so-called “many-to-one, form-to-function” outcomes in evolution, and I was aiming to show something similar for display behaviour.

To be clear, there were differences in how Anolis and Draco lizards responded to environmental conditions, and how plastic changes in behaviour have contributed to display differentiation among species. In fact, the head-bob component of the territorial display has been entirely lost in some Draco species.

But the similarities were stunning and outweighed the differences by a large margin. Even the loss of headbobs in some Draco have intriguing similarities to how some Anolis species have shifted their display effort to the dewlap, which seems to be a more energetically efficient means of producing a conspicuous, complex visual display, than the more tiresome head-bob and push-up movements.

We have also confirmed experimentally in anoles that the manner in which Anolis lizards tailor their displays does actually improve display detection in visually difficult environments. This took a lot of work in itself and required the development of a robotic playback system, but this is now ancient history.

But to complete the loop, a similar type of playback experiment needed confirm the same adaptive benefit in Draco.

Some years ago we had conducted a lengthy field experiment using robot playbacks that were designed to test the response of Draco lizards to different coloured dewlaps. That experiment showed little effect of dewlap colour on detection, but a tangible effect that once lizards saw the dewlap, they used it to evaluate the species identity of the signaller.

I was in the lab one day looking at these old Draco robots to get some inspiration for designing a new system for some other crazy idea I had. As I was fiddling with the mechanism, I noticed that the robots weren’t exactly the same, with the lever controlling the dewlap of one being slightly longer than another. This meant the display probably differed in speed between the robots. These things happen and I didn’t think much of it at the time. The treatments used in the field experiment were systematically inter-changed across the robots to make sure this type of thing didn’t cause any problems.

Later, however, it occurred to me that perhaps this might offer a serendipitous opportunity to confirm the adaptive benefit of at least one of the key convergences exhibited by Draco lizards. I downloaded the data from the original study from its dryad repository, extracted the response times of lizards to the two robots that differed in dewlap speed, and sure enough, detection times were much quicker to the robot with the faster dewlap display.

The top panel (a) shows the differences in dewlap speed between the two robots, while the bottom panel (b) shows the detection time of free living Draco melanopogon.

If you’re interested in a short video introduction to this work, or want to know more about how these findings relate to our general understanding of adaptation and animal communication, you’ll find some answers in this 5 minute video below.

Brown anole eggs in the field. Photo by Jenna Pruett.

Most oviparous reptiles (excluding birds) bury their eggs in the ground. Usually, after laying, females abandon the eggs and provide no parental care thereafter. As such, non-avian reptiles (henceforth “reptiles”) have often served as model organisms to understand how the environment influences embryo development. Environmental factors of interest are usually temperature and moisture. Indeed, nest temperature can have large effects on development. For example, warm incubation temperatures often result in hatchlings that can run relatively fast while cool temperatures result in hatchlings that run slow. Moisture is also important during development since relatively wet incubation conditions improve the conversion of yolk to body mass resulting in larger hatchlings compared to dry conditions. This process by which the environment has lasting effects on development is known as developmental plasticity. Despite decades of research concerning developmental plasticity in reptiles, there are still many aspects of natural nest environments that are understudied.

One example of such an understudied environmental factor is the type of substrate (i.e. soil) in which females bury eggs. Although many field studies demonstrate that females lay eggs in a diversity of substrates, very few studies have considered exactly how these different substrates might influence development. These few existing studies have focused on turtles. For example, Mitchell and Janzen (2019) buried turtle eggs in three types of substrates in the field: loam, sand, and gravel. Despite all nests experiencing the same prevailing weather conditions, important aspects of the nest environment like moisture available to eggs and temperature differed among the substrates. This resulted in important differences among the hatchling turtles. Indeed, because this species exhibits temperature-dependent sex determination (i.e. the egg temperature determines if hatchlings are male or female), the sex ratios of the hatchlings differed according to the type of substrate in which the eggs were buried.

No study has rigorously considered how substrate types influence development of squamates (lizards and snakes). Therefore, my research associates and I decided to conduct a lab experiment using our good friend the brown anole (Anolis sagrei). This study was recently published in the journal Integrative Zoology (Hall et al. 2021). At our field site in Florida, female anoles lay eggs in two main types of substrates: sand/crushed sea shells and organic debris (Figure 1). We collected male and female lizards from one of our study islands and brought them back to our lab at Auburn University. We also collected a few buckets of the two substrates in which females commonly nest. We collected eggs from the breeding colony and incubated them in each substrate at 4 different moisture concentrations. The goal was to understand if these two substrates had any important effects on development. Moreover, using different moisture concentrations in each substrate allowed us to see if the two substrates might have similar effects on development given particular moisture concentrations.

Figure 1. Representative photos of (a) a female brown anole (Anolis sagrei), (b) aerial view of the substrate collection island, (c) ground view of substrate collection island, (d) organic substrate, and (e) sand/shell substrate. In panel (b), the area inside the red circle is the portion of the island that is most densely populated with lizards. The area within the black line is an example of open canopy habitat where substrate is primarily sand and crushed shell. The area inside the white line is an example of closed canopy habitat with dark, organic substrate. Panel (c) shows the ground view of the same open and closed canopy sites outlined in panel (b).

We measured a variety of traits including water uptake by eggs (eggs absorb water during development), developmental rates of embryos, egg survival, hatchling body size, and hatchling performance (i.e. endurance). The amount of moisture available to eggs provided expected results: greater moisture content resulted in greater water absorption by eggs and larger hatchling body size. We found that the two substrates had little effect on most traits; however, egg survival and developmental rate differed between the substrates: eggs were more likely to die and developed more slowly in the organic substrate than in the sand/crushed shell. Although statistically significant, these effects were not large. The difference in egg survival was about 6% and the difference in developmental rates between the substrates resulted in a one-day difference in the incubation period (i.e. the number of days it takes for the egg to hatch).

It isn’t completely obvious why we observed these differences in egg survival and physiology (i.e. developmental rate). We think the organic substrate might support a greater load of microbes (i.e. fungal spores and bacteria) than the sand/shell substrate. Thus, in the organic substrate, eggs may compete with microorganisms for resources like oxygen during development. Additionally, when exposed to an abundance of microorganisms, eggs may expend energy to fight infection which could slow development and reduce survival. Regardless, other studies have also found that developmental rate can be influenced by the type of incubation substrate, but no mechanism has yet been rigorously tested. Thus, there is still much to learn about how reptile embryos interact with natural nest environments!

In conclusion, the type of incubation substrate can have important effects on embryo physiology and survival, but only a few studies have explored these relationships. What would be most helpful now is a series of studies that consider how microbial communities differ among substrates and how these communities might interact with eggs. Perhaps this work will rest on the shoulders of Kaitlyn Murphy who is currently using microbiology techniques to understand effects of the microbiome on embryo development using brown anoles. If so, the future of this unexplored area of research is in capable hands.

You can read the full article here: http://doi.org/10.1111/1749-4877.12553

Hall, J. M., Miracle, J., Scruggs, C. D., & Warner, D. A. (2021). Natural nest substrates influence squamate embryo physiology but have little effect on hatchling phenotypes. Integrative Zoology.

Mitchell, T. S., & Janzen, F. J. (2019). Substrate influences turtle nest temperature, incubation period, and offspring sex ratio in the field. Herpetologica, 75(1), 57-62.

A male A. distichus favillarum (a.k.a. a male Fav) extending it’s dewlap. This animal was photographed in the contact zone between orange- and yellow-dewlapped Favs.

Color and color-pattern research is a powerhouse in the study of evolution. Don’t believe me? I bet that at least one of your top five examples of evolution includes either color or color pattern. It is also very likely that some of the gene names you know by heart are from either color or color-pattern genes. Here’s an exercise: think which were the ‘textbook’ examples of evolution that you were taught in school. I’m sure that at least one of those included either color or color pattern. Here’s a famous example: Peppered moths. Another one? Deer mice. Another one? Heliconius butterflies. Another one? Coral snakes. What about color genes? Does MC1R ring a bell? Another one? ASIP (a.k.a. agouti)? Another one? Well, I should stop here before DJ Khaled sues me for copyright infringement.

Most of these early studies, however – and specially studies that attempted to unveil the genetic basis of color and color pattern – focused on melanin-based traits. The reason for this bias was simple: human color is melanin-based. This means that when these early studies took place, we knew more about the genetic basis of melanin synthesis than any other pigment by a long shot. As a consequence, melanin-based traits were ideal for candidate gene approaches – like the ones implemented in early color and color-pattern studies. As you and I know, though, the world isn’t black and white (see what I did here?). Color is all around us, and it plays all kinds of amazing roles, such as intra-specific communication (think dewlapping anoles), inter-specific communication (think dewlapping anoles), and crypsis (think non-dewlapping anoles). This means that, until recently, we didn’t have the tools to connect the genetic basis of most colorful traits to their phenotypes, specially in non-model organsisms.

Then, something happened: second generation sequencing came around. Illumina, a key player in second generation sequencing, was founded in 1998, the same year that Brazil lost the World Cup Final to France (many Brazilians, like me, think about time in four-year cycles due to the World Cup… and we don’t talk about 2014). With second generation sequencing, we could finally gather loads of data to do all kinds of glorified regressions (sorry generalized linear mixed models), and run computers for very long times so that we could try every feasible parameter combination (sorry Markov Chains) to identify candidate genes for the trait we are interested in. Connecting genotypes to phenotypes and understanding how both genotypes and phenotypes interact and change due to selection is, in fact, one of my main research interests.

I’m particularly interested in understanding the genetic basis of two phenotypes: those associated with color and color pattern, and those associated with the evolution of reproductive isolation.

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Photo by Lindsey Swierk

Although most people use “personality” to describe human characteristics, animals also exhibit personality traits, which behavioral ecologists categorize as aggressiveness, exploration, activity, sociability, and boldness. Each personality trait is linked to inherent trade-offs that could affect one’s overall fitness, and may differ between the sexes due to different life history strategies. Boldness is a personality trait that includes behaviors such as risk-taking, response to predators, and resistance to being handled. It is assumed that bolder individuals are more likely to “take chances” and forage under predation risk compared to less bold individuals, whereas less bold individuals may spend more time scanning for predators and less time foraging.

Austin Carriere (The University of Oklahoma), Dr. Lindsey Swierk (Binghamton University – SUNY), Dr. Bree Putman (California State University San Bernardino) and I investigated the sex differences in the trade-offs between boldness and predator avoidance in water anoles (Anolis aquaticus), using the voluntary shedding of the tail (tail autotomy) as a proxy for predation risk. This project involved a two-year mark-recapture study, morphological data collection, and behavioral trials. We conducted and recorded boldness trials in the field for all captured adult anoles, and we analyzed the video footage in the lab. We quantified boldness as the latency for a lizard’s head to emerge from a refuge into a novel environment.

Fig 1. Adjusted survival curves showing how tail break (yes or no) affected time to head estimated from the Cox proportional hazard model in a) female and b) male water anoles. Survival rate is the proportion of individuals still in the refuge.

We found that there were sex-differences in the costs of boldness, as tail autotomy was positively associated with boldness in males but not in females. Tail autotomy has been shown to have serious fitness consequences in lizards; therefore males likely suffer a higher cost of boldness. We also found that males tended to be more likely to show evidence of tail autotomy. Our results could be due to the fact that lizards exhibit a polygynous mating system, wherein males defend territories to acquire mates, and so males may exhibit bolder behavior to increase their reproductive success. However, the trade-off of boldness in males is the higher probability of tail autotomy, probably due to increased exposure to predators or more involvement in aggressive encounters with conspecifics. Our study contributes to the understanding of sex differences in behavior within an ecological context.

Source: Talavera, J.B., Carriere, A., Swierk, L., Putman B.J. Tail autotomy is associated with boldness in male but not female water anoles.  Behav Ecol Sociobiol 75, 44 (2021). https://doi.org/10.1007/s00265-021-02982-w