Category Archives: New Research

Evolution 2017: Thermoregulation Simultaneously Impedes and Impels Evolution

Major Anole Annals contributor Martha Muñoz gave a brilliant talk at the Evolution meeting  as an awardee of a well-deserved ‘Young Investigator’ award from the American Society of Naturalists. In her talk, Muñoz discussed how two classic papers by Janzen (1967) and Huey et al. (2003) influenced the way she thinks about the interplay between behavior, physiology, and evolution. Not surprisingly, Anolis lizards played a leading role in her exposition.

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Martha Muñoz introduces the Cybotoid Anoles.

Martha’s talk, entitled “Janzen’s hypothesis meets the Bogert effect: a synthesis nearly 100 years in the making”, started by describing Janzen’s hypothesis. In short, Janzen (1967) predicted that physiological differences among populations across altitudinal bands would be stronger in tropical mountains than in temperate ones. The main argument was that populations can more easily adapt to a given temperature range in tropical environments because these ranges are stable throughout the year, whereas the temperatures of different altitudinal bands overlap more in temperate areas due to seasonal variation.

Martha explains how daytime and nighttime temperatures in the tropics mirror seasonal patterns in temperate and tropical climates.

Martha explains how day and night temperatures in the tropics mirror seasonal patterns in temperate and tropical climates.

Expanding on Janzen’s idea, Muñoz hypothesized that diurnal and nocturnal temperature variation in a single tropical mountain could also generate differences in physiological divergence among lowland and highland populations. The idea was that daytime temperatures were variable with overlap across elevation (similar to the seasonal picture in temperate areas) and nighttime temperatures were more constant and differed between elevations (similar to the seasonal picture in tropical areas).

To test this, Martha sampled populations in the Dominican Republic at sites ranging in elevation from sea level to 2400m. She then analyzed heat and cold tolerance of several species of anoles from the Anolis cybotes group. Results on cold tolerance (CT min) seem to agree with Janzen’s hypothesis: cold tolerance strongly covaries with altitude at night, with higher elevation populations having lower critical thermal minimums. Interestingly, however, heat tolerance (measured as CT max) was not at all associated with elevation.

Why did Janzen’s hypothesis fail to explain the evolution of heat tolerance across the altitudinal range? This question led to a key point of Muñoz’s talk: Janzen’s hypothesis might fail to predict evolution of CT max because it is agnostic about behavior. In the case of ‘cybotoid’ anoles, lizards from different altitudes could actively adjust their habitat use to achieve optimal temperatures. As a consequence, thermoregulatory behavior could forestall evolution of physiology in heat tolerance. By studying habitat use across different elevations, Muñoz showed that, although anoles behave as thermo-conformers at low elevations, they clearly thermoregulate at high elevations. In other words, anoles were at similar temperatures to the average available substrates in lowlands but their body temperatures were significantly higher than perches at higher elevation.

Martha explains how the thermoregulation can lead to slower evolution in a trait (the Bogert effect)

Martha explains how the thermoregulation can lead to slower evolution in a trait (the Bogert effect)

This was at least partially explained by habitat use differences: anoles at high elevations perched most frequently on boulders, which are on average about 5º C warmer than trees –the most used substrate in low altitudes. In fact, 90% of the trees Martha sampled at these high elevation sites were lower in temperature than the preferred temperature of the lizards! These data indicate that anoles from the A. cybotes group have buffered natural selection in physiology by means of behavioral adjustments –a phenomenon known as the Bogert effect (also called behavioral inertia; Bogert 1949).

Finally, the talk had a third part. And yes, it got even more interesting! Due to the observed habitat use differences in high latitudes, Muñoz and her collaborators predicted that although behavior could buffer physiological evolution on heat tolerance, it could spur evolutionary change in ecologically-relevant morphological traits (the behavioral drive hypothesis). Specifically, they predicted that increased use of boulders (for thermoregulation) at high elevations should drive morphological shifts in traits related to boulder use: head and limb morphology. They found evidence for these hypothesized morphological differences: high elevation lizards had higher head heights and longer hindlimb,  in agreement with functional predictions. Finally, a captive breeding experiment confirmed that these differences were the consequence of genetic changes and not simply due to developmental plasticity.

Martha’s research is a great example of how, as Huey said, studying behavior can be crucial to improve our understanding of evolutionary processes. We are looking forward to hear about future research from the Muñoz lab, which is about to open at Virginia Tech!


Janzen, D.H. 1967. Why mountain passes are higher in the tropics. American Naturalist 101:233–249

Huey, R.B., Hertz, P.E., Sinervo, B. 2003. Behavioral drive versus behavioral inertia in evolution: a null model approach. American Naturalist 161: 357–366.

Muñoz, M.M. et al. 2014b. Evolutionary stasis and lability in thermal physiology in a group of tropical lizards. Proc. R. Soc. B 281: 20132433.

Muñoz, M.M., Losos, J.B. Thermoregulation simultaneously promotes and forestalls evolution in a tropical lizard. (Accepted pending minor revision). American Naturalist.

Evolution 2017: Spatial Structuring of Urban Green Anoles

In his Masters thesis conducted in Simon Lailvaux’s lab at the University of New Orleans and presented this week at Evolution 2017, David Weber used a multiyear data set of Anolis carolinensis lizards’ locations and morphology as well as a DNA-based pedigree to investigate the effects of body size and relatedness on the spatial distribution of these lizards. Specifically, he set out to test three hypotheses: first, are males’ home ranges larger than females’ home ranges? Second, are bigger males more likely to be surrounded by smaller males that are related to them? And third, is there any evidence for the inheritance of home ranges from parent to offspring?

Anolis carolinensis dewlapping. Photo by Cowenby available on Wikipedia.

Anolis carolinensis dewlapping. Photo by Cowenby available on Wikipedia.

Lizard locations were sampled in an urban New Orleans park twice a year, in the fall and in the spring, from 2010 to 2015. The dataset included over 800 individuals, and what struck me most about these data was that, of these 800+ individuals, fewer than 100 were observed often enough to estimate home range volumes–death and dispersal can rule these lizards’ lives! Male and female home range volumes did not differ significantly (and the trend was in the direction of females moving over larger areas, which concurs with data from Robert Gordon’s 1956 thesis on green anoles, but with little else, I think). Curiously, smaller neighbours of the biggest males were less related to them than were males found farther away, suggesting that male anoles don’t preferentially tolerate their kin over non-kin. And though philopatry  (aka site fidelity aka staying the same place) was rare overall, females were a bit more likely to co-occur with their male offspring than males were. In a result that conforms to traditional wisdom, Weber found that the biggest males in the site seemed to avoid each other, potentially spacing themselves as far apart as possible.

Following a kind shout-out to my and Jonathan Losos’ recent paper on Anolis territoriality or the lack thereof, Weber chose to interpret his results as making sense only outside of a territorial framework. Unsurprisingly, I concur with this decision entirely, and am excited to see where Weber goes with this idea in the publications resulting from this mammoth dataset!

Evolution 2017: Integrating Ecological, Antagonistic and Reproductive Character Displacement


The arrival of an outsider that overlaps in resource use and habitat with local species can lead to intense competition between the two. A result of this competition can be character displacement, where traits of the species (one or both) change in sympatric populations (where the co-occur), but not in allopatric populations. Claire Dufour (Post-Doctoral researcher at Harvard University) presented her work on character displacement for two anole species on the island of  Dominica: the native Anolis oculatus and the introduced Anolis cristatellus. Her objective was to integrate ecological, antagonistic and reproductive character displacement. Specifically, she tested whether competition  between these new island-mates leads to changes in habitat use, morphology, and display behavior.


Location of populations of the introduced A. cristatellus with the sampled area, Calibishie inset

Claire compared allopatric populations of the two species with sympatric populations in the northern area of the island in Calibishie, where Anolis cristatellus has been present for two years. She found that in sympatry, both morphological and behavioral shifts have occurred. In sympatry, Anolis oculatus perched higher and had shorter limbs. She also found differences in display behavior, which she tested with an anole robot programmed to dewlap and do push-ups. This experiment showed that in sympatry, Anolis cristatellus dewlapped less, but Anolis oculatus does not alter its display behavior. Future work will test for reproductive character displacement and contrast populations where Anolis cristatellus has been present for a longer time span.

Evolution 2017: Sensory Drive and Lizard Adaptive Radiation


The Sensory Drive hypothesis predicts that species will evolve communication signals that are effective in the particular light environment in which they occur. Anolis lizards are an excellent example: in dark habitats, they tend to have light-colored, highly reflective (and transmissive) dewlaps that are usually yellow or white in color, whereas in bright, open environs, dewlaps tend toward blue, black, orange or red. However, demonstrating that these dewlaps are actually effective at being visible in their particular habitats has proven surprisingly challenging.

Leo Fleishman has been a leader in this area and in a talk at the sensory ecology symposium at the evolution meetings, he presented new and exciting developments. First, in line with previous work, he showed that the spectral reflectance/transmittance of dewlaps is not particularly well-matched to that of the background. Rather, the same colored dewlaps appear to be maximally contrasting with the radiance of the background across all habitats:  basically all habitats have mostly green backgrounds, and red or orange stands out the best against the green background, no matter what the habitat.  So much for sensory drive, it would seem!

But more recent work saves the day: it turns out that habitats differ in the total intensity of light (number of photons coming down) they receive and that, furthermore, across species, dewlap intensity (total photons reflected and/or transmitted) is negatively related to habitat intensity (with one notable outlier, the enigmatic A. gundlachi). Under the relatively low light conditions of forest shade or partial shade, color discrimination becomes more difficult, and colors such as red and orange and other dark colors do not stand out well against the background, because they simply do not emit enough photons to efficiently drive color vision.  Yellow or white works better. Conversely, in intense light environments, there is enough light to easily see the darker colors, and these stand out well against the green background. Moreover, behavioral experiments confirm that in bright light conditions red stimuli are most visible against a green background, whereas in low light yellow stimuli are more visible.  Thus, even though most Anolis habitats have similar spectral properties, differences in total light intensity strongly influence what colors are most effective, and thus appear to have played a major role in the shaping the evolution of dewlap colors.

Leo Fleishman discusses color space in 4-dimensions, corresponding to the four cones in the anole eye. For each species, red dots are color of the dewlap and green dots are the color of the background, indicating that dewlaps stand out against their background.

Leo Fleishman discusses color space in four dimensions, corresponding to the four cones in the anole eye. For each species, red dots are color of the dewlap and green dots are the color of the background, indicating that dewlaps stand out against their background.

Evolution 2017: Introduced Miami Anoles Exhibit Character Displacement

Bright and early on the last day of the annual Evolution meeting, James Stroud (Florida International University) presented his work on character displacement in novel communities of introduced anoles in Miami. In this elegant use of a natural experiment, James looked at the novel co-existence of two anoles in their introduced range and wondered if character displacement was occurring as predicted when two ecologically similar species are found in sympatry. Specifically, James wanted to know if Anolis cristatellus and Anolis sagrei would shift their habitat use when in sympatry, resulting in correlated shifts in morphology. These species are both trunk-ground anoles of roughly the same body size. They are native to Cuba/Bahamas and Puerto Rico (respectively) and are diverged by ~50 million years.

James hypothesized that in their introduced range in Florida, these two species would diverge ecologically in sympatry but be more similar in allopatry. He found that in allopatry, both species attained similar relative abundances and perched at similar heights. However, in sympatry, both decline in relative abundance suggesting that these species are interacting strongly with one another. Even more interesting, in sympatry A. sagrei perches lower and spends more time on the ground than it does in allopatry, while A. cristatellus perches higher!

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Next James hypothesized that these ecological shifts could lead to shifts in morphology. If A. sagrei is spending more time on the ground, perhaps longer limbs would be favored. Similarly, if A. cristatellus is spending more time higher up in the trees, perhaps there would be selection for stickier toepads. As predicted, A. sagrei had longer forelimbs and hindlimbs in sympatry. However, he did not find any difference in toepad morphology between sympatric and allopatric populations of A. cristatellus. Instead, he observed that A. cristatellus in sympatry with A. sagrei had significantly smaller heads.

James ended by wondering if alternative behavioral and social mechanisms may drive these observed shifts in head morphology. Either way, this case study provides an interesting insight into how a complex range of adaptive responses can result from a seemingly simple ecological interaction.

Evolution 2017: Experimentally Testing Perch Choice in Urban and Forest Lizards

Cities and urban areas are expanding rapidly around the world, altering the environment and creating very different ecological and selective pressures for organisms that live in urban habitats. A few of the most striking differences between urban and natural habitats are higher temperatures and a huge increase in artificial substrates like the walls of buildings. These artificial substrates (e.g., metal, concrete) are not only significantly smoother than natural (i.e., trees) substrates, but also absorb, retain, and radiate heat differently. Consequently, organisms may alter their behavior to better deal with these and other challenges of city life. Since anoles cannot internally regulate their temperature, behavioral shifts may be driven by perch substrate properties, temperature, or some interaction of the two.


Kevin Aviles-Rodriguez (U. Mass. Boston) addressed this question in urban Anolis cristatellus in San Juan, Puerto Rico. He created experimental enclosures in which each wall was a different substrate: wood, plastic, painted cement, and metal. He placed individual lizards into the enclosures and observed which wall they were perched on throughout the day. He also recorded the temperature of each wall, to determine how perch temperature of each substrate type influenced perch choice. Aviles-Rodriguez conducted this experiment in both urban and forest populations, and predicted that urban lizards would use artificial substrates more readily than forest lizards.

Interestingly, he did not find that to be the case – lizards from both urban and forest habitats used bark much more than any other surface. However, when lizards did use artificial substrates, they tended to use metal and cement when these perches were cooler, suggesting that perch temperature is a factor in perch choice. Aviles-Rodriguez plans to test these hypotheses more thoroughly by conducting additional experiments across more urban replicates to see if the same pattern emerges. He also plans to experimentally control the temperatures of different perch substrates in his enclosures to see whether lizard choices are primarily driven by perch substrate or temperature.

Evolution 2017: What Jumping Genes Can Tell Us about Anole Genome Evolution

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I find Transposable Elements (TEs) to be some of the most fascinating features of genomes. Also known as selfish genetic elements, these sequences contain the genetic machinery to create copies of themselves and insert these new copies in locations throughout the genome. The genomes of different organisms vary widely in their degree TE abundance. For example, 20% of the human genome is composed of just one kind of TE!

This morning Robert Ruggiero, a Postdoctoral Fellow in the lab of Stephane Boissinot at NYU Abu Dhabi, presented his work on the population genomics of TEs in the genomes of Anolis carolinensis populations. Robert employed a clever approach that uses a feature of next-generation sequence data to identify TE insertions. In this way, he can characterize all of the TE insertions in an individual’s genome and determine what portion of a population contains any particular insertion.

It’s easy to see how Transposable Elements could be bad for an organism. If a TE inserts itself into the middle of an important gene, the function of that gene could be interrupted, and render the bearer of that insertion less evolutionarily fit. The ability of natural selection to purge this type of deleterious insertion is governed in part by the effective population size of the group where that insertion arises. In essence, natural selection is more effective in larger populations.

Using the information he collected on TE insertions in anole populations, Ruggiero created a population genetic summary called an Allele Frequency Spectrum, the count of insertions that exist at a particular frequency in a population. This distribution can then be used to infer how well populations control the frequency of TE insertions, and in addition, estimate the effective size of those populations. Robert found TE insertions in Floridian populations of Anolis carolinensis were maintained at lower frequencies than other populations suggesting that selection is better able to purge deleterious insertions in the Florida population. He also found that different families of TEs appear to employ strategies that mirror ecological r/K theory. Some TEs create insertions frequently but few of these insertions get to high frequency, whereas other TEs insert infrequently, but those insertions that do occur are more likely to reach high frequency. Moving forward, using this line of inquiry in anoles will be an excellent opportunity to understand the control and evolutionary consequences of TEs, particularly as more Anolis genomes come online allowing comparative analyses.

Evolution 2017: Genetics of Ecologically Divergent Anoles

Anolis distichus is well-known in the anole world for the high degree of ecomorphological variation within the species, especially in dewlap color. In fact, there are 18 described subspecies! While there is some gene flow between various subspecies and populations, the phenotypic differences are maintained, which suggests strong selection. But the fine-scale genetic structure underlying these traits is not well understood. Anthony Geneva and colleagues decided to explore the genomic basis of adaptive divergence in a well-described hybrid zone between two A. distichus subspecies. The first, A. d. ignigularus, has a white dewlap, and occupies a dry forest habitat while the second, A. d. ravitergum, has a red dewlap and inhabits a wetter habitat. The two subspecies occur along a transect from dry to wet, and they hybridize in a narrow contact zone in the middle. These two subspecies provide a great system to explore the link between adaptive and genetic divergence.


Anolis distichus. Photo by Rich Glor

Geneva sequenced individuals using RNASeq across an environmental transect from wet to dry, including allopatric and sympatric populations of both species. He examined levels of divergence and introgression to explore which genomic loci might be the basis for the ecological adaptive divergence between these two species. He found a suite of candidate genes that differ between the two subspecies, as well as several that show signs of introgression between the two. Interestingly, several of the divergent genes are involved in two traits that likely are impacted the environment – insulin signaling, which may relate to metabolic differences between hot and cool climates, and vision, which may relate to differences in light availability and signal efficiency. Most of the introgressed genes, on the other hand, relate to conserved pathways, suggesting that these genes play similar roles in both subspecies.

Adpative divergence in anoles has been a topic of interest for a long time, and Geneva’s study provides and a valuable insight to the genetic basis of this interesting phenomenon.

Evolution 2017: Does Molecular Convergence Underly Ecomorph Convergence?

2017-06-25 16.15.01On each of the Greater Antillean islands, habitat-specialist Anolis ecomorphs have independently evolved complex suites of shared phenotypes and behaviors. This remarkable convergence has motivated the work of generations of anolologists. With anoles entering the once-exclusive club of genome-enabled organisms, a new line of investigation has become possible: Is the convergence observed in anole ecomorphs caused by molecular convergence? Such convergence can take many forms, including shared changed at individuals sites, or shared changes in the rates of protein evolution of individual genes.

Russ Corbett-Detig of UCSC sought to answer this question using whole-genome sequence data from 12 species – four from each of the Trunk-Ground, Trunk-Crown, and Grass-Bush ecomorphs drawn from different islands and different evolutionary lineages. Accurately detecting molecular convergence is fraught and much recent research has focused on avoiding pitfalls that could lead to a positively misleading inference of convergence where none actually exists. Previous studies have trumpeted amazing cases of molecular convergence in a variety of animals, only to be later shown to be artifacts of data analysis.

Corbett-Detig did everything right. He used null models that account for the expected background levels of convergence caused by processes other than natural selection. He found no evidence of extra shared non-synonymous mutations in any of the three ecomorph groups. Similarly, he found no signal of shared changed in protein evolution in Trunk-Ground or Trunk-Crown but Grass-Bush anoles seemed to share elevated rates of changes in many genes. This result was exciting, but Corbett-Detig dug deeper and discovered a new way this type of analysis could be mislead – two of the four Grass-Bush anoles exhibited accelerated evolution across their entire genomes and, as a result, seemed to share faster rates at more genes than expected by chance. When Corbett-Detig corrected for this bias, the signal of convergence disappeared.

While this result was in one sense disappointing, it is also fascinating and suggests the evolutionary pathways to shared ecomorphological traits are numerous and strongly influenced by contingency. Furthermore, anole ecomorphs have evolved such a stunning set of similarities that other forms of convergence like genome structure, gene family expansion, or convergence in gene regulation may still hold the key to understanding the genetic basis the remarkable convergence of Anolis ecomorph classes.

Evolution 2017: Sexually Antagonistic Selection in Juvenile and Adult Anoles

Sexually antagonistic selection occurs when traits are beneficial for one sex, but detrimental to the other. This commonly occurs in species with sexual dimorphism, such that one trait is positively correlated with fitness in one sex, and negatively correlated with fitness in another. But in many organisms, the sexes do not become dimorphic until maturity – that is to say, juveniles all look pretty much alike, even when adults show clear differences between males and females. Which leads to the question: how does sexually antagonistic selection change over an organisms’ lifespan? Research from studies of Drosophila flies suggests that this is the case, but the question hasn’t been well-studied in vertebrates.

Everyone's favorite anole, Anolis sagrei

Everyone’s favorite anole, Anolis sagrei

Until now. In his Evolution talk, Aaron Reedy (University of Virginia) described his work testing whether sexually antagonistic selection changes over ontogeny using our favorite workhorse of evolutionary ecology, the brown anole (A. sagrei). Anolis sagrei are sexually dimorphic, with adult male body sizes up to 30% larger than females, but juveniles are monomorphic. Reedy and colleagues  sampled A. sagrei on several small islands in a Florida watershed four times a year, capturing thousands of adults and juveniles. They measured the body size of all lizards captured, and combined this morphological data with survivorship data to determine how selection was acting on body size in adults and juveniles.

They predicted that juvenile males and females would experience concordant selection, while adult males and females would experience antagonistic selection. And this is exactly what they found: for juveniles, body size was correlated with survival in the same way between sexes. But in adults, this was not the case. In the first year of sampling, there was no selection on body size for adult females, but positive selection for males, such that bigger males survived better. Interestingly, during the second year of sampling, the relationship flipped – females experienced positive selection on body size, and males experienced negative selection. The reasons for this shift are uncertain, but the main point is clear – sexually antagonistic selection does indeed change over ontogeny. Reedy et al. are planning to follow up this great new research by expanding their study to look at more islands and more traits to get at the finer points of these selective differences, so stay tuned!

Evolution 2017: It Doesn’t Pay to Be Risky When Predators Are About


Oriol Lapiedra opened up the penultimate day of Evolution by discussing his results of a recent field experiment in the Bahamas. In this project, Lapiedra and colleagues evaluated how inter-individual variation in behavior – specifically risk-taking – influenced survival. To do this, the research team took advantage of a well-understood model system in evolutionary ecology: brown anoles (Anolis sagrei) on islands with and without anole-predators (curly-tailed lizards; Leiocephalus carinatus) in the Bahamas. Male and female brown anoles were collected and subjected to a behavioural trial which measured the amount of time it took for a lizard to leave a refuge after being exposed to a predator. These observations were used to quantify each individual’s propensity to take risks. For example, those individuals that left their refuge shortly after seeing a predator were interpreted as being more ‘risky’ than more conservative individuals. Following these trials, each lizard was x-rayed to assess morphology and individually tagged, before being released onto one of 4 predator-free islands or 4 predator-present islands, all of which were currently void of anoles.

Lapiedra et al. started with a priori hypotheses that overall survival would be lower on those islands with predators, and those that did survive would be individuals considered less risky. After waiting 4 months, the research team returned to the Bahamas to collect all lizards from each island and see which individuals had survived. The authors report that, as expected, overall survival was lower on islands with predators, and that there was a significant relationship between behaviour and survival such that high risk-taking individuals had much lower survival when predators were present. This suggests that under those biotic conditions, natural selection operates against those riskier phenotypes. On closer inspection, this relationship was largely driven by a strong relationship in females, with no significant relationship existing between risk-taking behavior and survival of males.

Lapiedra et al. then contrasted these results by independently assessing how morphology was related to survival. The authors found that both risk-taking behavior and morphology influenced survival, however – and, important to this study – the relative effect of an individual’s risk-taking behaviour was much more influential on survival.

Evolution 2017: Urban Lizards Are Larger but Show No Consistent Trend in Dewlap Area or Injury Rate


At last night’s poster session, undergraduate Derek Briggs (U. Mass. Boston) presented findings from his senior capstone project in which he looked at several traits related to dominance and health. Using a dataset of x-rays and dewlap photos collected over a 4 year period from various urban and forest sites across Puerto Rico (by Kristin Winchell), Derek looked at body size, body condition, dewlap size, and injury rates (broken bones and missing digits) to see if there was a difference in frequency between urban and forest habitats.

Derek and his co-authors chose these traits because they thought they might be impacted by shifts in lizard density and distribution in the urban habitat which may lead to increased male-male competition. Specifically, in urban habitats, lizards tend to perch closer to one another because the potential perches are more clustered. This increase in local density could lead to increased encounter rates and fights over optimal perch sites, food resources, or mates. Derek hypothesized that this shift in distribution should lead to shifts in these traits, although he did not have a prediction about the direction of these shifts.

Derek Briggs with his poster.

Derek found that urban lizards were consistently larger than forest lizards in terms of snout-vent-length (SVL) but that body condition (mass~SVL) did not consistently differ between sites. Although all paired populations had significant differences in body condition, in some municipalities lizards were fatter in urban habitats and in some they were fatter in forests. In terms of dewlap size, Derek did not find any significant trends, although he still has quite a few dewlap photos to analyze still, so stay tuned!

In terms of injuries, Derek did not find significant differences between forest and urban animals for bone breaks or missing digits. However, these are rare events to begin with, so it is possible that a much larger sample size is needed to detect a difference. His findings do suggest a trend of more bone breaks in urban populations, and more missing digits in forest populations. He attributes this trend to either elevated male-male competition in urban habitats or differences in predator communities.

We look forward to seeing the full results from Derek’s honors thesis.

Evolution 2017: Urban Anoles Sprint Faster on Smooth Substrates

Kristin Winchell gives her talk on urban anoles at Evolution 2017.

Kristin Winchell gives her talk on urban anoles at Evolution 2017.

When I think of Puerto Rico, the first thoughts that come to mind are of sunny beaches and lush rainforests. There are, however, also lots of urban habitats in Puerto Rico. San Juan, for example, has two million human residents, and also lots and lots of anoles. Doctoral candidate Kristin Winchell has been studying adaptation in urban anoles for several years. Last year, she published1 her work showing that Anolis cristatellus in urban habitats have longer hindlimbs, bigger toe pads, and more lamellae than lizards in rural habitats.

A connection that was missing, however, was how the morphological shifts she documented related to performance differences in urban versus rural habitats. To get at this question, she conducted sprinting trials with different substrates to see how limb and toe characteristics affect sprinting capacity. Lizards in urban habitats use much smoother perches, such as fences and posts, and so the hypothesis was that the longer limbs and toe pad differences she detected improved sprinting performance on smoother substrates. She used three different substrates for sprinting trials – bark (rough surface), metal (smooth surface), and painted concrete (very smooth surface). She found that, overall, lizards sprinted more slowly on more slippery substrates. On average, lizards sprinted at 60% of their maximum capacity, indicating a strong performance hit when using slippery substrates.

Kristin confirmed that the urban anoles were better at sprinting on all substrates – including the slippery ones – than rural anoles. When she explored the results in greater detail, she found that only lamella number explained variation in sprint performance, with no appreciable effects of limb length or toe pad area. Kristin’s elegant study demonstrate how we can document evolution on recent timescales, and shows how urban environments provide strong selective pressures for the animals that live in them.

1. KM Winchell, RG Reynolds, SR Prado‐Irwin, AR Puente‐Rolón, LJ Revell. 2016. Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus. Evolution 70:1009-1022

Evolution 2017: Genetic Constraints in the Anolis Adaptive Radiation

As a lineage splits and diversifies, species’ traits diverge in different ways.  For example, as anoles diversified in the Caribbean, trunk-ground anoles’ bodies become muscular and stocky, trunk-crown anoles’ heads become long and thin, and grass anoles’ tails become long and slender. This process of adaptation to different environments seems simple and intuitive, but the evolution of traits is not so simple.

Most traits don’t evolve independently – changes in one trait are often correlated with changes in another trait, which can constrain a species’ response to selection. This correlation between traits is represented by the genetic variance-covariance matrix (G matrix). The size, shape, and orientation of the G matrix determine the speed and direction of morphological change, and defines the “line of least genetic resistance” along which a species can evolve. But of course, as species diverge and their traits shift, the correlations between these traits themselves may not stay constant – that is to say, the G-matrix itself can evolve. Which means that G represents both a constraint on evolutionary change, as well as a product of evolution itself. So does the G matrix evolve along with species divergence, or does it limit morphological evolution?


In his talk at Evolution 2017, Joel McGlothlin (Virginia Tech) described his efforts to address these question in anoles. As a poster child of adaptive radiation, Anolis provides an excellent opportunity to explore the dynamics of G matrix evolution and evolutionary constraint. To that end, McGlothlin and colleagues estimated G matrices for seven anole species (no easy task), including representatives from three ecomorph categories. He laid out the following question: has the G matrix evolved as Anolis diversified? Or do we see a signature of constraint conserved across anoles?

First, McGlothlin and colleagues found that the G matrix has indeed evolved in the course of Anolis diversification: the shape, orientation, and size of the G matrix was different for each species studied. More closely related species had more similar G matrices, and there was a weak link between ecomorph and G matrix structure, but overall, G was clearly different across the seven anole species. This suggests that trait correlations (and therefore species’ potential responses to selection) are not necessarily constant across the anole radation.

However, despite this overall divergence, one important aspect of the G matrix – its orientation – was similar across all anole species sampled. This suggests that the line of least genetic resistance has remained constant throughout the diversification of anole ecomorphs, and is deeply conserved. So even though individual species’ trait correlations have changed as anoles have diverged, the signature of morphological constraint has persisted. The study provides a fascinating illustration of the complexity of morphological evolution, and provides a fresh new link between micro- and macro- evolutionary processes in Anolis lizards.

Evolution 2017: Speciation and the Anolis Dewlap

When, why, and how does speciation take place? Travis Ingram, professor at the University of Otago in New Zealand, tackled this question in his talk at Evolution 2017 (and in this paper) by examining Anolis speciation in the context of anoles’ most enigmatic trait–the dewlap.

Anolis sagrei with its dewlap extended. Photo by Bonnie Kircher.

Anolis sagrei with its dewlap extended. Photo by Bonnie Kircher.

Ingram posited that we can think of relationships between speciation rates and the value of particular traits in two ways. One possibility is that the value of a particular trait in a lineage influences the probability that that lineage speciates, trait evolution facilitating speciation. Conversely, particular traits may be especially likely to diversify at speciation events, in response to speciation.  Ingram tested these two hypotheses in Anolis, crowd-sourcing photographs of outstretched anole dewlaps  to quantify dewlap size and ending up with analyze-able dewlap size information for 184 species from across the whole clade.

Ingram detected no relationship between speciation rates and dewlap size,  indicating no evidence for dewlap-size-dependent speciation in anoles (possibility 1 above). However, probing a bit further, Ingram considered why bigger dewlaps may be related to speciation rates–what if a bigger dewlap allows for greater pattern complexity, allowing more species to coexist by accessing more axes along which their dewlaps can diverge? Quantifying dewlap complexity as the number of colours on a dewlap, Ingram did find a relationship between size and complexity, but curiously, more complex dewlaps were linked to lower, and not higher, speciation rates. Why remains a mystery. Suggesting evidence for speciational evolution (possibility 2 above), 34% of dewlap size evolution was associated with speciation events. Intriguingly, this pattern was driven almost entirely by mainland and not island anoles.

In sum, though the precise processes linking speciation and dewlap evolution remain rather enigmatic, it seems to me that Ingram’s macroevolutionary approach has given us a number of directions in which to take microevolutionary and behavioral ecological studies to understand why dewlaps vary in the ways that they do!

Evolution 2017: Sexual Dimorphism in Anolis sagrei

Sexual dimorphism, or phenotypic differences between the sexes, is characteristic of nearly all animal species. Males and females often differ in size, shape, color, and many other morphological and behavioral phenotypes. This dimorphism can often make it difficult to study selection on various phenotypic traits – how do you measure selection on a trait accurately when that trait may be expressed differently in each sex?

Anolis sagrei exhibits sexual dimorphism. (Photo by Bob Reed)

In a talk at the annual Evolution meeting, Robert Cox and Joel McGlothlin help us answer this question. Using dewlap and skeletal measurements – which differ widely between males and females – and data from breeding experiments on Anolis sagrei, they examine the quantitative genetic architecture of these sexually dimorphic traits. Using a matrix-based model, which accounts for genetic correlations between and within sexes, Cox and McGlothlin are also able to see how these sexually dimorphic traits react to a variety of selection regimes, including selection that acts in opposite directions in males and females. In addition, using these simulations, they are able to estimate how different traits can be evolutionarily constrained: genetic correlations between the sexes appear to constrain selection on skeletal phenotypes, but not dewlap-related phenotypes.

These methods are likely to be extremely useful to anyone hoping to measure selection in natural population of anoles, or any other sexually dimorphic species. Sex differences often play an important role in how an organism can evolve in the wild, and introducing them into the way we quantify selection and its response is a key contribution to understand this process. I encourage anyone interested in the details of this method to check out the recent paper by the authors below for more details!

Cox, R. M., Costello, R. A., Camber, B. E., & McGlothlin, J. W. (2017). Multivariate genetic architecture of the Anolis dewlap reveals both shared and sex‐specific features of a sexually dimorphic ornament. Journal of Evolutionary Biology.

Evolution 2017: The Evolution of Anolis Adenovirus

We all wish anoles were invincible, but, sadly, they aren’t. Sofia Prado-Irwin’s poster at the Evolution 2017 meeting discussed one of anoles’ putative foes–the adenovirus. Adenoviruses infect a wide diversity of hosts, from amphibians to mammals, and though they are well characterized in captive and domesticated populations, we know very little about their evolution in the wild.


Sampling opportunistically from deceased animals in a breeding colony of Anolis sagrei as well as from one fecal sample, Prado-Irwin (Harvard University) was able to examine the prevalence of adenovirus in lizards caught on six different Bahamian islands. In particular, she was curious about three questions:

  • Was the mortality of animals in the breeding colony associated with adenovirus?
  • Is adenovirus present in anoles in the wild?
  • Does adenovirus coevolve with its hosts? In other words, does the phylogeny of A. sagrei from these 6 islands match the phylogeny of those animals’ viruses? Or perhaps, instead, the geographic distance between hosts’ islands explain how strains of adenovirus are related to one another?

Extracting genomic DNA and then amplifying virus-specific genomic regions, Prado-Irwin was able to show that adenovirus was certainly found in wild as well as lab-housed animals. However, mortality was unlikely to be due solely to the virus–only 23% of the deceased animals were infected. Finally, there was no evidence for for the adenovirus phylogeny matching either the lizard hosts’ phylogeny or tracking their geographic distribution. Instead, adenoviruses seem to shift hosts readily, with some A. sagrei adenovirus protein sequences being more closely related to mammalian adenovirus strains than to other anole strains! In a nutshell, virus evolution is complicated, and much remains to be learned about these submicroscopic maybe-destroyers of our favourite lizards.


Evolution 2017: Are We Wrong about Territoriality in Anolis Lizards?

Anolis lizards have long been thought to be territorially polygynous reptiles, meaning specifically that males maintain and defend a small area in which they sire all (or the vast majority) of the offspring produced by females residing in said area. Ambika Kamath (UCSB) challenged that long held belief today in her presentation at this year’s Evolution meeting.

A conventional model of territoriality: a male defends a territory containing multiple females (from, photos by Rachel Moon)

When Ambika looked at the historical basis of the initial assertion that anoles are territorial she found that this claim  was made with little to no empirical evidence and that there are several studies documenting  females residing within a male’s territory producing offspring sired by multiple males. This made her wonder if the species she works on (Anolis sagrei) are, in fact, territorially polygynous. She did so with an extensive empirical study of 253 lizards over an area of 7100m2. Her results clearly indicate that male A. sagrei do not maintain the assumed small territory, rather, they regularly travel outside of their projected 10m diameter range throughout the breeding season (photo below). Additionally, the majority of females in the study both encounter and produce offspring sired by multiple males.

Dark circles = static territory, small circles = observed sightings of A. sagrei males over the breeding season

Ambika concludes that  A. sagrei does not fit the definition of a territorially polygynous species. Males do not maintain the expected territories and there is significant polyandry. Importantly, Ambika points out that the assumption of territoriality influences study design by limiting sampling area and duration and that such limitations simply reinforce the territoriality assumption. Her findings call for the potential re-tooling of study designs and empirical investigation into the mating systems of other species long considered territorially polygynous.

For more on this research, check out the recent publication on this work:
Kamath A, and JB Losos. 2017. The erratic and contingent progression of research on territoriality in Anolis lizards. Behavioral Ecology and Sociobiology 71:89.

Effects of Age- and Sex-specific Density on Behaviour and Survival of the Brown Anole

A perching brown anole.

An adult male brown anole.

Greetings anole biologists and enthusiasts! I write to you from Fred Janzen’s 30-year field site along the Mississippi River in northwest Illinois, where I’m collecting data for my dissertation studies. Unfortunately, there aren’t any anoles here, but the painted and common snapping turtle densities are impressive. Fortunately for this post, however, current field work has been paused as a team of inmates are cleaning up debris from recent flooding of the area. Thus, I’ll give a brief update on the last chapter of my master’s research with Dan Warner and the brown anoles* of northeastern Florida.

A good bit of Anolis work has shown that species partition perch height and width to reduce competition. However, less work has focused on habitat partitioning within species of anoles. Thus, my thesis work examined whether similar partitioning exists between age and sex classes of the brown anole, and attempted to identify the drivers and mechanisms of such age-specific habitat use. First, we found that juveniles on Dan’s study islands perch on lower and thinner perches, and use the ground more frequently, than adults (discussed in another Anole Annals post). We then altered the density of adult males in mesh enclosures in the lab, and found that juveniles perch lower in the presence of adult males and have a greater response as adult male density increases (discussed in another Anole Annals post also).

Fig 1

Juvenile Anolis sagrei survival in response to adult male and female density (F4, 164 = 3.67, P = 0.0069).

Quite excited by our findings that adult male density influences juvenile microhabitat choice, we set up two field experiments to assess 1) how adult male and female densities independently affect juvenile microhabitat use and survival, and 2) how juvenile presence affects adult male and female microhabitat use. Interestingly, we found that after just four days of exposure, adult male, but not female, presence reduced juvenile survival (Fig 1). However, we found no evidence that juveniles shifted microhabitat use behaviorally, nor were juveniles selected against in a pattern consistent with the observed age-specific habitat use in the field (e.g., selection favoring low perching juveniles) in response to either adult males or females. One large difference between the lab and field experiments is that the lab experiment used larger juveniles than the field experiment. Perhaps the smaller field juveniles innately perched in safe microhabitats, thus reducing their ability to behaviorally respond to adult threats. In addition, strong past selection favoring low perching hatchlings may have reduced the phenotypic variation needed to detect any selective patterns. The second field experiment revealed that adult microhabitat use is not affected by the presence of juveniles.

This last chapter has recently been published and is freely available through this link until 25 July 2017 (Delaney and Warner. 2017. Animal Behaviour 129:31-41). After that, shoot me an email.

For now, I’ll be studying fitness tradeoffs in maternal investment strategies in turtles. However, once an anologist, always an anologist. So I’ll keep an eye on Anole Annals to get my Anolis fix, until I find my way back south.

Happy noosing!

*Note – I’m certain that “Dan Warner and the Brown Anoles” should be a band name.


Phylogeny and Diversity of Monkey Lizards, Anoles’ Closest Relatives


Monkey lizards (Polychrus) are unique among Neotropical arboreal lizards in having strikingly long whip-like tails, as well as long limbs and digits. Interestingly, they resemble Old World chameleons in both morphology and behavior: slow-moving lizards with a laterally compressed body and cone-shaped eyes with partially fused eyelids. Although their phylogenetic position in the iguanid tree of life remains controversial, many authors argue that monkey lizards are the living sister taxon of anoles.

In a study published last week in PlosONE, we present a molecular phylogeny of all eight currently recognized species of Polychrus based on the largest geographic sampling to date. Our species tree places P. acutirostris as sister to all other species of Polychrus. While the phylogenetic position of P. gutturosus and P. peruvianus is poorly resolved, P. marmoratus and P. femoralis are strongly supported as sister to P. liogaster and P. jacquelinae, respectively. Moreover, recognition of the recently described P. auduboni and P. marmoratus sensu stricto as distinct species suggests that the populations of “P. marmoratus” from the Amazon and the Atlantic coast in Brazil represent separate species. Finally, species delimitation analyses suggest, among other things, that the populations of P. femoralis from the Tumbes region (southwestern Ecuador and northwestern Peru) might belong to a cryptic undescribed species.