Anole Annals

When I mentioned to Jonathan Losos that I had applied a new biogeographic model to anoles, he gave me a copy of Lizards in an Evolutionary Tree. What could I do but take it as both a generous gift and gentle suggestion? This is all to say that I’m no herpetologist. I know this, and so should you. I write humbly to the AA readers as a twig anole standing on the shoulders of crown-giants.

With that said, several close colleagues (Ignacio Quintero, Martha Muñoz, Felipe Zapata, Michael Donoghue) and I recently had a paper published that introduces a new modeling framework that allows regional features of geography to inform phylogenetic rates of dispersal, extinction, and speciation – called FIG (Feature-Informed GeoSSE). We then applied FIG to the phylogenetic and biogeographic Anolis dataset published by Steven Poe and co-authors. This piece summarizes that work and subjects its readers to a few lame jokes.

Cartoon of FIG model behavior.

The first aim of our project was to propose a new framework for modeling historical biogeography using GeoSSE, a diversification model introduced by Goldberg et al. (2011). Under GeoSSE models, all species occupy different sets of regions in a shared geographical arena. As time advances, species stochastically disperse, go extinct, and speciate. Speciation itself might occur within a region or between regions (e.g., in a manner consistent with allopatric speciation).

Thinking realistically, when and where these events happen should somehow depend on the set of regions each species occupies and the geographical features of the relevant regions. Unless instructed otherwise, however, GeoSSE estimates every possible event rate from phylogenetic and biogeographic data alone. Regional features of geography aren’t used. This leaves historical biogeographers with at least one technical problem and one missed opportunity.

First, concerning the technical problem, the number of event rates explodes with the number of regions. A geographical system with two regions (A and B) requires seven rate parameters: two within-region speciation rates for regions A and B, two extinction rates for A and B, two dispersal rates for A into B and B into A, and one between-region speciation rate for splitting the widespread ancestral species with range A+B into two daughter lineages with ranges A against B. Three regions requires 18 rates, four regions requires 45 rates, and so on. Between-region (“allopatric”) speciation rates and, to a lesser degree, the dispersal rates fuel this explosion in rate parameters. Somehow the number of rates must be reduced if we hope to estimate any of them at all.

In FIG, regional features (size, distance, barriers) can inform event rates. Different features are free to have different relationships with each process. For example, region size may increase within-region speciation rates while decreasing local extinction rates. Distance may decrease dispersal rates but increase between-region speciation rates. FIG also allows for barriers and distances to inform the rate and way in which a widespread range splits following between-region speciation.

Second, concerning the missed opportunity, biogeographers often hypothesize how geographical features should influence evolutionary outcomes – for example, that a single species should “split” in two more rapidly when its range is subdivided by a barrier – but GeoSSE has not really been used to test such hypotheses, in large part because of the technical issue mentioned above.

For hypothesis testing, FIG analyses estimate the probability that each geographical feature has an effect on a corresponding class of evolutionary rates. This is done with Bayesian reversible-jump Markov chain Monte Carlo to turn “on” and “off” different relationships between features and rates. For example, if FIG estimates that the effect of distance on dispersal was “on” in 97% of MCMC samples, you might make the bold claim that distance influences dispersal rates between regions. Or, if the effect of size on extinction was “on” in only 31% of samples, you might say no conclusive relationship or non-relationship was detected.

The other aim of our work was to see if FIG produced any biologically interesting inferences. If not, why bother? Anolis led the pack when selecting a clade to feature for empirical analysis. Anoles are well-known for their distribution throughout the Caribbean and the neotropical mainland, with some expectation of moderate, but not rampant, dispersal. Because anole phylogeny and biogeography has been studied in such detail over the decades, the clade is also ideal for test driving phylogenetic models.

Geographical distribution of Anolis.

We adapted the Poe et al. (2019) dataset into a nine-region biogeographical system with five continental and four insular regions of varying sizes and distances. There are ~380 anoles in this dataset, with nearly as many insular as continental species, but nearly [*] all widespread anoles are restricted to adjacent continental regions. This is exactly the type of pattern you’d expect to see if geographical distance and oceanic barriers restricted anole movement. That is, widespread fragmented ranges should be difficult to maintain and should therefore be rare.

Biogeographic rates. Left: extinction (nodes) and dispersal (edges) rates. Right: within-region speciation (nodes) and between-region speciation (edges) rates.

Reassuringly, FIG inferred that dispersal was limited by distance, especially over water. Similarly, between-region speciation rates split ranges the fastest when the inhabited regions were far apart and/or separated by water. Region size and island-status did not have a predictable effect (or non-effect) on extinction and within-region speciation rate. The network diagrams above summarize different regional rates of evolutionary change.

Dispersal rates, between-region speciation rates, and distances.

We also were interested in a critical distance that we defined – the maximum range cohesion distance – beyond which widespread species tended to split into two rather than remain as one. The idea is that if dispersal rates are low, interpopulation migration rates should be low, and therefore rates of allopatric speciation should be high. If we assume that FIG’s dispersal rates approximate the rates of pulsed migration needed to maintain gene flow between regions, we predicted the corresponding distance at which organismal movement became too slow to maintain range cohesion. So how far is too far?

Our scrappy little estimator predicted that range cohesion is almost certainly degraded beyond ~470km over land and ~160km over water. As it turns out, six pairs of continental regions had average distances closer than 470km, where we find all widespread continental anoles today. We don’t expect that these distances perfectly describe the limits of range cohesion for all anole species in all contexts, but a cursory review of the anole population genetic literature convinced us that our estimates were at least reasonable.

Extinction rates, within-region speciation rates, and sizes.

We didn’t recover an analogous relationship for the ratio of extinction and within-region speciation rates with region size. But neither does FIG reject those relationships. Still, recalling the histogram of regional species richness above, it seems unlikely that size alone dictates richness in anoles across continental and insular regions – as they’re defined here – since Amazonia has so few species relative to much smaller regions, like the island of Hispaniola. More work on this issue is needed.

In its conclusion, our paper reflects on how phylogenetic models of biogeography treat allopatric speciation. With anoles under FIG, for example, the consequence of dispersal into a new region depends on the geographical context. If dispersal is between adjacent continental regions, dispersal tends to result in range expansion. But, if dispersal is between distant regions or involves insular regions, it tends to result in cladogenesis that’s consistent with allopatric speciation. In large part, this inference was made possible because regional features inform evolutionary rates in FIG, letting us predict where anoles tend to “split or spread.” We think this historical view of allopatric speciation in a phylogenetic context will be worth exploring further.

Not to pander, but Anolis has played and continues to play such an instrumental role in the development of biologically meaningful models of ecology and evolution. Many of the statistical phylogenetic models that I’ve looked to for inspiration in my own research over the years were introduced by anolologists. Maybe this is a second meaning for model clade? Rambling aside, our project was a true collaboration among some of the most creative organismal and mathematical biologists I’ve known. Our hope is that our small contribution lives up to the high standard of modeling anole diversity.

*–An innocent question from an outsider: is A. sagrei really a single species? Pretty wild.

Paper:
MJ Landis, I Quintero, MM Muñoz, F Zapata, MJ Donoghue. 2022. Phylogenetic inference of where species spread or split across barriers. Proceedings of the National Academy of Sciences 119: e2116948119. doi:10.1073/pnas.2116948119

Code:
https://github.com/mlandis/fig_model

Lab site:
http://landislab.org

Body Condition and Jumping Predict Initial Survival in a Replicated Island Introduction Experiment

By Colin Donihue

On April 20, 2022

In New Research

Back in 2014, collaborators Panayiotis Pafilis, Anthony Herrel, Johannes Foufopoulos and I initiated a multi-island lizard introduction experiment, inspired by the foundational anole evolutionary ecology work of Losos, Schoener, and Spiller. Our twist: we were going to do it in Greece, with a different genus of lizard – Podarcis. Wall lizards haven’t radiated like anoles, but there is fascinating work demonstrating rapid evolution in the genus and a large descriptive literature documenting the phenotypic differences of populations living on mainland, large islands, and small islands.

We introduced 20 marked individuals from the large, predator-rich island of Naxos to each of five Podarcis-free islets, and revisited the populations annually (up until pandemic), censusing each island. Each year we gathered new morphology, performance, behavior, and diet data, and released the lizards back to the experimental islets. We’ve just published a new paper showing that the traits that best predicted initial survival were not all the ones we’d expected. Body condition – sure – lizards with a higher body condition probably have the reserves that enable them to weather the stressful introduction. Bite force? Not so much. We’d expected bite force to be an important predictor of survival because lizards with harder bites would be more competitively dominant and also have access to defended prey items like gastropods. Contrary to our expectation, bite force was not a predictor of survival (but stay tuned, bite force has become more and more important as the experiment has continued).

If you’re interested, I’ve written lots more about the experiment on my blog over the years. We also have photos and videos from the islets:

Finally, a quick call to the community: I have six years of tissue samples from the five islet populations, but don’t have the molecular chops to ask any of the fantastically interesting questions we might be able to with paired survival, phenotype, and molecular data. If you’re interested in a collaboration, let me know!

New Literature Alert:

Colin M Donihue, Anthony Herrel, Johannes Foufopoulos, Panayiotis Pafilis, Body condition and jumping predict initial survival in a replicated island introduction experiment, Biological Journal of the Linnean Society, 2022;, blab172, https://doi.org/10.1093/biolinnean/blab172

Abstract: Over-water dispersal to small islets is an important eco-evolutionary process. Most often, new arrivals on islets find the environment harsh or mate-less, making their footholds on these islets fleeting. Occasionally, introduced animals are able to survive the strong selection following their arrival, leading to subsequent propagation and, in several famous cases, adaptive radiation. What traits predict that initial survival? We established a replicated island introduction experiment to investigate this process in lizards. In 2014, we introduced 20 Podarcis erhardii lizards to each of five small islets in the Greek Cyclades Islands. We found that the lizards that survived were those with better initial body condition, longer distal portions of their limbs and a greater propensity for jumping. Contrary to our expectations, neither body size nor the strength of the lizards’ bite – two traits positively related to competitive ability, which becomes important later in the colonization process in lizards – predicted survival. This is the first selection study of its kind investigating an experimental introduction of Podarcis, and whether the traits that determined initial survival are important in driving the future evolutionary trajectories of these populations remains to be determined.

Dorsal Pattern Formation in Anolis Lizards

By Nathalie Feiner

On April 18, 2022

In All Posts

Picture of a female A. sagrei with the diamond pattern.

Readers of this blog will be well aware of the conspicuous variation in dorsal color patterns of Anolis lizards – think of the spots of A. sabanus, or the bands of A. transversalis (both worthy a google search if you happen to be unfamiliar with them). Such patterns are particularly interesting when several patterns exist within a single population – a polymorphism. This is the case in A. sagrei where females have either a chevron-like pattern, same as all males of this species, or a diamond-like pattern on their backs.

In 2016, I visited some A. sagrei populations in Florida and became interested in this female-limited color pattern polymorphism. Being a developmental biologist, what puzzled me most was not if selection can maintain multiple patterns, but how the two patterns actually develop.

On the one hand, the difference between the two patterns ought to have a simple genetic basis. Diamond- and chevron-females mix within the same population and the two morphs are discrete (although there is a continuous variation within both morphs, and the diamonds sometimes look more like a band [1]). On the other hand, the developmental biology of pattern formation is far from trivial. Here is a little teaser of the complexity: in vertebrates, pigment cells are derived from neural crest cells that originate along the dorsal midline of the early embryo. Once detached from the crest of the neural tube, pigment cell precursors migrate towards their final destination in the epidermis, where they differentiate into pigment cells – xanthophores, melanophores and iridophores. What these cells do and how they organize themselves are what gives rise to patterns. And this does not seem to be very simple at all. So how can we reconcile a simple genetic basis with the complex developmental biology of pattern formation of diamonds and chevrons?

The two female morphs and a male of A. sagrei.

Simply out of curiosity, we set out to solve this puzzle. Thanks to our anole breeding group at Lund University, we already had three generations of A. sagrei of both morphs that we could use to address the pattern of inheritance of diamonds and chevrons, and to identify the underlying gene(s). Our intuition about the simple genetic architecture of the polymorphism held true, and we identified a single Mendelian locus that perfectly segregated with the morph patterns.

Surprisingly though, the locus was not on a sex chromosome, so this could not explain why only females are polymorphic. Instead, the identity of one of the two genes located at the Mendelian locus pointed to a solution: the estrogen receptor 1 gene is crucial for the development of female traits and therefore expressed at higher levels in females compared to males. Because of the close physical proximity of the two genes at the Mendelian locus, also the second gene shows a female-biased expression pattern. So while the estrogen receptor 1 gene does not explain the pattern differences, it explains why the polymorphism is only present in females.

But what is this second gene at the Mendelian locus, and how does it explain the difference in patterning? It is a gene encoding the coiled-coil domain-containing protein 170, or CCDC170. Not exactly a usual suspect of color pattern formation. In fact, not much is known about this gene, but the cancer literature had demonstrated that it codes for a structural protein that regulates the migratory capacity of cells (mutations in CCDC170 can make cancer cells migratory and are associated with an aggressive type of breast cancer). The proteins encoded by the diamond and chevron alleles were predicted to form CCDC170 proteins with structural differences. This is likely to affect the function of the protein – perhaps by influencing migratory behaviors of pigment cell precursors.

Testing this hypothesis is easier said than done. As a first proof-of-principle, we used an in silico modelling approach to test if tinkering with the migratory capacity of cells can switch a system from generating chevron-like to diamond-like patterns. Miguel Brun-Usan is a magician with cell-based computer modelling and his trick is to create computer models that are complex enough to capture real biological phenomena, yet simple enough to allow us to trace and understand what is going on. To get to the bottom of the diamond/chevron morph differences, he implemented cells on a growing epithelium with a Turing-type mechanism consisting of a gene regulatory network (GRN) with up to five genes. By running a number of experiments (yes, computer scientists also run experiments, I learned), Miguel could demonstrate that some GRNs generated back patterns that very much resembled those of real lizards. Moreover, he found that modifying a single gene in the GRN that regulates the migratory capacity of cells is sufficient to switch the system from generating chevrons (if migration is switched ON) to diamonds (if migration is switched OFF).

A brief graphical abstract of our study.

So it seems that what reconciles the simple genetic basis of the polymorphism with the complex process of pattern formation is that the underlying developmental system exhibits a high degree of controllability. Simply modifying migratory capacities of cells by tinkering with one gene in the core GRN leads to changes in collective cell migration, visible as a distinct and new dorsal color pattern. Such high controllability could explain the evolvability of dorsal color patterns and result in high turn-over rates between patterns, as beautifully demonstrated by geckos [2]. I am excited to continue this research to see if the model can be substantiated mechanistically. I would also like to test if convergent evolution of diamond patterning in different Anolis species is underpinned by convergent developmental and genetic mechanisms. If you are interested in joining our research group, please get in touch (nathalie.feiner@biol.lu.se; www.feiner-uller-group.se).

You can read the full article here:

Feiner, N., M. Brun-Usan, P. Andrade, R. Pranter, S. Park, D. B. Menke, A. J. Geneva, and T. Uller. 2022. A single locus regulates a female-limited color pattern polymorphism in a reptile.
Science Advances 8:10 DOI: 10.1126/sciadv.abm2387

Other references:

Moon, R.M., and Kamath, A. (2019). Re-examining escape behaviour and habitat use as correlates of dorsal pattern variation in female brown anole lizards, Anolis sagrei (Squamata: Dactyloidae). Biol J Linn Soc 126, 783-795.
Allen, W.L., Moreno, N., Gamble, T., and Chiari, Y. (2020). Ecological, behavioral, and phylogenetic influences on the evolution of dorsal color pattern in geckos. Evolution 74, 1033-1047.

Anoles Are Powerful Educators, Use ’em!

By Terry Ord

On March 31, 2022

In All Posts, Anole Videos, Education and Anoles

Did you ever read those choose-your-own-adventure books as a kid? I had a whole collection. What if lectures were like that too? Check this one out on anoles (above).

This lecture came about from the need to update a lecture on ecological competition for a second year undergraduate course. In the past, someone might have handed me a textbook and I would have quickly shelved it, never having opened its cover. As a student I hated textbooks and things really haven’t changed for me now as an educator. The real challenge isn’t the content, it’s presenting that content effectively. We’re now on the other side of “the great digital shift of 2020,” but this challenge of engagement remains the same, if not more so. Does this choose-your-own-adventure lecture offer the solution?

Let’s step back for a moment so I can first make the case for anoles…

Anoles first came into view for me way back in my first year of graduate school. Not in real life, of course — there were no anoles at any of my field sites in Sydney. Instead, I happened across a remarkable paper appearing in one of the weekly tabloids. It recounted how researchers had returned to some tiny islands in the Bahamas where a bunch of lizards had been introduced a decade or so before. I couldn’t make head nor tail of the PCA plots or Tables. But the scatterplot later in the paper was clear to even a dunce like me. These lizards had adapted their limbs over a matter of years (years!) to cope with living on spindly bushes. Evolution happening in real-time? Holy cow, this was revolutionary for me. Why am I only seeing this now?

I’d never really thought about adaptation outside of centuries or millions of years. But then my undergraduate experience was the usual, tired textbook fodder of ecology and evolution that never came to life, regardless of how glossy the graphics might have been. My undergraduate experience was mostly about memorising facts and figures, and there was a great mental chasm between those and the real world around me. What I actually saw in nature were animals doing weird and crazy things, so I ultimately gravitated towards animal behaviour for my PhD. But when I discovered this paper, I had just finished reading Richard Dawkin’s “selfish gene” and Dan Dennett’s “Darwin’s dangerous idea,” and I was now fascinated by evolution.

And here was some character named Jonathan Losos, along with his mates Ken Warheit and Tom Schoener, reporting in a glossy magazine called ‘Nature’ years before (in 1997 no less) that evolution happens now, not in the past… Now! If only I had been exposed to this and other stuff like it as an undergraduate. [NB: Jonathan gives a great backstory in his book about how this study almost never left the bottom drawer].

These days I am towards the other end of the student-teacher continuum and I make a point of not teaching from a textbook. First, they are WAY too expensive for students. Second, they are out of date by the time they are published. Third, if classic works are covered (like those on anoles), the format of a textbook makes even the most exciting example remote and dull. My approach has always been to go directly to the source. And anoles offer such a rich collection of content for educators.

But what of this new “choose-your-own-adventure” style format? What is really being achieved here? My sales pitch to you is that it prompts student engagement at strategic points. By doing so, it maintains an active connection between the student and the content. In other words, it should stop students cognitively dropping out while writing copious amounts of notes that they will only ever read just before the exam and promptly forget soon afterwards. By forcing students to direct their own learning experience, they are being subtly pushed to reflect on the content explicitly and intuitively, and they might not even realise it. The hope is they not only grasp the concepts being presented more effectively, but retain (and apply) that comprehension outside the bounds of the course and into the future. And it’s fun too.

Convinced?

The danger is the format could just be a gimmick that’s great as a one-off, but quickly becomes annoying or distracting. The analogy I think of here is the transition from slides to powerpoint in my early conference days at the start of the 2000s. For the ancients among you who remember that time, you might recall having to sit through a plague of animated slide transitions with cheesy swirly sounds as presenters explored the seemingly infinite number of options on offer. Oh, the liberation of going digital! Then most of us eventually realised how annoying and distracting it all was and went back to simpler presentations. Perhaps “choose-your-own-adventure” lectures are the same? Would you have an entire course with choose-your-own-adventure lectures?

Huge thanks to Mike Kasumovic and Arludo for both the hideous yellow shirt and putting the lecture together for me. I use a lot of Arludo’s interactive digital games in my teaching as well – they’re free, the students love them, and they have clear educational outcomes. Evolution, ecology or behaviour, whatever you need, they’ll have something you can engage your students with. Do check them out.

More Evidence Of Seed Dispersal In Anoles

By Aryeh Miller

On March 28, 2022

In All Posts

Anolis porcatus is the most recent Caribbean anole to have been documented to consume and disperse seeds. Natural history research by Armas (2022) observes A. porcatus feeding on West Indian holly, and finds successful germination of the fecal pellets. Credit Thomas Brown (Wikimedia Commons).

Recent research on Anolis lizards has suggested their omnivorous tendencies might aid in the dispersal of seeds. Most recently, this was discussed by Giery et al. (2017), who reported Cuban Knight Anoles (A. equestris) to consume and disperse royal palms. This year, Armas (2022) reports Anolis porcatus consumes and disperses West Indian holly. Check it out!

New literature alert!

Consumption and Dispersal of West Indian Holly (Turnera ulmifolia, Turneraceae) Seeds by Cuban Green Anoles, Anolis porcatus (Squamata: Dactyloidae)

In Reptiles & Amphibians

Armas (2022)

Literature Cited:

de Armas, L. F. (2022). Consumption and Dispersal of West Indian Holly (Turnera ulmifolia, Turneraceae) Seeds by Cuban Green Anoles, Anolis porcatus (Squamata: Dactyloidae). Reptiles & Amphibians, 29(1), 115-116.

Giery, S. T., Vezzani, E., Zona, S., & Stroud, J. T. (2017). Frugivory and seed dispersal by the invasive knight anole (Anolis equestris) in Florida, USA. Food Webs, 11, 13-16.

How Do Anole Species Tell Each Other Apart?

By Terry Ord

On March 26, 2022

In New Research, Research Methods

When it comes to finding a mate or defending a territory, animals need to recognise members of their own species. The reasons are intuitive: you only want to mate with your own species to ensure viable offspring, and you should only invest the effort in being territorial when confronted by rivals from your own species. There are exceptions and these are interesting—hybridization or territorial competition between species—but generally animals need a system for species recognition.

The large, often spectacularly coloured throat fan or dewlap of anoles seems like an obvious way to evaluate species identity. Taxonomists have historically thought so, too. Each species appears to display a dewlap that’s unique in colour and pattern. But there are various Anole Annals posts highlighting this is not always the case. Instead, the colour of the dewlap is often an adaptation to the light environment for enhancing the detection of territorial displays.

So what about those territorial displays? Might anoles use the complex movements of the head-bob and push-up display to figure out species identity?

Classic work by Charles Carpenter and Tom Jenssen revealed how often the head-bob movements of lizards, and anoles in particular, seemed specific to each species. Pioneering experiments using video playback by Joe Macedonia in the ’90s has also provided evidence that anoles are able to distinguish displaying rivals of their own species from those of other species. But what is it about the pattern of movements used in the head-bob and push-up display, or even how the dewlap is extended and retracted, that conveys species identity? Is there one feature that varies the most among species that anoles commonly rely on to identify species?

Display-Action-Pattern graphs (above) showing the complexity of movements used by Puerto Rican anoles for territorial advertisement displays

These are hard questions to answer. Anole displays are complex, using many different types of movements, so there’s a huge number of possibilities. One approach would be to isolate and manipulate each type of movement and use video or robot playbacks to ask the anoles themselves. But doing that would take an entire career. There are a seemingly infinite number of combinations to consider. In fact, it would be impossible without a way to narrow things down.

Claire Nelson is a creative (and courageous!) graduate student who had an eye for solving the challenge. She figured it was possible to leverage the large archive of footage I’d accumulated over many, many years. These videos were of free-living male lizards performing territorial advertisement displays. Her idea was to develop an objective method for identifying which movements used in the head-bob, push-up or dewlap display had the potential to convey species identity. She’s just published her solution in Animal Behaviour.

Claire (above) doing a balancing act with some non-anoles

Claire used this archive of display videos to create Display-Action-Pattern graphs, a method developed by Carpenter back in the 60s. These track the up-and-down movement of head-bobs and push-ups as well as the extensions and retractions of the dewlap during the territorial display. To keep it manageable, she limited her efforts to anole species on Puerto Rico, and graphs of about 10 territorial advertisement displays per male. But there was an important biological reason for selecting this number of displays as well. It effectively mimicked the number of displays an anole might typically see on first encountering another lizard. That is, anoles likely make judgements on species identity from only a handful of displays.

From these Display-Action-Pattern graphs, Claire took a host of measures, ranging from the duration and number of movements used, to variation in amplitude and pauses between movements. She also noticed that anoles tend to perform certain combinations of movements together in what she came to call ‘motifs.’ After many many hours of effort, Claire accumulated a huge amount of data for nearly 20 different types of display movement for eight Puerto Rican Anolis species, and in many cases, for different populations of the same species.

Claire asked me for advice on how to analyse it all. I have to admit I was completely useless on this front. I muddled something about using coefficients of variation and some other nonsense, but really I had no idea. I was still in shock over how much data she had accumulated, and the novelty (and implications) of discovering motifs in the displays. She knew what she was doing, though. Her analytical solution was vastly superior to anything I could have suggested.

Claire investigated a variety of approaches, but in the end she settled on the method of random forest tree classification. It’s a sophisticated machine learning algorithm that, in a nutshell, takes data and groups like with like. It doesn’t require any prior direction or preconceived notion on how data should be grouped. It just uses the variation in the data itself. You could view the algorithm as an anole brain using basic rules of variation to make judgements on which displays are likely to be different and which displays are likely to be the same.

The outcome was impressive. The algorithm correctly assigned the vast majority of lizards to their correct species based on just a handful of displays. Where errors occurred, it was partly because lizards were assigned to the right species, but the wrong population. This means anoles from different populations tend to share some display features because they’re still from the same species. Yet the algorithm was able to correctly assign most lizards to the right population. In other words, there was still enough variation in the displays between populations of the same species to identify them as belonging to separate populations. This is very interesting!

Random forest tree classification (above) can assign over two thirds of displaying lizards to their correct species.

The evolution of new species begins with individuals of the same species starting to segregate from each other in some way. Often it’s physical separation (on opposite sides of a mountain range), but changes in social signals can also prompt behavioral separation as well. This could be the case for some anoles on Puerto Rico. Once individuals stop recognising each other as the same species, they no longer reproduce with one another, and the door to speciation is propped open.

The other discovery Claire made was the apparent lack of any common display feature that could be used to identify species (and population identity). Instead, different features were important for different species. The duration and number of headbob movements were features that could be used to identify the territorial displays of Anolis poncensis—a species that is striking in its use of lots of extremely rapid, up and down body movements—whereas the way the dewlap was extended was influential in identifying different populations of Anolis gundlachi—a species that has an unusually long dewlap display. Other species like Anolis pulchellus and Anolis krugi were best identified by effectively considering features of the entire territorial display.

Whether or not anoles actually use the features identified by the algorithm in species recognition remains an open question. But Claire has managed to identify the potential candidate cues that could be used. It is now possible to develop a focussed research program to test whether, and how, anoles used these features to identify species. Again, the obvious way to do this would be to ask the lizards themselves using robot playbacks.

Random forest tree classification sounds awfully complicated, and it is very sophisticated, but it’s actually easy to implement. Any dummy can do it. I taught myself how and wrote a step-by-step tutorial so you can as well. We’ve published this tutorial alongside Claire’s paper in Animal Behaviour. Give it a whirl!

How Many Anoles Are There in Captivity (Pets, Zoos, Labs) Worldwide?

By Jonathan Losos

On March 23, 2022

In All Posts

Photo from http://www.petworldshop.com/

Nigel Rothfels, a historian of animals and culture at the University of Wisconsin-Milwaukee, asks:

Given the previous AA post on anoles in the pet trade, the amount of in-country breeding there must be of anoles, the general life-span of anoles, and the general growth in pet-keeping since Covid, what is your highly educated guess on the number of anoles currently being kept in captivity world-wide (as pets, for educational supply companies, in labs, or zoos). With 350,000/year being collected in just Louisiana in 2006, it makes me think that something like 3-5 million might still be an underestimate.

Anyone want to venture an estimate?

Shape Variation of the Pectoral Girdle of Anolis Ecomorphs

By Alex Tinius

On March 16, 2022

In Education and Anoles, Research Methods

The first three paragraphs of Jane Peterson’s contribution to the Second Anolis Newsletter.

Jane Peterson’s contribution to The Second Anolis Newsletter remains one of the most comprehensive exemplars of functional-morphological research of the anoline appendicular girdles. In just a few short paragraphs Peterson (1974) outlined the key differences in pectoral girdle morphology between the Anolis ecomorphs, drawing information from both field observations and anatomical dissections of anoles from all four Greater Antillean islands. The outlined study could have formed a major contribution to our understanding of ecomorphology, had these brief observations ever been expanded into a scientific publication. Sadly, they remained as notes, confined to a brief communique on an informal basis (that continues to be formally cited). Several intriguing studies hence have examined anole appendicular morphology, but rarely allowed for implications that reach across multiple island radiations (e.g. Anzai et al. 2014, Herrel et al. 2018).

With my 2016 Ph.D. thesis, I set out to quantify what Jane Peterson had observed forty years prior, and must confess that I still fall short of reproducing the multitude of implications that Peterson’s (1974) brief descriptions alluded to. Instead of combining video-recorded movement cycles with morphological descriptions, my comparisons are solely based on three-dimensional shape analysis of the skeletal elements that comprise the breast-shoulder apparatus (BSA): the clavicle, interclavicle, presternum, and scapulocoracoid (Fig. 1). Employing the power of computed tomography scanning, and geometric morphometric analysis, I quantified the shapes of the central elements of the pectoral girdle, and compared these across anole radiations.

As with earlier work, I focused on the Jamaican ecomorph representatives, and sought out their ecomorph counterparts from Hispaniola and Puerto Rico, particularly targeting those species that are the most and least similar to the Jamaican forms. That last line of thought did not reveal any straightforward answers, as the complex structural shape of the BSA allows these anoles to be relatively distinct in some aspects, while being quite similar in others. For example, the general shape of the presternum and interclavicle are quite similar between the two trunk-ground anoles Anolis lineatopus (Jamaica) and A. gundlachi (Puerto Rico), while that of the scapulocoracoid differs quite remarkably between the two. These complex associations will take a more detailed analysis than what is warranted here, so I’ll focus on the bigger picture instead.

Fig. 1: CT-rendition of the skeletal components of the breast-shoulder apparatus of Anolis baleatus in lateromedial view, depicting all anatomical features described in the text. The gray arrow denotes anterior.

Skeletal elements of the BSA in isolation

Previous analysis of the scapulocoracoid in isolation revealed that its shape differs between Anolis habitat specialists, and resembles a particularly dorsoventrally tall shape in twig anoles (Tinius et al. 2020). The other ecomorph groups (trunk-ground, trunk-crown, and crown-giant) show obvious tendencies towards a particular structural organization, but in none of these does the scapulocoracoid resemble a truly characteristic shape.

The New Yorker Features an Anole Cartoon

By Jonathan Losos

On March 12, 2022

In All Posts

John David Curlis

By Anthony J Geneva

On March 1, 2022

In Scientist Profiles

Where do you work and what do you do?

I am currently a graduate student at the University of Michigan, but I conduct most of my research in the tropics of Central and South America. I am broadly interested in trying to answer the question of how to explain patterns of phenotypic diversity found in nature, especially in the context of color and signaling. In other words, why do organisms look the way they do – why do they have certain colors over others, and what sort of information are they conveying by showing off those colors? When not focusing on my research, I spend virtually all of my free time photographing as many animals as I can find, as well as spending countless hours sorting said photos into their respective taxonomic groups. What can I say, I’m a biodiversity nerd!

What aspects of anole biology do you study, and what have you learned?

I study the evolution of color in anole dewlaps. Even with over 400 species, all anoles possess this extendable throat fan, and it’s often brightly colored. Although we have some understanding of how the dewlap functions as a signal (e.g., species recognition, competitive interactions, courtship, predator avoidance/deterrence), it remains unclear why there are so many different colors of dewlaps. To try to tackle this question, I am looking at how the evolution of these colors may be influenced by the light environment. Since the reproduction and/or survival of an anole can depend on whether its dewlap is serving as an efficient signal, it’s easy to see how the light environment might determine which colors are favored by selection. For instance, a bright orange dewlap would likely show up much better than a dull green one under the dense canopy of the rainforest, just as a pitch-black dewlap would probably be an excellent signal in a bright, open field. I am testing this idea using an experimental island study in the Panama Canal. My study species is the Panamanian slender anole, males of which can have a mostly orange dewlap or a mostly white dewlap. By introducing these lizards onto a multitude of very tiny, highly variable islands in the canal, I can test which color will “win out” over time in different light environments.

How and why did you start studying anoles?

I have loved reptiles since I was a child, so it was by no coincidence that the very first lab I worked in as an undergraduate had a breeding colony of anoles. While there, I studied physiology and metabolic rates. While I can say that metabolism work is not for me (shout out to the scientists who love it!), I very much enjoyed taking care of and working with the anoles, so I decided to stick with them throughout my undergraduate and graduate career.

What do you love most about studying anoles?

As someone interested in color, I think that dewlaps are anoles’ coolest feature. I love studying anoles and their dewlaps because I am constantly amazed by the astounding amount of diversity in this little flap of skin. In addition, as a researcher, it’s hard to complain about the incredibly high abundance and ease of capture for many of these species.

What is your favorite anole species?

My favorite anole species would have to be the Meyer’s anole, Anolis johnmeyeri (named after the scientist, not the singer). This species, found in Honduras, has an absolutely gorgeous dewlap in both males and females. While large, colorful dewlaps are possessed exclusively by males in many anole species, female Meyer’s anoles have a dewlap that’s almost as large and equally as beautiful. Female dewlaps are bright yellow with a brilliant blue spot, and male dewlaps are bright red with the same blue spot.

Where can people learn more about you and follow you online?

Website: www.colorinnature.org

Instagram: @johndavidcurlis