Anole Annals

A view across Conception Island from the North.

Female A. sagrei

As part of our saga chasing Anolis sagrei around the Caribbean, we had the incredible fortune to visit the remote Conception Island Bank in the Bahamas. Conception Island and its associated small satellites are situated on their own bank, adjacent to Long Island which occupies a southeastern edge of the Great Bahamas Bank. Conception Bank and all its satellite islets are protected by the Bahamas National Trust as a National Park, and the bank is presently uninhabited though there is some history of human habitation in the past. Conception Island is quite small, totaling only 9 km by 2 km and has never been connected to any other island banks, meaning that the plants and animals here have almost certainly arrived via dispersal. Though located only 25 km ENE from the northern tip of Long Island, the 2400 m deep water and strong NW currents mean that the Conception Bank has a relatively depauperate terrestrial fauna owing to the vicissitudes of over-water dispersal. For example, in the latest comprehensive list of island herpetofaunal records, Long Island boasts 16 native extant species of reptiles and amphibians, relative to just five on the Conception Bank. Granted, this is potentially owing to lower sampling effort on Conception, as it is a remote, difficult, and expensive place to conduct extensive surveys. Indeed at least one record, that of the Bahamas Boa Chilabothrus strigilatus, is poorly documented and probably spurious.

An unusual dewlap color for A. sagrei

Alberto Puente-Rolon (UIPR-Arecibo), Anthony Geneva (Glor/Losos labs), Nick Herrmann (Losos Lab), and Kevin Aviles-Rodriguez (Kolbe/Revell labs) traveled with me to the Conception Bank aboard the Golden Bear out of Stella Maris, Long Island for two days in July 2015. Our goal was to sample Anolis sagrei from the bank, as well as generally conduct herpetofaunal surveys. We were particularly interested in verifying and attempting to build upon the last report of a herpetofaunal survey there (Franz and

Male Anolis sagrei displaying a light orange/ yellow dewlap in coastal palm scrub habitat.

Buckner 1998). While we expected Anolis sagrei to be present (it was), we also thought that the lack of a record for Anolis distichus might not stand up to our surveys. Alas, we checked multiple habitat types both day and night, from beach scrub to mature forests to mangroves and failed to turn up A. distichus. Though present on nearby Rum and San Salvador Banks (as well as Long Island), this species is curiously apparently absent from Conception.

Happily, we did find Anolis sagrei in abundance, and with some unusual features to boot. For one, the largest males are really quite large, tipping the scales at over 7 grams. Many males sported tall tail crests, and in the coastal scrub habitat, their yellowish dewlaps, combined with large size and tail crests, gave them an overall appearance very similar to Puerto Rican Crested Anoles (A. cristatellus). Interestingly, dewlaps in the forest appeared more traditionally sagrei-red, so we will see what our spectrometer and photographic data tell us about dewlap color variation on the bank. We will continue to update AA on our work with A. sagrei in the Bahamas.

Male Anolis sagrei with a large tail crest.

Kevin and Nick at work

Ragged Island, Bahamas, Lizard Research

By Graham Reynolds

On August 2, 2015

In Notes from the Field

Air approach to Great Ragged Island

We have been on the move quite a bit for our project on Anolis sagrei. On a recent trip to the Bahamas, Alberto Puente-Rolon (UIPR-Arecibo) and I were able to visit the remote Great Ragged Island, located at the southeastern edge of the Great Bahamas Bank only 115 km from the coast of Cuba. Great Ragged is the only inhabited island in the Ragged Island/Jumentos Cays range, a necklace of islands stretching in a sweeping concave arc from Long Island and the southern Exumas to the range terminus at Little Ragged Island. A mere 70 or so people live on Great Ragged, concentrated in Duncan Town, a small settlement perched atop a surprisingly high hill overlooking the deep ocean to the east and dark green expanses of mangroves to the west. Duncan Town is picturesque in the authentic Bahamian sense–brightly colored houses are dotted between crumbling ruins dating back a century or more. Chickens cover yards, and old stone walls snake from the town out into the bush. An artisanal and on-demand salt raking operation continues here, and small pyramids of bleached salt dot the edges of an expansive salina filled with shallow waters reflecting varying hues of pinks and reds in the morning sunlight.

Duncan Town salina and tropical dry scub habitat

Duncan Town salina and tropical dry scrub habitat shallow waters reflecting varying hues of pinks and reds in the morning sunlight. Photo by Alberto Puente.

Anolis smaragdinus from Ragged Island. Photo by Alberto Puente

The Anolis sagrei here are, as in most locations, abundant. We had great success locating them at night, where they sleep exposed on branches and reflect a pale glow in the beam of a headlamp. We sampled anoles from different habitat types on Great Ragged, including coastal Cocoloba uvifera stands, mangrove forest, stunted closed canopy tropical dry forest (where we had to crawl to make our way through), and highly disturbed goat pasture. We are excited to see how the population here compares to the rest of the range. In particular, we are wondering whether the sagrei on Great Ragged belong to the eastern or western Bahamas genetic lineage, which we have uncovered in previous work. The A. distichus here certainly resemble the populations in the western Bahamas, rather than the eastern Bahamas, to which Great Ragged is connected by the Jumentos Cays. We will follow up on these distichus observations in a later post. I will keep AA updated on what we find as we begin analysis of our data.

Anoles Talks at SSAR 2015

By Jonathan Losos

On July 30, 2015

In All Posts

A little while ago, Alexis Harrison asked why there were so few anole talks at the ASIH meeting in Reno. Now we know the reason–they’re all at the SSAR meeting in Lawrence, Kansas, which began today. In total, there are 13 anole presentations (talks plus posters). You can find them in the Meeting Program (also available at meeting website)–just search for “anol” (11) or “Norops” (2).

At the moment, we have no one lined up to provide first-hand reports from the meeting. If any readers out there are at the meeting and want to report in, we’d very much appreciate it!

Anole Annals Turns a Million

By Jonathan Losos

On July 29, 2015

In All Posts

While no one was looking, AA welcome it’s one millionth page view last Thursday, four years in the making. Here’s to the next million!

20-Million-Year-Old Fossils Reveal Ecomorph Diversity in Hispaniola

By Emma Sherratt

On July 27, 2015

In Anole Videos, Lizards in an Evolutionary Tree, New Research

Twenty exquisitely preserved anole fossils in 20 My old Dominican Amber have been reported on in a paper out in Proceedings of the National Academy of Sciences (PNAS) this week.

Previously on AA, I reported that the search was on to find anole fossils in order to piece together the anole family tree. We were extremely fortunate to find in the end 38 amber fossils with anole inclusions, sourced from museums such as the Staatliches Museum für Naturkunde Stuttgart, Germany, American Museum of Natural History, and Naturhistorisches Museum, Basel Switzerland, as well as from generous private collectors.

All of the fossils were exquisite, stunningly-preserved anoles in Dominican Amber. Sometimes just a foot or tail was preserved, sometimes a whole limb or two, or an isolated head, but occasionally a whole lizard was preserved laid out as if it has been pressed into resin just moments before.

Modified from Figure 1 of Sherratt et al. 2015 PNAS.

Using micro-CT scanning to peer inside the fossils, we were delighted to find well-preserved skulls and skeletons. We were surprised to find that many of the amber pieces had air-filled pockets representing where the lizard body had once been (but subsequently mostly rotted away), and the scales had left their impression on the amber. This allowed us to view the scales of the limbs and toepads in the greatest of detail.

The forelimb lying atop belly scales of a trunk-ground fossil, specimen M of Sherratt et al. 2015.

Twenty of these fossils were complete enough, or preserved with the right body parts (limbs with a pelvis, or toepads with countable lamellar scales) to study qualitatively. I micro-CT scanned 100 modern specimens from the Harvard MCZ collection, representing adults and juveniles of all the ecomorphs in Hispaniola. With these data, I build up a dataset of measurements of the limbs, skulls and pelvic girdles that could be used to compare with the fossils. Working fossil by fossil, I used discriminant function analysis to assess the probability that the fossil matched each of the modern ecomorphs.

The fossil twig anole, from Jose Calbeto of Puerto Rico.

The results were very exciting. We found evidence for four of the six ecomorphs in the amber. Trunk-crown were the most abundant, but there was also one that fell within the twig anoles, two that fell with trunk and two with trunk-ground anoles. Not all the fossils could be assigned to an ecomorph with high probability. Though, my gut feeling is that there is a second twig anole (specimen P) based on the distinct few lamellar scales on its widely-expanded toepads, but sadly it didn’t have enough skeleton and no hind limbs preserved to add to the analysis.

We didn’t find any fossils that resembled crown-giants or grass-bush anoles. Why?

Sexual Dimorphism in Asian Big-Nosed Lizards and a New Lizard Species Named after David Attenborough: the Whiting Lab Hard at Work

By Jonathan Losos

On July 26, 2015

In All Posts

Introducing Platysaurus attenboroughi

David Attenborough, fascinated by flat lizards.

Martin Whiting’s lab at the University of Macquarie has been very busy of late. In a single day, I received notice of two new, fascinating papers.

First, Whiting and colleagues described a gorgeous new species of flat lizard (Platysaurus) after Sir David Attenborough. Enough said. Read all about it in Zootaxa or on the Whiting Lab website, The LIzard Lab.

The second paper, available online in Biological Journal of the Linnean Society, concerns a topic near and dear to Anole Annals: lizards with projections on their noses. We’re particularly hung up on horns (1,2), but some species have rostral blobs. Like the Sri Lankan Ceratophora tennentii. Whiting and colleagues examined this species, finding very little difference between the sexes, although males did have longer heads and bigger nasal projections. However, bite force did not correlate with nose size. What’s going on with the rostral appendages, as well as the color on the throat. labials, and inside the mouth, is unknown. A fascinating lizard worth more study!

Here’s the paper’s abstract:

Measures of physiological performance capacity, such as bite force, form the functional basis of sexual selection. Information about fighting ability may be conveyed through a structural feature such as a rostrum (i.e. horn) or a colour signal and thereby help reduce costly conflict. We quantified sexual dimorphism in key traits likely to be the targets of sexual selection in Tennent’s leaf-nosed lizard (Ceratophora tennentii) from Sri Lanka, and examined their relationship to bite force and body condition. We found body length and bite force to be similar for males and females. However, head length was significantly greater in males and they had significantly more conspicuous throats and labials (chromatic contrast and luminance) than females. Males also had a proportionally larger rostrum, which we predicted could be an important source of information about male quality for both sexes. Rostrum length was correlated with throat chromatic contrast in males but not females. Nonetheless, the rostrum and aspects of coloration did not correlate with bite force or body condition as we predicted. We have no information on contest escalation in this species but if they rarely bite, as suggested by a lack of difference in bite force between males and females, then bite force and any associated signals would not be a target of selection. Finally, males and females had similar spectral reflectance of the mouth and tongue and both had a peak in the ultra-violet, and were conspicuous to birds. Lizards only gaped their mouths during capture and not when threatened by a potential predator (hand waving). We hypothesize that conspicuous mouth colour may act as a deimatic signal, startling a potential predator, although this will need careful experimental testing in the future.

Condition Dependence of Sperm Morphology in the Brown Anole

By Ariel Kahrl

On July 23, 2015

In New Research

When I was first designing projects for my dissertation, a result from one of my advisor’s papers caught my attention – brown anole males in better body condition (relatively more massive for their body size) sired more offspring and more sons. We didn’t have an explanation for how or why this trend existed but as a wannabe sperm biologist, I was immediately suspicious that it had something to do with sperm quality. I had some preliminary data showing that brown anole males varied in their sperm morphology and sperm count, but I wanted to know if some of this intraspecific variation was due to condition dependence and if there were fitness consequences associated with this variation.

Male brown anole in St. Augustine, FL.

In our recent experiment, we tested whether body condition was correlated with sperm quantity and quality, and whether the variation in sperm traits resulted in differences in a male’s competitive ability. To do this, we placed two groups of males on high-intake and low-intake diet treatments, where males were fed either five crickets three times a week or one cricket three times a week to experimentally alter their body condition. They were fed this diet until the two groups diverged in condition, and then kept on the diet treatments long enough for them to develop a fresh batch of sperm while in this altered body condition. We collected a sperm sample and measured sperm count and the morphology of 25 cells for each male. We focused on measuring the three largest regions of the cell, the head, the midpiece and the tail (see image below). To test for differences in the ‘competitiveness’ of each group’s sperm, we designed reciprocal mating trials so that a pair of males (one male from each group) would compete for fertilization of a female’s brood. Each male pair was mated to two females, and the order in which the males mated with the female was reversed for the second female to account for mate order effects.

Figure 2 from Kahrl and Cox 2015, (A). Anolis sagrei sperm cell B. Individual means (±SD) for head length, midpiece length, and tail length of 25 sperm cells per individual for each of 17 males from each treatment group (high- and low-intake). (C) Treatment means (± standard error) of individual means in head length, midpiece length, and tail length. (D) Treatment means (±SE) of individual CV in head length, midpiece length, and tail length.

To complement this lab study, we collected sperm from a wild population of brown anoles to look for condition dependence of sperm morphology in the wild. We also reanalyzed paternity data from Cox et al. 2011 to test for condition-dependent reproduction in a lab population of brown anoles. It should be noted that the lab population in this study (Cox et al. 2011) differed from our experimental population in a few ways. First, the males from that study did not have experimentally manipulated body condition. They were all fed the same diets, and the pairs of males that contained both a male in naturally high-condition and low-condition were included in this analysis. Secondly, though the mating design in that study was the same as our experimental reciprocal design, in Cox et al. 2011 males were allowed unlimited access to the females for an entire week, where in our experimental study males were limited to a single copulation.

Figure 4 of Kahrl and Cox 2015. Mean (± standard error) proportion of progeny sired by males that were (A) categorized into high- and low-condition pairs (data reanalyzed from Cox et al. 2011) and (B) assigned to high-intake and low-intake diet treatments. Condition dependence was assessed in 3 ways: 1) using each dam as a unit of observation and estimating the proportion of paternity for each of her 2 mates, 2) using each pair of potential sires as a unit of observation and estimating the proportion of paternity for each male, and 3) using each pair of potential sires as a unit of observation but restricting the comparison to the subset of pairs for which both dams produced offspring.

We found that in both the lab and field, males in low body condition or on a low-intake diet treatment had significantly larger and more variable sperm midpieces than males in high body condition. We also found that males on the low-intake diet treatment had significantly lower sperm counts. When we analyzed the paternity data to test for correlations between fertilization success and sperm traits, we found significant negative correlations between sperm head and midpiece length, sperm count and fertilization success (though it should be noted that we only found these correlations for the average proportion of paternity and not when males were analyzed by either the proportion of paternity from their first or their second mating). We tested for condition-dependent fertilization success in our experimentally manipulated population and reanalyzed the data from males who varied naturally in body condition from Cox et al. 2011. We found a significant difference in fertilization success in males who varied naturally in body condition and had unlimited access to females, but found no difference in fertilization success in males who were in the experimental diet treatment groups (though the trend was similar in our experiment). Together, these data suggest that condition-dependent fertilization success is partially mediated by sperm quantity and morphology, and may also be influenced by a male’s ability to mate multiply with the same female.

This is the first paper that is part of my dissertation on the evolution of sperm morphology. I’m using anoles and phrynosomatid lizards to assess the sources and consequences of inter- and intraspecific variation in sperm morphology. Hopefully I’ll have more to share about anole sperm biology soon!

Kahrl, A.F., and R.M. Cox. 2015. Diet affects ejaculate traits in a lizard with condition-dependent fertilization success. Behavioral Ecology (advance access).

ASIH 2015: Biogeography of Central American Anoles

By Jonathan Losos

On July 21, 2015

In All Posts

AA‘s correspondent in the West Coast Bureau, Alexis Harrison, just filed this report from Reno:

At the Joint Meeting of Ichthyologists and Herpetologists in Reno, Nevada this week, the most surprising news for an anolologist may be the lack of presentations focusing on anoles. Given the ubiquity of anoles in ecology and evolutionary studies, I’ve come to expect a steady stream of anole presentations and posters, anole discussions, anole-themed paraphernalia and other anole-centric events. Maybe I’ve been living too much in an anole-shaped bubble.

The sole anole-focused talk was a presentation by Kirsten Nicholson (with co-authors Craig Guyer and John Phillips) entitled “Biogeography of Central American anoles in the genus Norops”. In this talk, Nicholson et al. explore biogeographic hypotheses developed in their 2012 paper in greater detail, with a particular focus on the timing and geographic context of diversification in the Norops clade. Current and ongoing work incorporates the addition of several new species and greater sampling of widespread species into the phylogeny. Although the results presented were preliminary (mitochondrial sequences are already available, with nuclear sequence data to come), the broad patterns in the data appear to be consistent with the conclusions from the 2012 paper: the estimated divergence times among three subclades of the Norops group are ancient, in the range of 40-50mya, while a reconstruction of the ancestral range of the Norops group suggests an early colonization of South America followed by re-expansion northward and then back south.

Regular readers of Anole Annals will probably remember the vigorous debate occasioned by the publication of Nicholson et al 2012. Based on this latest research, I think we can expect further provocative papers and ensuing discussion in the near future. Let’s hope this will stimulate more Anolis talks at next years JMIH meeting in New Orleans!

Evolution 2015: Population Divergence in Anolis meridionalis

By Jonathan Losos

On July 19, 2015

In All Posts

Anlolis meridionalis. Photo from the Reptile Database

Recently, Kristin Winchell reported on the 2015 Evolution meetings in Guarujá, Brazil. Kristin noted: “Fernanda de Pinho Werneck gave a lightning talk titled “Cryptic lineages and diversification of an endemic Anole lizard (Squamata, Dactyloidae) of the Cerrado hotspot” that I am sad to have missed. If anyone did catch it, please let us know in the comments.”

Well, Fernanda herself responded and summarized her talk: “Hi Kristin, really cool summary of the Anole talks! Here is what I presented at the meetings for Norops meridionalis lighting talk: we found five highly divergent lineages, confirmed by multiple phylogenetic and species delimitation methods. These lineages (potential candidate species) diverged in the early-mid Miocene, when most of the geophysical activity of the Cerrado took place. Population-level analysis for the broader distributed lineages showed evidence for non-stationary isolation by distance, when the rate at which genetic differentiation between individuals accumulates with distance depends on space. Finally, niche conservatism, rather than niche divergence, seems to be the main mechanism that promoted the fragmentation of main populations across the Cerrado. Cheers!”

Fernanda also pointed out that the work is the basis of a paper by Carlos Guarnizo et al. that is in revision at Molecular Phylogenetics and Evolution. We’ll hear more when the paper appears!

Studying Lizard Behavior with Lizard Robots

By Jonathan Losos

On July 16, 2015

In All Posts

Researchers have previously shown that anoles and other lizards will respond to moving robot lizards. In a recent elegant study in Herpetologica, Joe Macedonia and colleagues have used such robots to investigate what aspects of a lizard’s body or behavior are most important in eliciting responses. The work was conducted in Bermuda, where A. grahami and A. extremus were introduced from Jamaica and Barbados, respectively, in the first half of the last century.

Macedonia and team built robots to look like these two species. It’s worth reading the details of how they built these realistic looking models: “We constructed a conspecific robot body and dewlap to resemble our study species, A. grahami, as well as a heterospecific robot body and dewlap to resemble A. extremus. Excluding the hind limbs and tail of each robot, which were made of airbrushed latex cast from lizard specimens (see Macedonia et al. 2013), each robot body was carved from a thick wooden dowel and attached to a servomotor pushrod. Anterior to the hind limbs, robots were covered with an image created in Adobe PhotoshopH from photos of the study species (Fig. 1). These images were mirrored and joined together at the body midline. Final images were printed onto adhesive-backed fabric and molded around the wooden body, which, together with the latex hindquarters, was attached to the polyvinyl chloride (PVC) perch. Dewlaps were fashioned from white, semitransparent guitar picks that fit into a slot carved in the neck of the robot body. A small hole that was drilled into the guitar pick was secured to a hinge pin that allowed it to pivot and extend. A second small hole in the pick allowed insertion of a thin wire that was attached to the pushrod, which in turn was attached to a servomotor.” The researchers were able to tune two servomotors to produce dewlap extension and head-bobbing patterns similar to those produced by each species. The following movies illustrate what the robots looked like.

In the first experiment, wild A. grahami were presented with robots in the following four treatments: grahami color and grahami display patterns; grahami color and extremus display patterns; extremus color and grahami display patterns; and extremus color and display patterns.

Sixty-seven of 145 lizards responded to the displaying robots, and the strongest response was to the normal-looking grahami. In addition, the lizards dewlapped more to the robot with grahami color but extremus display pattern than they did to either of the robot treatments with extremus coloration; however, in terms of head-bobbing, the grahami did not distinguish between the three other treatments, responding similarly to all three at a lower headbobbing rate than to the normal- looking and behaving grahami robot.

In a second experiment, wild grahami were exposed to robots that looked like grahami and that: bobbed and dewlapped; only bobbed; or only dewlapped. Unexpectedly, they dewlapped the most to the robots that only dewlapped, and headbobbed the most to the robots that only headbobbed.

Macedonia et al. conclude the paper by suggesting that in the future, the best way to further this line of research will be to develop robots that can be controlled in real-time such that the robot’s behavior can be responsive to what the subject lizard does.