Anole Annals

Male Anolis nebulosus

With few exceptions, there has been far less research on the ecology and evolution of anoles inhabiting islands off Central and South America compared to anoles on islands in the West Indies. Siliceo-Cantero, Garcia, Reynolds, Pacheco and Lister (2016) have recently taken a step towards leveling the playing field by making a detailed comparison of a mainland A. nebulosus population residing in the Chamela-Cuixmala Biosphere Reserve in western Mexico, and a population inhabiting the small island of San Agustin in the Bay of Chamela just 5 km from the mainland study site. Their research focused on three central questions: (1) To what extent has the island population diverged morphologically, behaviorally, and genetically from the ancestral mainland population? (2) Does the morphology of the island and mainland populations correspond to any of the six West Indian ecomorphs?, and (3) In the absence of mainland competitors, has the island population undergone niche expansion and evolved towards a generalist phenotype?

Initial analyses of morphology indicated that both island and mainland populations were dimorphic, with each sex in each location having a large-headed, short-limbed morph, and a less common small-headed, long-limbed morph. The only other anole known to exhibit such intra-sexual dimorphism is Anolis agassizi from Mapelo Island, where there are large and small male morphs that also differ in coloration. In keeping with a pattern often found in anoles, island and mainland A. nebulosus morphs showed a significant positive correlation between average size-adjusted upper limb lengths and the mean logarithm of their perch diameters, suggesting that the morphs may be adapted to different microhabitats. Island morphs were also significantly larger than their mainland counterparts, and both the CV and Shannon diversity of the SVL distribution of all four morphs combined were significantly greater for the island population. The authors calculated the area of morphospace occupied by the morphs, as defined by the first two axes of a principal components analysis based on several morphological characters. On both island and mainland, the existence of a second morph doubled the total morphological space of each population. With respect to divergence in shape, mainland male and female morphs had significantly longer snouts and wider mandibles than the corresponding Island morphs. A PCA clearly separated island and mainland males from males of all the West Indian ecomorphs.

Female A. nebulosus

The genetic divergence of the island and mainland populations was assessed by sequencing both mitochondrial and nuclear genes. Genetic diversity of mtDNA was low on the island (haplotype diversity (h)= 0.50; nucleotide diversity (π) = 0.0007) relative to the mainland (h= 0.95; π= 0.006), and the populations were fairly divergent (Fixation Index = 0.34). Haplotype diversity of nuclear DNA, however, was somewhat higher on the island (h = 0.38 vs. .32). Based on 16,382 SNPs, island and mainland individuals were grouped cleanly by both Discriminant Analyses of Principal Components and STRUCTURE, a Bayesian clustering algorithm, and had 100% posterior support in STRUCTURE for membership in their respective populations. The authors conclude that these results indicate incomplete lineage sorting in mtDNA, as well as a relaxation population genetics model in which the island population is evolving independently of the mainland population under the influence of drift and lack of gene flow.

While the A. nebulosus population on San Agustin has undergone niche expansion in the absence of mainland competitors, there was no detectable evolution towards a generalist morphology, defined as a hypothetical phenotype intermediate between the shapes of the six West Indian ecomorphs. The authors suggest, however, that this definition is unrealistic given that the selective forces necessary to produce such a Jack-of-All-Trades ecomorph are most likely absent on the small islands harboring solitary Anolis populations. Alternatively, they propose that reduction in death rates, higher densities, increased intraspecific competition, and greater male-male competition for females are the major selective forces common to many small islands. A large body of theory and data indicate that all of these forces can drive the evolution of larger body sizes and greater SSD. The authors point out that Schoener’s work documenting wide-spread convergence in body size and SSD among solitary anoles in the West Indies, supports this hypothesis, and predict that the distributions of body size and SSD on single species continental islands should converge on those found in the West Indies (see Figure below).

A. Distribution of SSD indices for 102 Anolis species from the Greater Antilles. Dark grey bars delineate trunk-ground and trunk-crown ecomorphs. B. SSD distribution for 28 solitary West Indian anoles (data from Schoener, 1977). C. SSDs for 60 mainland species. D. Histogram of SSD for four solitary species including A. nebulosus, inhabiting islands off Central and South America (data for A. concolor and A. pinchoti from Calderon-Espinosa and Barragan-Forero, 2011. Data for A. agassizi from Lopez-Victoria et al., 2011). After Fig. 3 in Siliceo-Cantero et al, 2016.

George Gorman in the field

George Gorman, guru of all things Anolis, writes in:

49 years before Barack Obama’s historic visit to Cuba , I made a historic visit to Cuba but did not visit the Castro brothers, nor was there a baseball game played in my honor. I did, however catch a lot of Anolis,and send a letter to Science about my trip … which was published.”

Read it here.

For those of you following the first ever Anole March Madness, the first eight matches were held on Monday and Tuesday evening live on twitter, taking us halfway through the round of 32!

Just a reminder, no animals were harmed in the making of this production and all matches are entirely fictional. We have done our best to make the battles realistic given what is known about the natural history of the species and their habitat. Of course, we have taken minor creative liberties with some details. We also want to point out that while these matchups are for entertainment, we hope you also learn a little about some of the more obscure anoles. It is also an opportunity for us to point out how little is known about some of these species. Please let us know in the comments if you believe some detail to be inaccurate or you have something to add!

And now, the recaps!

Day 1 was exciting with Anolis insignis versus Anolis nebulosus, Anolis onca versus Anolis macrolepis, Anolis cristatellus versus Anolis pulchellus, and Anolis lividus versus Anolis richardii.

Anolis nebulosus (photo by Cheryl Harleston)

Anolis insignis (photo by Shawn Mallan)

Anolis insignis versus Anolis nebulosus
High in the treetops of Mexico perches the diminutive clouded anole, Anolis nebulosus. A loud rustling of leaves announces the arrival of the massive crown-giant, Anolis insignis. The lizard, famished from his travel from Panama, spots the tiny A. nebulosus and decides he looks like a tasty snack. He slowly ambles across the canopy towards his meal, pauses, then lunges with mouth agape. The agile A. nebulosus leaps to the side, narrowly avoiding the cavernous mouth. Anolis nebulosus watches with curiosity as the striped giant slowly turns toward him, preparing his next attack. Again, A. insignis lunges towards his hopeful meal and again A. nebulosus narrowly avoids being consumed. Wary of the newcomer, Anolis nebulosus retreats below the canopy, to the lower branches where he spots an attractive female. Foolishly thinking he has escaped the unknown giant in the tree top, he begins to dewlap at the prospective mate. Meanwhile, the hungry Anolis insignis stealthily descends to the lower branches and lunges again at the distracted A. nebulosus. This time he doesn’t miss and consumes the tiny anole in a single gulp. ***Anolis insignis wins***

Anolis (no image)

Anolis macrolepis (photo by fernandocastro)

Anolis onca versus Anolis macrolepis
At the terminal end of the babbling brook, the habitats of two Colombian anoles, Anolis onca and Anolis macrolepus, converge. Following an escaped beetle downstream, Anolis macrolepis leaps from rock to rock over the rushing water. On his last leap he finds himself no longer on a rock, but on soft sand. Here his troubles are much bigger than an escaped meal as he meets the larger Anolis onca, basking in the sun on the sand. Charged full of energy, A. onca confronts the intruder. Anolis macrolepis attempts to turn to flee, but his feet are poorly adapted to run on this strange, hot substrate. He moves his legs frantically attempting to run, but only digging himself into a hole. Now half buried in the sand, A. macrolepis realizes he is in a precarious situation. Anolis onca approaches his competitor and flings sand in his face. Temporarily blinded, A. macrolepis panics. He begins to flail out of desperation as A. onca firmly grabs him and flings him back into the stream where he is carried out to sea. Anolis onca resumes basking in his sandy home. ***Anolis onca wins***

Anolis pulchellus (photo by K. Winchell)

Anolis pulchellus versus Anolis cristatellus
In a patch of secondary tropical forest on the north coast of Puerto Rico, Anolis cristatellus and Anolis pulchellus both enjoy the afternoon, each happily unaware of the other as they occupy distinct structural habitats. The afternoon sunshine begins to wane and A. pulchellus climbs up the side of a tree trunk towards one of the remaining patches of sunlight. Anolis cristatellus suddenly darts around from the other side of the trunk to confront the trespasser. Anolis cristatellus  raises his dorsal crest and stands strong and proud, seeming to grow by almost 2 cm. Anolis pulchellus, with his eye on the prized sunlight, accepts the challenge. He too raises a dorsal crest, dark spots suddenly appear behind his eyes, he sticks his tongue out, and he flashes his large crimson dewlap with confidence. Unfazed, A. cristatellus in turn flashes his bright orange and yellow dewlap and does several pushups as a last warning. Anolis pulchellus does not heed the warning and darts toward A. cristatellus, delivering a sharp blow to his midsection with his pointy snout. Despite the sting of the assault, A. cristatellus manages to bite onto the tail of A. pulchellus. Unable to autotomize his tail, A. pulchellus is swiftly flung from the tree trunk, flying several meters back to his rightful place among the reeds of grass where he decides it prudent to remain, defeated. ***Anolis cristatellus wins***

Anolis richardii (photo Wikipedia)

Anolis lividus (photo Wikipedia)

Anolis lividus versus Anolis richardii
On the tiny isle of Montserrat, Anolis richardii has arrived on a piece of driftwood to make its stand against Anolis lividus. There are perches and food for the taking, and only a puny mid-sized anole to defend them. Anolis lividus has spotted this unwelcome intruder and rushes up the tree to evict him. Unaware of their shared evolutionary history, they are briefly confused when they flash their orange dewlaps and, for a moment, wonder whether they’re the same species. Anolis richardii, massive to begin with, cuts an even more impressive figure with an erected nuchal crest, but A. lividus does not back down. However, the Montserratian anole is no match for the massive A. richardii. Its lunges and parries are met with vicious attacks. Anolis richardii delivers a strong bite to A. lividus’ flank. At that moment, the Souffriere Hills volcanic dome collapses, launching a column of ash and pyroclastic material into the air. Anolis lividus is unfazed by the volcano, but A. richardii is terrified by this ominous neighbor and decides to find fertile ground elsewhere. It abandons the perch and the island, leaving A. lividus in disbelief at his luck and the unexpected victor of this encounter. ***Anolis lividus wins***

Day 2 was equally exciting with Anolis limifrons versus Anolis humilis, Anolis frenatus versus Anolis transversalis, Anolis placidus versus Anolis distichus, and Anolis trinitatis versus Anolis pogus.

Anolis limifrons (photo by Loïc Denès, Flickr)

Anolis humilis (photo by Tobias Eisenberg)

Anolis limifrons versus Anolis humilis
It is early morning in the Costa Rican rainforest. Anolis limifrons has been awake for an hour already, foraging in the leaf litter near the towering buttress roots of a tree. As it plucks a roach into its mouth it freezes. There, not one meter away, is the red and yellow flash of the dewlap of Anolis humilis, a much bigger species. Anolis humilis charges, vying for the insect-rich territory. Anolis limifrons retreats to a crevice in the roots, but then charges back out and and lunges at A. humilis. Anolis humilis is stockier, but slower and less tenacious. Anolis limifrons won’t give up, biting at A. humilis often, displaying, and refusing to back down. Anolis humilis gives one last lunge, but misses, as A. limifrons deftly dodges and swings back around to nip his opponent’s throat. Harangued and weary, A. humilis retreats, leaving A. limifrons to go back to his cockroach feast. ***Anolis limifrons wins***

Anolis frenatus (photo by Tobias Eisenberg)

Anolis transversalis (photo by John Sullivan)

Anolis frenatus versus Anolis transversalis
It is early morning and Anolis transversalis, wide-eyed and nervous, glances around. There are so many things that can eat him here in Amazonia. From above comes an Anolis frenatus, crashing down from the canopy. The crown-giant, startled by his misstep and fall, barely grasps the tree branch as he falls. Swinging upright, he notices he is not alone. Anolis transversalis, petrified that his worst nightmares have come true, turns to run. Anolis frenatus, still confused from the fall, watches as A. transversalis flees frantically, jumping from the branch to an adjacent tree, then to another and another and another until he is out of sight. Uncertain about what just occurred, A. frenatus unknowingly claims victory. ***Anolis frenatus wins***

Anolis distichus (photo by John Sullivan)

Anolis (no image)

Anolis distichus versus Anolis placidus
It’s late evening now on Hispaniola and the placid anole, Anolis placidus, peacefully perches high in the treetop hugging the twig he plans to sleep on tightly with his tiny legs. Anolis distichus, thinking it best to sleep higher up tonight, ascends to what looks like the best sleeping site only to find it occupied by the little twig anole. Anolis distichus, feeling entitled to this perch, strolls up to A. placidus and begins to display his dewlap. Anolis placidus, ever the pacifist, looks at A. distichus with a sidelong glance and decides there is room enough for them both. Anolis placidus sidles to the end of the perch, pressing his body close to the twig. Anolis distichus, upset that his opponent does not accept his challenge, advances and begins to push-up violently, thinking he may shake the twig anole off of the branch. Anolis placidus edges closer to the end, his tiny legs giving him an unshakeable grip. Clearly his friend needs more room to sleep, that’s fine with him, they can share. Anolis distichus, frustrated with his opponent and now struggling to keep balanced on the moving twig decides intimidation is not enough and leaps towards A. placidus, who skillfully moves to the underside of the twig with only two steps. Anolis distichus lands on the edge of the twig but is unable to grip the tiny perch with his longer limbs. As he flails attempting to grab onto the twig and his opponent, A. placidus inches back away from the edge to the top side to avoid contact. Anolis distichus manages to catch the tip of the branch with a single toe, momentarily hanging on before falling to the branch just below. As his toe releases it turns the twig into a catapult and even the powerful grip of A. placidus isn’t strong enough to hold on. Anolis distichus looks up as A. placidus is flung far out of sight. Anolis distichus ascends to his chosen sleep site, pleased with his skillful removal of the competitor. ***Anolis distichus wins***

Anolis pogus (photo by Mark Yokoyama, Flickr)

Anolis trinitatis (photo Wikipedia)

Anolis pogus versus Anolis trinitatis
Aboard floating vegetation following a hurricane that tore through the Northern Lesser Antilles, Anolis pogus patiently awaits making landfall on St. Vincent island. As the flotsam approaches the shore, the weary castaway spots movement in the trees. Flashes of bright green and blue announce the presence of the resident trunk-crown anole, Anolis trinitatis. Anolis pogus disembarks on the rocky shore and wearily climbs up the nearest trunk, basking in the sunlight and surveying his new home. But there will be no rest for the tired traveller, immediately an A. trinitatis descends and sizes up this newcomer. Anolis trinitatis, a good 2cm larger in body size, decides he does not like new, strange looking anole. He angrily advances and grabs A. pogus by the nape of the neck and flings him. “Welcome to St. Vincent” he thinks, hoping A. pogus will choose somewhere else to call home. Suddenly energized, A. pogus climbs up the adjacent tree and begins to dewlap at his assailant, undeterred by his aggression and larger size. Anolis trinitatis leaps to the tree, accepting the challenge. They trade blows repeatedly – A. trinitatis bites at the face of A. pogus; A. pogus leaps and bites off a sizable portion of A. trinitatis’ tail – both sustain substantial injuries in the battle. Now weary himself and impressed with his opponent’s stamina and scrappiness, Anolis trinitatis attempts one last time to disarm his opponent with intimidation, he dewlaps and pushups but his vigor is gone. The bloodied A. pogus returns the threat by advancing and delivering a calculated blow to the throat, tearing the dewlap of A. trinitatis. Anolis trinitatis has had enough and limps away, defeated, back to the canopy to inform the other native lizards that there is a new lizard on the block and that he’s not one to be messed with. ***Anolis pogus wins***

Tune in tomorrow and friday on Twitter for the next matches, and of course we will bring you the recaps here afterwards. Bracket busted already? Did we miss an important detail? Let us know in the comments!

Get ready! Anole March Madness begins with the first battles this evening (Monday 3/21/2016) . We will be live broadcasting the bouts on twitter with the handle @AnolisMM2016 starting at 8pm EDT (Boston time). Tonights matches include: A. insignis v. A. nebulous, A. onca v. A. macrolepus, A. cristatellus v. A. pulchellus, and A. lividus v. A. richardii.

Get your brackets filled out, share them on twitter with #AnoleMM2016, and follow along with the live tweets. We will also be posting the recaps of the battles tomorrow morning here on Anole Annals!

Let the games begin!

A recent paper in Science Advances by Daza et al. reported on 12 amber lizard fossils from Myanmar. First author Juan Daza provided an author’s view of the paper two days ago, but I thought I’d add a little more–mostly some cool visuals and links to reporting in the press–here. Particularly notable were a specimen that appears to be on the evolutionary way to becoming a chameleon and gecko with different toepad structures. You can read nice summaries of the articles in the Christian Science Monitor and the BBC.  Anoles even make an appearance in the nifty figure summarizing what we know about fossil amber lizards (more on amber anole fossils).

A Mid-Cretaeous lizard. This one individual’s long digits earned it the nickname “Nosferatu,” after the long-fingered German movie vampire,

When lizards prove too fast, slippery or downright squirrely to catch using other methods, herpetologists will sometimes turn to glue traps to snare their quarry. This technique is particularly useful when trapping elusive scansorial species (e.g. Bauer & Sadlier 1992, Ribeiro-Júnio et al. 2006), but is also proving useful for those of us who study fossil species. Sticky tree resin provides a naturally occurring glue-trap, and inclusions in fossilized resin, or amber, show that this material has been snaring and preserving small animals for many millions of years. Amber fossils are particularly important for three main reasons. Firstly, they preferentially preserve small, delicate specimens that are rare in the fossil record by dint of being too fragile to survive the fossilization process. Secondly, because they tend to be formed in tropical forested environments where decomposition happens rapidly and deposition is limited, they often contain snapshots of ecosystems that are rare in the fossil record. Finally, they preserve specimens in startling detail, often retaining soft anatomy at a resolution that no other fossilization process is capable of.

The term “Amber fossils” inevitably brings to mind images of frozen mosquitos, stuffed to the eyeballs with DNA-rich dinosaur blood and, while it is true that an enormous amount of arthropod diversity has been recovered from amber fossils, lizards have also been found in fossilized amber, from three continents and across six horizons that span 100 million years. Last year this blog discussed a series of anoles in amber that were featured in an impressive study by Sherratt et al. (2015) which documented the presence of ecomorphs 20 million years ago in the Hispaniola and Mexico. These fossils allow us to see directly into the past, and in the case of anoles, it was possible to document the early morphological diversification into some of the five basic ecomorphs (although, not all of them fitted in such categories).

Earlier this month, a paper in Science Advances revealed the oldest amber lizard assemblage known to-date. This work is the result of teamwork between Ed Stanley, Phillip Wagner, Aaron M. Bauer, David Grimaldi and myself (Juan Diego Daza). We document the remains from 12 lizards that lived 99 million years ago in a tropical forest in an area of what is today Myanmar. Most modern lizards are pretty easy to identify to at least to family level–skinks have cycloid scales, geckos have toepads (not all), lacertoideans tend to have square scales, etc.–so naturally, you start looking for these traits in order to identify these animals. When I learned from my mentor, Dr. Richard Thomas, to use plastic bags in the field to collect lizards, these bags can be labeled and this makes sorting easy after a day of work. I remember the day that when we all met at the American Museum of Natural History with David Grimaldi; he started to bring plastic containers with small amber inclusions. It was like taking a Herpetology exam, and we kept asking each other, “what do you think it is?” You could only hear our wild guesses–gecko, skink, anguimorph, teiid, agamid–but none of us was entirely sure. This is because when these lizards were trapped, they looked very different to their modern relatives.

To determine the identity of these animals, we decided to look deeper, using a combination of light microscopy and high-resolution Computed Tomography (CT) to extract as much data from the specimens as possible.

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Are you ready for March Madness?! No, not the basketball tournament… this year we are staging the very first Anole March Madness! We should acknowledge that we came up with this idea after following the popular Mammal March Madness for the past couple of years and feeling a little left out.

What is Anole March Madness? Just like the basketball tournament, we start with 32 of the best teams from 4 regions. The groups doing battle will be Mainland (Central America and South America) versus Island (Greater Antilles and Lesser Antilles). The rules are simple, if a lizard wins a bout it advances, if it loses it is out of the tournament.

Anole-March-Madness: download this pdf, fill in the text boxes, play along!

Don’t worry, no animals will be harmed in any way during this tournament. In fact, the matches are entirely fictional and come from the imaginations of AA contributors Kristin Winchell, Martha Muñoz, and Pavitra Muralidhar. We will pick the winners of each bout based on what is known about the morphology, ecology, and behavior of each species and will give a full recap of the (fictional) battles every few days.

Do your best to predict the winner of each match, and ultimately the champion! Fill in the empty text boxes in the PDF of the bracket above and pick your winners for each match. Take a photo of your completed bracket and tweet it with #AnoleMM2016 so we can all see your picks! You earn 1 point for each correct match in the first round (round of 32), 2 points in the second round (Sweet 16), 4 points in the third round (Elite 8), 8 points for the fourth round (Final 4), and 16 points if you guess the champion. Keep score and let us know how you’re doing! First matches will be posted in a few days. The Championship match will be on April 4th.

Now, meet the teams!

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A common question is whether green anoles (A. carolinensis) and brown anoles (A. sagrei) can interbreed. I am unaware of any hybrids between the two species, and given their long evolutionary separation, it seems unlikely that they could reproduce successfully. Nonetheless, occasional reports of interspecific matings are made, and here’s another.

Mitchell Gazzia posted this photo on his Facebook page, and provided these details:

Took place in late June of 2012 in Melbourne, the Lake Washington area in Brevard County…very close to the intersection of Lake Washington and Turtlemound roads.

Dewlap morphology and colouration of Fan-throated lizards. Clade 1: A. Sarada darwini sp. nov., B. Sarada deccanensis comb. nov., C. Sitana superba sp. nov.; Clade 2: D. Sitana spinaecephalus sp. nov., E. Sitana laticeps sp. nov.; Clade 3: F. Sitana ponticeriana, G. Sitana visiri sp. nov., H. Sitana cf. bahiri. Scale bar = 10 mm

V. Deepak and his colleagues from five different institutions in India have published a revision of the systematics of fan-throated lizards in India. This work nicely expands on the project of figuring out the diversity of this clade of magnificent lizards, following the description of two new species from Sri Lanka last year.

I’ll be writing more about this paper and these lizards in weeks to come, but for now, here’s a figure from the paper, and below, the abstract!

Abstract

We revise the taxonomy of the agamid genus Sitana Cuvier, 1829, a widely distributed terrestrial lizard from the Indian subcontinent based on detailed comparative analyses of external morphology, osteology and molecular data. We sampled 81 locations spread over 160,000 km² in Peninsular India including type localities, which represented two known and five previously undescribed species. Based on general similarity in body shape and dewlap all species were hitherto identified as members of the genus Sitana. However, Sitana deccanensis and two other morphotypes, which are endemic to north Karnataka and Maharashtra in Peninsular India, are very distinct from the rest of the known members of the genus Sitana based on their external morphology and osteology. Moreover, members of this distinct morphological group were monophyletic in the molecular tree, and this clade (clade 1) was sister to two well-supported clades (2 and 3) constituting the rest of the Sitana. The interclade genetic divergence in mtDNA between clade 1 and clades 2 and 3 was 21-23%, whereas clade 2 and clade 3 exhibited 14- 16% genetic divergence. Thus, we designate a new genus name “Sarada” gen. nov. for species represented in Clade 1, which also includes the recently resurrected Sitana deccanensis. We describe two new species in Sarada gen. nov. and three new species in Sitana. Similarity in the dewlap of Sitana and Sarada gen. nov. is attributed to similar function (sexual signaling) and similarity in body shape is attributed to a similar terrestrial life style and/or common ancestry.