JMIH 2016: Late-season Lizards Hatch More Quickly and Run Faster

Previous research in the Warner lab has shown that temperature during egg development influences fitness and performance in Anolis sagrei. In particular, a warmer incubation temperature increases sprint speed. The breeding season of A. sagrei spans from March through October, with lower temperatures early in the season and higher temperatures late in the season. Phil Pearson, a masters student in the Warner Lab, conducted an experiment to test whether embryos are developmentally adapted to their incubation temperature. He collected eggs from two temporally-separated cohorts and incubated them under two different temperatures, simulating seasonal temperature differences. He found that late season hatchlings had higher egg survival when incubated under late season temperature. Regardless of incubation temperature, late season embryos had higher sprint speed, larger body size and longer tails. This might compensate for the late start, since they are competing with early cohort individuals in the population.

Late season hatchlings have higher sprint speed regardless of incubation temperature

Late season hatchlings have higher sprint speed regardless of incubation temperature

Overall, this suggests that timing of oviposition has greater effect on morphology and performance than incubation temperature. Future analysis will show whether timing of oviposition affects survival. Phil released the hatchlings on small islands to measure fitness using a mark-recapture approach and will hopefully present his findings at future meetings.

 

JMIH 2016: Jonathan Losos, Distinguished Herpetologist

JMIH

The Joint Meeting of Ichthyologists and Herpetologists (JMIH) kicked off here in New Orleans yesterday. In the morning, Jonathan Losos got started with the first of many anole themed talks. Jonathan gave one the plenary addresses as the Herpetologists’ League’s “Distinguished Herpetologist” of 2016. As such, he joins a long list of accomplished herpetologists, including the first recipient of the honor in 1981, the great anole biologist (and Jonathan’s undergraduate advisor) Ernest E. Williams.

In Jonathan’s talk entitled “Known knowns and unknown unknowns: herpetological progress in fits and starts”, Jonathan started by paying homage to Ernest Williams. He managed to find slides from Ernest’s 1981 plenary address in which the perception at the time of anole biology was compared to a well-built building. All there was to know about anoles was known… or so people thought. In reality, the building looked more like this:

2016-07-07 11.03.34

E.E. Williams slide on the state of anole knowledge from 1981

The metaphorical building at the time was in fact only partially built, with bits and pieces of different areas more complete than others. Jonathan’s talk focused on the fact that despite over 3 decades of progress, so much is still unknown about anoles, including basic natural history of many species. And so Jonathan shared with us a few stories highlighting some surprising anole findings and remaining unknowns, featuring the work of his students from the past 20 years:

Genetic diversity:
One surprise finding over the past 30 years is that several anole species have deep 2016-07-07 11.07.29mitochondrial splits. Anolis oculatus, for example, on the tiny island of Dominica has 4 distinct lineages with as great as 10% mtDNA divergence (Malhotra and Thorpe 2000)! And they aren’t the only ones. Rich Glor and Jason Kolbe really broke this story open with their analysis of several anole species showing multiple mitochondrial lineages for each (Kolbe et al. 2007). This brings into question our estimates of diversity. If every species is actually 4+ species, have we underestimated diversity?

New Species:
According to Jonathan, it seems that the “dawn of anole discovery” peaked in the 1970’s – the last very distinctly different anole was discovered nearly 40 years ago. And yet just last month, Luke Mahler et al. published a record of a new species of anole discovered on the island of Hispaniola! Hispaniola has been intensely studied by anole biologists, making this all the more surprising. In honor of the naturalist that found the species in the wild, the authors named the new species Anolis landestoyi. This new species has a striking appearance, similar to a chameleon and to the Cuban “false chameleons” (Chamaeleolis clade of anoles), and brings up the question of whether there might be a seventh ecomorph.

Anolis landestoyi, photo by D. Luke Mahler

Anolis landestoyi, photo by D. Luke Mahler

Territoriality:
Highlighting the work of two other Losos Lab members, Alexis Harrison and Ambika Kamath, Jonathan talked about how little we know abut anole territoriality. Conventional knowledge says that males maintain polygynous territories and don’t move too far. But Ambika has shown in her dissertation work that male Anolis sagrei actually move quite a bit, and Alexis has shown that male Anolis carolinensis mate with females on opposite sides of their site, not just nearby females! In general, Jonathan commented that there is a large amount of work to be done still on social behavior in anoles.

Anolis proboscis (photo by Luke Mahler)

Anolis proboscis (photo by Luke Mahler)

Basic Biology:
Jonathan talked about the Anole Annals darling, Anolis proboscis. This understudied species sports a large nasal projection of unknown purpose. This odd species was thought to be extinct for many years until it was “rediscovered” only a few years ago. While sexual selection seems like an obvious cause of this structure (the females do not possess horns), its not clear what the males use it for. The obvious hypothesis, that it is used for male-male combat, is easily refuted by video demonstrating that this structure bends easily. Moreover, it appears that they can bend the horn, as seen in this video! The mystery of this structure’s function remains unsolved.

Finally, Jonathan talked about an interesting anecdote: that Anolis agassizi from Malpelo island seems to have a strange preference for the color orange, as described by Rand et al. (1975). Jonathan described a recent test of this preference replicating the Chuckles candy experiment (the experiment has been described here on Anole Annals) and confirming that  this species does, in fact, prefer the colors orange and yellow when it comes to Chuckles candy. He also showed a video of A. agassizi swooping in from afar to eat (attack?) an orange. Why are they so attracted to this color? Sounds like a project waiting to happen.

In short, Jonathan emphasized these two main points:
1. Natural history information is key; you need to know basic aspects of biology and natural history to dig into the deeper questions.
2. There are so many questions to be answered about anoles still, and room for all who want to join the party.

 

 

Anole Adventures in the Cayman Islands

A sagrei on bluff - Cayman Brac NH

A. sagrei on Cayman Brac.

As part of an ongoing study of Anolis sagrei, recently posted about here with additional links therein, I had the pleasure of joining Anthony Geneva and Shea Lambert on a trip to Cayman Brac. We later met up with Graham Reynolds and his undergraduate student Amy Castle on Little Cayman, and closed the trip out with two days on Grand Cayman. Spending time on all three Cayman Islands was a real treat, in large part because of visually stunning anoles like Anolis conspersus and Anolis maynardi. These two species have received a lot of attention on Anole Annals. Rather than rewrite what’s already been written, I’ve decided just to share some pictures from the team. If you’d like to learn more, click on the species names above and explore to your heart’s content. Enjoy!

A conspersus - hotel NH

A. conspersus on Grand Cayman.

A maynardi - Little Cayman SL

A. maynardi on Little Cayman. Photo by Shea Lambert.

Resolving Phylogenetic Uncertainty in Anoles Using Treescape

It’s an all-too-common situation: you would like to infer a phylogeny for a set of organisms, you try a few different methods and you end up with many different trees. Even with the most careful choice of software, settings, tree priors, and the most beautifully converged Bayesian posterior likelihood, you may find that the maximum clade credibility (MCC) tree has low posterior support for certain deep clades.

MCC tree with posterior supports

Anole MCC tree with posterior supports, from Geneva et al. [1]

Tree inference is very complicated, particularly for species trees, and is hampered by factors which include the vast size of tree space, conflicting signals from different genetic loci, confusing signals from convergent evolution, and non-tree-like evolution (recombination, hybridisation, etc.). Geneva et al. experienced just this sort of difficulty when they performed a comprehensive Bayesian phylogenetic analysis of the distichus group of trunk ecomorph anoles [1]. Their MCC tree is reproduced here, and the posterior support values show uncertainty in the branching structure of various deep clades. There are many combinations of ways to resolve these uncertain splits. We wanted to see which alternative trees were supported by the data.

In our recent paper [2] we present a method for handling phylogenetic uncertainty and incongruence. It takes a set of trees and “maps” them into a simple plot where similar trees are grouped together and more different trees are placed further apart. Where many similar trees are clustered together, contour lines indicate the density of points in that region. We began the development of our method theoretically, making sure we had designed a robust mathematical definition for tree distances which would correspond to biological intuition and lend itself to good quality map projections. Then, working closely with biologists, we fine-tuned our method for specific applications with real data and wrote the R package treescape [3] so that anyone can use it – there’s even a handy web app version which requires no knowledge of R.

treescape MDS plot: each point represents a tree, and proximity of points represents similarity of trees. 1000 trees are plotted here, many identical, so contour lines indicate density of points. Colours correspond to clusters of similar trees.

treescape MDS plot: each point represents a tree, and proximity of points represents similarity of trees. 1000 trees are plotted here, many of which are identical, so contour lines indicate the density of points. Colours correspond to clusters of similar trees.

When we applied our method to the trees from the analysis of Geneva et al. [4], we found that there were distinct “clusters” of equally likely tree topologies. It is reassuring that the MCC tree belongs to the largest of these clusters (highlighted on the plot by a yellow triangle), but clearly it cannot represent all of the likely tree shapes on its own. By taking a representative tree from each of the six or so tight clusters, we obtain a more thorough summary of the range of trees supported by the analysis. Such representative trees, taken from the geometric “centre” of each cluster, are credible summary trees with real branch lengths, unlike trees from other summary methods which can suffer from strange behaviour such as negative branch lengths.

We find that there are alternative placements of certain taxa, particularly the ocior, distichus, dominicensis2 clade, and (in our supplement) we explore some of the knock-on effects of using these different tree shapes when analysing the evolution of the anoles, specifically their geographical origins and transitions in their dewlap colour. For instance, we show here a representative tree from each of two different clusters on the map. The trees support ocior, distichus, and dominicensis2 being more closely related to anoles from the East of Hispaniola (the North paleo-island) or the South-West (the South paleo-island) respectively. Both evolutionary histories are supported by the data; in the absence of further research, there is no reason to exclude any of the alternative representative trees identified by our method.

Representative tree from top left cluster

Representative tree from top left cluster

Representative tree from top right cluster

Representative tree from top right cluster

 

 

 

 

 

 

 

 

[1] Geneva, A. J., Hilton, J., Noll, S. and Glor, R. E. (2015). Multilocus phylogenetic analyses of Hispaniolan and Bahamian trunk anoles (distichus species group). Molecular Phylogenetics and Evolution, 87:105-117.

[2] Kendall, M. and Colijn, C. (2016) Mapping phylogenetic trees to reveal distinct patterns of evolution. Molecular Biology and Evolution, first published online June 24, 2016. DOI: 10.1093/molbev/msw124

[3] Jombart T., Kendall M., Almagro-Garcia J., Colijn C. (2015). treescape: statistical exploration of landscapes of phylogenetic trees. R package version 1.9.17.

[4] Geneva A. J., Hilton J., Noll, S. and Glor, R. E. (2015). Data from: Multilocus phylogenetic analyses of Hispaniolan and Bahamian trunk anoles (distichus species group). Dryad Digital Repository.

Anole Hunting in Southern Nicaragua

Fig. 1 Anolis cupreus

Figure 1. Anolis cupreus.

Spending two weeks searching for amphibians and reptiles along Nicaragua’s southern border proved very successful for a band of nature enthusiasts. Accompanied by my primatologist wife Barbara, fellow herpetologist, Joe Furman and his daughter Sadie, and our expert guide Lenin, we visited several nature reserves hoping to observe as many species of herps as possible. Our journey began in Ticuantepe, at the Montebelli Reserve, where we spent our first night searching the forest for any creatures that were out and about. The rainy season had not yet begun and the lack of rain resulted in a paucity of herpetological sightings. We did manage to find a few frogs (Smilisca baudinii and Scinax staufferi), a small fossorial snake (Enulius flavitorques), as well as a sleeping Copper Anole, Anolis cupreus (Fig. 1). Our stay here was brief and the following day we were on our way to the Ecological Center of Los Guatuzos, near the town of Papaturro.

Fig. 2 Anolis limifrons

Figure 2. Anolis limifrons.

The forests here were much more expansive and bordered the Papaturro River. and as a result the abundance of amphibians and reptiles was significantly greater. The river, which ran immediately in front of our accommodations, contained large numbers of Spectacled Caimans (Caiman crocodilus), ranging from yearling size to two meter long adults. At night their glowing orange eyes could clearly be seen scattered throughout the waterway like dim headlights on a busy thoroughfare. On our first night’s outing we observed more than a dozen species of amphibians and reptiles including the iconic Red-eyed Treefrog (Agalychnis callidryas), Fleischmann’s Glass Frog (Hyalinobatrachium fleischmanni) , the giant Smoky Jungle Frog (Leptodactylus pentadactylus), Clouded Snail-eating Snake (Sibon nebulatus), and two species of anoles: Slender (Anolis limifrons  Fig 2.), and the Neotropical Green Anole (Anolis biporcatus  Fig 3.).

Fig. 3 Anolis biporcatus

Figure 3. Anolis biporcatus.

Fig. 4 unidentified white anole

Figure 4. ???.

The following night we came upon an almost white-colored male anole (Fig. 4) sleeping on a leaf some two meters above the ground that we couldn’t readily identify. We realize that many anole species have different body color and patterns at night than they do during the day, so we decided to check the dewlap to see if that might help us render a positive identification. The dewlap was mostly light in coloration with several dark green spots scattered throughout (Fig. 5). Despite this characteristic coloration, the species remained unknown to us.

Fig. 5 dewlap of unidentified white anole

Figure 5. Dewlap of unidentified white anole in Fig. 4.

Figure 6. Second unidentified white anole.

Figure 6. Second unidentified white anole.

Fig. 7 dewlap of second unidentified anole

Figure. 7 dewlap of second unidentified anole.

Shortly after finding this anole, another unidentified white anole was observed (Fig. 6) however, this one had a bright orange-colored dewlap (Fig. 7).

Our final destination took us up the Rio Bartola to the Reserva Naturale Indio Maiz. Like our previous sites this one had large, expansive forests with no other visitors anywhere in the vicinity. Fortunately, the rains had now begun and we were treated to a greater diversity of wildlife including more than two dozen species of amphibians and reptiles. Perhaps due to the onset of the rains or maybe because this reserve is naturally abundant in snake fauna, we ended up seeing more than a dozen serpents in just a few days time. Most notable among them was the seldom seen White-headed Snake, or Panda Bear Snake (Enuliophis sclateri  Fig 8), a small fossorial species known from only four other individuals from Nicaragua.

Figure 8 Enuliophis sclateri, White-headed Snake

Figure 8 Enuliophis sclateri, White-headed Snake

Figure 9. Anolis capito

Six species of anoles were found here including the mossy-looking Anolis capito (Fig. 9), the Slender Anole (Anolis limifrons), the Lion Anole (Anolis lionotus  Fig. 10), of which several were observed during the day on rocks in a shallow stream as well as at night on thin branches overhanging the waterways, a species we were unfamiliar with but which our guide identified as Anolis  quaggulus (Fig 11).

Australian Cryptoblepharus: Convergence across a Continent

When it comes to adaptive radiations, the diversification of Anolis is one of the most striking examples. While Anolis is therefore a well-known rock stars in the league of adaptive radiations, in this blog post I would like to introduce you to one of the mere mortal examples; skinks from the genus Cryptoblepharus.

Cryptoblepharus skinks (“Cryptos”) are small diurnal lizards that have rapidly diversified and are known for their widespread distribution with species present in the Malagasy region, on the Australian continent and on many island archipelagoes in the Indo- and wider Pacific. Furthermore, species that occur on similar substrates are notoriously difficult to identify based on morphological characteristics and a more accurate estimate of species diversity has only recently been accomplished using a widespread genetic screen with allozyme markers (Horner & Adams, 2007).

Distribution of Australian Cryptoblepharus and the three habitat specialists. (a) Topographic map of Australia with the mean point of each species’ distribution plotted and coloured according to habitat type (for complete distribution maps, see Horner & Adams (2007). In situ photographs of (b) arboreal, (c) littoral, and (d) rock specialists (green, blue, and red dots on the topographic map, respectively).

Distribution of Australian Cryptoblepharus and the three habitat specialists. (a) Topographic map of Australia with the mean point of each species’
distribution plotted and coloured according to habitat type (for complete distribution maps, see Horner & Adams (2007)). In situ photographs of (b) arboreal, (c) littoral, and
(d) rock specialists (green, blue, and red dots on the topographic map, respectively).

Whereas species within the same habitat are highly cryptic, species that occur on different substrates (‘rock’, ‘trees’ or ‘beaches’) are relatively easy to distinguish. Rock Cryptos for example, traverse the red sandstone escarpments that are iconic for the Australian outback (think ‘Uluru like’ in terms of color and rock type) and they look very different from Cryptos that occur in a more mesic or coastal habitat. In a recent paper (Blom et al., 2016) we focused on the Australian radiation and explored whether habitat specialization explains current patterns of phenotypic variation in ecologically relevant traits. Using a comparative approach, we quantified the presence of distinct adaptive peaks, the frequency of shifts between such peaks and ultimately discuss the role of ecology in promoting continental radiation.

Anolis Photos from Cuba: ID Help Needed

Anolis_rubribarbus-5

I spent a few weeks on Cuba in February-March, and photographed a bunch of different anoles, but I have no way of identifying them. I put all photos on one page with very tentative captions. I’ll appreciate any comments/corrections.

Here are some of the uncertain ones:

1.

2.

3.

4.

5.

Brown Anoles Invade New Orleans: What Will Happen to the Greens?

Just in time for the American Society of Ichthyologists and Herpetologists meeting in New Orleans next week. From the New Orleans Advocate:

It flashed across the walkway like a lightning bolt, so fast that Bob Thomas had to do a double take. In that split second six months ago, he knew they had finally arrived.

“I’d been waiting for them to arrive in my neighborhood in Metairie. What I saw moved too fast for what we’re used to around here,” said Thomas, a herpetologist who taught at Loyola University and served as the founding director of the Louisiana Nature Center.

“It could only be one thing: a brown anole, Anolis sagrei.”

You’ve seen them — the speckled brown lizards that come out of nowhere and streak across the sidewalks. They travel in hordes — tiny, large and everything in between. Careful! You’re liable to step on them if you don’t pay attention.

Thomas’ neighborhood is far from being the first to experience an invasion of brown lizards. But where did they come from? Why are they so plentiful?

“Brown anoles are an invasive species, not native to the United States,” said David Heckard, curator of reptiles and amphibians at the Audubon Institute. “They are natives to Cuba and the Bahamas and first appeared in the U.S. in Florida. From Florida, they’ve been slowly expanding their range across the Gulf Coast. They’re aggressive and competitive and have even been spotted in Taiwan. They hitch rides on plants and are spread inadvertently by plant nurseries.”

The brown anole looks a lot different than the sleek green lizards we grew up with here in New Orleans (Anolis carolinensis). Generally, A. sagrei has a more compact physique and a shorter skull. A prominent hump appears where muscles attach at the back of the skull. When the brown anole extends its orange and red dewlap (the skin flap below its chin), it looks ferocious, indeed.

By contrast, the green anole looks far friendlier, even when its rosy-hued dewlap is extended. Native to the southeastern parts of the United States (although DNA studies suggest they originated in Cuba and came here a couple of million years ago), green anoles range as far north as North Carolina and as far west as Austin, Texas. They have delicately shaped heads and long, lean bodies. They were once plentiful in New Orleans, but sightings are becoming rare.

So, are the brown anoles killing off the green anoles, fighting over territory and winning? Consuming the green anole’s food supply?

“The theory is that the brown anoles are displacing the green anoles but not necessarily replacing them,” Heckard explained. “It’s believed that green anoles are more arboreal than brown anoles, which are more terrestrial. So, green anoles are being pushed to higher elevations — up into trees and the like. It may seem as though there are fewer of them, but they’re present — you just can’t see them hiding in the leaves and up in trees.”

Simon Lailvaux, a professor in UNO’s department of biological sciences, has studied anoles since working on his doctorate and supports the displacement theory.

“In the Caribbean, where there are dozens of species of lizards, they have learned to partition the habitat and have evolved to live in a specific part of it,” Lailvaux explained. “Green anoles there are trunk/crown inhabitants, whereas brown anoles are trunk/ground inhabitants. Over the millions of years that green anoles have been in the United States, they evolved to be able to occupy the ground because they didn’t have any competition for it. So, the relatively recent invasion of brown anoles has simply forced them back up into trees where they originally lived.”

Are we sure about that? Is anybody counting?

“How can you count green lizards way up on tree trunks and in the leaves at the crowns of trees?” answered Lailvaux. “You can’t.”

According to all three scientists, both types of anoles eat the same things: insects and other invertebrates. There are plenty of those to go around here, so it’s improbable that the green anole’s food supply is in jeopardy. Luckily for the green anoles, they may have a significant competitive advantage over the invaders.

“Brown anoles are cold sensitive and can survive only in a limited temperature range. That means the population of brown anoles crashes when we get a hard freeze, and it takes forever for their numbers to recover,” Lailvaux said. “The green anole, on the other hand, has evolved to be able to withstand lower temperatures, so they won’t be bothered by a freeze. We’re seeing, though, that it is taking less and less time after a freeze for the brown anoles to recover, which means they’re already beginning to adapt.”

The mild winters of the past few years may account for the explosion in the visibility of the brown anoles. But if A. carolinensis is being replaced (not merely vertically displaced) by A. sagrei, it would be a case of a native species dying out because an invasive species outcompetes it. Should we be looking into how to reverse that trend?

“The green anole may be a nostalgic favorite, but we don’t know yet what impact the proliferation of the brown anole will have on it or on other species. The sense is, however, that it won’t be wonderful,” Thomas said.

We know too well what an invasive species can do: Witness the nutria. By consuming the marshes, the animals not only reduced storm surge protection for our area but caused the demise of other species that called the marshes home, Thomas pointed out. Without further study, there’s no way to predict if the success of the brown anole could be similarly dire for the green anole and for biodiversity.

Anole Fabric

anole fabric 2

I’m not sure I like anoles being referred to as “ditsy,” but here’s a great opportunity to create lovely anole-wear, not to mention anole curtains, anole quilts and all kinds of other anoliana.

anole fabric

Prince of Thar–Sands of Time…

An adult nipping grass in the morning; notice the bluish tinge on the inner side of the thigh and dorsal part of tail.

An adult nipping grass in the morning; notice the bluish tinge on the inner side of the thigh and dorsal part of tail.

Here is Saara hardwickii , spiny tailed lizards. I observed these lizards in their natural habitat, in the Thar desert in Indian state of Rajasthan. It’s a medium-sized lizard which dwells in semi-arid to arid landscapes of northern India, Pakistan and some regions beyond. A drab colored lizard with a pug head and a distinct fleshy and spiny tail.

Habitat fragmentation and hunting for its tail is the main reason for its dwindling numbers. Folklore has it that its tail has aphrodisiac powers, so its tail is cut and ‘oil’ extracted from it and consumed for the intended purpose.

Interestingly, like iguanas, these lizards also live in a social structure, a ‘society’ composed of adults as well as young ones. They live in ground burrows or termite mounds. Spiny-tailed lizards are diurnal; their activity starts around early morning sun and when the sun sets, surprisingly not even a single individual can be seen! A considerable ontogenic shift in dietary inclination towards herbivory can be seen. Adults feed on grass or diminutive terrestrial flora, whereas young ones are omnivorous, feeding on arthropods.

This fellow was just out of its home and carefully observing its habitat.

This fellow was just out of its home and carefully observing its habitat.

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