Meeting Summary: Anolis Evo-devo and Genomics

The Anolis Gene Nomenclature Committee (AGNC) recently held an open discussion regarding our ongoing efforts to develop Anolis as a model system for integrative biology* and genomics at SICB 2012 in Charlestown, SC. To facilitate further discussion from the community I wanted to post a summary of this meeting here. If anyone would like to add to this discussion or propose additional objectives or concerns please leave your comments below. This is an exciting and fast-paced time for Anolis biologists and discussions such as this are necessary to continue the productive development of this genus for research in a post-genomic era.

Ongoing efforts

The AGNC was formed to efficiently develop resources that will be useful to the Anolis research community. We opened the meeting with short presentations about our ongoing resource development efforts. Carlos Infante (UGA) described work from the Menke Lab to develop cell culture protocols that will be used to test transgenic constructs directly in anole tissues rather than distantly related model systems such as the mouse or chicken. He noted that they recently had promising results testing the piggyBac transposon system in cultured anole fibroblasts. Building on her poster presentation Jeanne Wilson-Rawls (ASU) described her experiences isolating and culturing satellite cells – small stem cells found in mature muscles – and her ongoing collaboration with Kenro Kusumi (ASU) studying the mechanisms of tail regeneration in A. carolinensis. Dr. Kusumi described a relatively new project aimed at obtaining genome and transcriptome sequences for A. apletophallus from Panama as part of a collaboration with the Smithsonian Tropical Research Institute (also see this abstract from E. Hutchins). Dr. Kusumi also reminded the audience of their recent release of additional transcriptome data for mid-stage A. carolinensis embryos (available through NCBI).

One of the AGNC objectives is to aid in the dissemination of laboratory protocols, genomic data, and to create a pipeline for integrating data from multiple populations and species (see below). Several web-based resources are now being created along these lines. Tonia Hsieh and Rob Kulathinal (Temple Univ.) concluded this introduction by describing their efforts to develop Lizardbase, a web portal for geographic and genomic data mining. While still in its development phase the portal promises to become a useful tool for the anole research community and its public outreach efforts as data is added. To build this database Drs. Hsieh and Kulathinal are soliciting geo-tagged data for this portal and are in the process of adding a searchable database of contributors.

Looking forward – Goals for 2012

Some anoles from Venezuela

Greetings, Anole Annals readers, from sunny Miami, Florida. For my first post I wanted to share with you an illustration I did of several Venezuelan anoles, which appeared in the latest 2011 issue of Herpetological Review. I thought this illustration would give readers an opportunity to take a peek at the diverse, but often overlooked anole fauna of northern South America.

1.—Anolis tropidogaster (male). This small, little-known anole is somewhat similar in behavior to the species associated with A. chrysolepis. In fact, it is the predominant “not very arboreal” anole in forests west of the Andes in Venezuela, where  A. planiceps is not found. Females have a rudimentary dewlap.

2.—Anolis fuscoauratus (male).

Name That Little Known Anole

Mystery lizard

Here’s a lousy photo of its dewlap, in case that helps.

lousy photo of dewlap

More on the Intriguing Anole of Curacao, Anolis lineatus

Anolis lineatus. Photo by Jonathan Losos

Matt Brandley recently posted on the remarkable anole of Curaçao,  Anolis lineatus, which is notable for having a dewlap that is different on its two sides. Taking advantage of an invitation to participate in a conference in Aruba in January (the travails of life as a scientist), I’ve come to Curaçao to check up on this lizard, which I’ve never previously seen. The dewlap situation sounds remarkable, but there’s a second reason this species is of interest.

Many islands in the Lesser Antilles are home to only one anole species, and the anoles on these islands are renowned for the extent of their convergent evolution to each other and to trunk-crown anoles of the Greater Antilles. Schoener was the first to show that one-species island anoles tend to be remarkably similar in body size, a pattern reaffirmed most recently by Poe et al. The convergence extends beyond size, however, as these species also are very similar in their habitat use (similar to trunk-crown anoles in being arboreal but using a wide range of microhabitats) and their body proportions, such as the length of their limbs and the size of their toepads.

That leads to the question: is this a phenomenon solely of the Lesser Antilles and the two anole lineages that occur there (the bimaculatus Group anoles in the northern half of the island chain and the roquet Group in the south)? Or do solitary anoles anywhere converge on this pattern? Anolis lineatus is a particularly good test, because it comes from a lineage (the chrysolepis species group, about which we will hear more soon) that is not only distantly related to the other two, but is composed of anoles whose habitat and morphology are nothing like those of the solitary anoles.

So, I’m aiming to not only take a peek at lineatus’s throat fan, but also collect data on where it occurs and what it’s morphology looks like. First indications are that lineatus is a chunky anole, not unlike some solitary anoles such as marmoratus or oculatus, but perhaps more similar to trunk-ground anoles than to trunk-crowns.

Habitat-wise, though, lineatus is clearly a surprise—it’s not very arboreal, at least in my day and a fraction of data collection. It’s usually pretty low to the ground, rarely over 1.5 meters high, and often on large rocks or rock walls. More like a trunk-ground anole than a trunk-crown. Moreover, though I’ve been looking for it in the vicinity of human habitations, I’ve yet to see it on a building wall. Bottom line: it’s just not that arboreal.

To be honest, the anole that immediately comes to mind is Anolis gingivinus. This species is a bit hard to categorize: it occurs on some Lesser Antillean islands by itself, but on others it is sympatric with a second species (A. pogus). Moreover, on all islands, it tends to be found relatively low to the ground and not surprisingly, morphologically it’s more trunk-ground-like than typical solitary anoles. Of course, I haven’t actually seen gingivinus in nearly 20 years, so my memory may be faulty.

And we shouldn’t forget the Malice of Nature, which leads me expect to open my door tomorrow and see an anole on the ground, which immediately runs up the wall and out of sight.

By the way, there are other cool lizards here. Lots of green iguanas, for example, but also the very cool and herbivorous Cnemidophorus murinus, endemic to Curaçao and nearby Bonaire.

Cnemidophorus murinus. Photo by Jonathan Losos

 

Anole Visual Ecology, Sans Vision

A riddle: What has four legs, eagle eyes, and can change colors?

Anoles are extremely visual animals, with vision being the primary sensory mechanism through which they perceive their surroundings. Accordingly, their vision is excellent, at least during the daytime. (“Eagle eyes” might be a bit misleading. A more accurate phrase might be “bifoveate retinae conferring excellent visual acuity and depth perception”). The amount of daytime light available for vision depends largely on the vegetative structure in the microhabitat. Indeed, many Anolis species occupy a distinct “photic habitat” due to sun/shade preferences. Variation in photic habitat provides a treasure trove of testable hypotheses for the visual ecologist. Is anole vision adapted to particular light environments? Is dewlap color selected for detectability in a given light environment? And so on.

Two very different photic habitats. (Photographed at approximately the same time of day, same cloud cover).

I totally dig visual ecology, but I’m using it as bait to draw your attention to a closely related (but under-studied) relationship between the light habitat and physiology/behavior. Anoles, like all other animals, use light in ways that do not require visual images at all. These so-called “non-visual” responses to light are used for things like the dilation and constriction of the pupils, the control of circadian rhythms, and seasonal responses to daylength. Non-visual photoreception is processed in the brain through different pathways than those involved in the formation of images, so these responses to light can occur even if the animal is visually blind.

Interesting stuff, but here’s where habitat enters the picture. Non-visual responses to light are irradiance-dependent, meaning that whether or not there is a response, and what the response entails, depends on how much light there is. Bright light, for example, is a wake-up signal to the sleeping lizard, whereas dim light (e.g., moonlight) is less effective in eliciting arousal. However, “bright” and “dim” are relative measures, thus one might expect that the sensitivity of non-visual photoreception would be “tuned” to the overall light levels in the microhabitat. After all, light that seems dim in an open, unshaded habitat might correspond to the brightest midday light available in closed canopy forest. A mismatch between non-visual photosensitivity and habitat irradiance would impair non-visual photoreceptive “performance,” and could even lead to the misinterpretation of photic cues.

In a recent paper published in Journal of Comparative Physiology A, we showed that a non-visual behavioral response to light (the photic induction of locomotor activity) is correlated with habitat irradiance using four species of Puerto Rican anoles (A. cristatellus, A. gundlachi, A. pulchellus, A. krugi). Most diurnal animals respond to light by increasing their activity level. The best way to demonstrate this is to give light when the animal is inactive, i.e., at night. We developed a special device to continuously detect and record anole locomotor activity (walking, running, jumping, etc.) for weeks on end.

Transparent enclosures with a very sensitive movement detector were used to continuously record locomotor behavior.

We quantified baseline activity levels during the day and night, then measured the increase in activity in response to light given at night. Species occupying relatively more shaded habitats were more sensitive to the effects of light (light induced more locomotor activity) as compared to closely related, ecomorphologically identical species occupying more brightly illuminated habitats. The differences were most pronounced at irradiance levels similar to natural twilight levels. This jives well with the notion that dawn is nature’s alarm clock, and that photosensitivity should be tuned to take advantage of morning light, whatever irradiance that may be in a given environment.

Still, there are a few gaps that need to be filled in to complete the story. (You’ll have to read the paper to find out what they are). Non-visual photoecology is still in its infancy, and the main challenge is to develop approaches to explore the links between the environment, non-visual photoreception, and fitness. If anyone’s interested in pursuing variations on this theme, I know a good post-doc for hire.

Species Richness Patterns in Caribbean (and Mainland) Anolis IV

This is the last post (for a while, anyways) about species richness patterns in anoles. Unlike the previous papers and discussions (found here, here, and here), Algar and Losos (2010) zoom out from the Caribbean and take aim at the entire Anolis radiation. 

Islands are often species depauperate relative to mainland settings, likely because their small size makes them difficult to colonize and those species that do make it are more susceptible to extinction. Yet, islands also house many iconic evolutionary examples of adaptive radiation. Algar and Losos (2010) point out that this discrepancy stems mainly from the role that in situ evolutionary diversification plays in these two scenarios. In their paper, Algar and Losos, using anoles of course, explore how in situ diversification on islands affects the relationship between island and mainland species richness.

Anolis (Embryos) Snag Another Cover!

Many editors have recently come to acknowledge that an anole on a book or journal cover generates much enthusiasm from the community (here, here, here, here, here, here and here– I hope that I didn’t miss any). The trend continues in the February issue of Proceedings of the Royal Society. In this issue Sanger et al. describe the developmental bases of limb length convergence among trunk-ground and trunk-crown habitat specialists (previously described on Anole Annals). It should be noted that the only thing that can  possibly trump the beauty and eloquence of an anole in its native environment are developmental series of anole embryos (see here for further proof)

Chromosome Evolution in Anoles: A Study Waiting to Happen

Anole karyotypes from Gorman and Atkins, Herpetologica, 1968.

George Gorman, who pioneered the use of molecular tools to study anole phylogenetics from the late 1960’s to the early 1980’s, asks:

“Why not examine karyotypes of Dactyloa?”

He says:

“In the 1960’s and ‘70’s, before the DNA revolution,  the systematic examination of karyotypes of reptilian taxa mushroomed, and, to some extent helped orient our thinking about relationships among various clades.  This was certainly the case within Anolis at various hierarchical levels,  from species determination to definition of distinct species groups.  To my knowledge, there has been very little added to our knowledge about karyotypes of mainland Anolis that Etheridge placed in the latifrons series of Alpha Anolis,  now frequently referred to as the Dactyloa clade.  (if these are long-lost terms, Etheridge’s Beta anoles are the Norops section; all other lineages are within his “Alpha” section).

Background

There is a very pervasive, either primitive or convergently arrived at, karyotype among the Sauria…consisting of 12 metacentric macrochromosomes, and 24 microchromosomes. This karyotype may be found in many families and in all species of many genera within families. This was also the known published karyotype of A. carolinensis….the only anole that had been examined until about 1965.

Here’s a brief summary of what followed:

Happy Anole New Year

Better late than never.

Winter Anoles: Thermoregulating in the Cold

Braving the elements in Charleson.

We all think of anoles as warm weather, tropical beasties, but of course, that’s not entirely the case. Many live at quite high elevations and are active at cool temperatures. For example, this past summer we saw A. orcesi active (as active as it gets) when temperatures were 20 C and below.

In addition, anoles get relatively far north into temperate areas of the United States. One might think that they’d just go to sleep in the winter and not come back out til the spring warmth, but that’s not the case. Faithful contributor Marc Tollis discusses one recent observation over on his own blog, Anolis Tollis.

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