Author: Katharina Wollenberg Valero

Katharina Wollenberg Valero is a Lecturer in Ecology & the Environment at the University of Hull.

Genomic Signatures of Climate Adaptation in Anolis cybotes

Anolis cybotes, female from Barahona, Dominican Republic

Anolis cybotes, female from Barahona, Dominican Republic

Katharina Wollenberg Valero & Ariel Rodríguez

Thermal adaptation is the evolution of the ability to persist in novel thermal environments. Phenotypic characters that allow such adaptation, as well as the resulting shifts in the geographic distributions of species, are an emerging field of study in the midst of a changing global climate. Yet, the genomic basis of such phenotypic adaptation is less well understood, so recent efforts of evolutionary biologists are now aiming at one emerging question: Which genes determine thermal adaptation, and are these the same across different populations and species? Luckily, Anolis is yet again at the forefront of novel discoveries being made in this field (see Campbell-Staton et al., 2017).

Many studies have independently identified genes that are responding to changes in the thermal environment, be it through change of expression under an acute stress, or through changes in the DNA sequence as evolutionary response. In 2014, we gathered information on such thermal adaptation candidate genes from Drosophila to Homo sapiens from the literature.

From the published evidence, we extracted a set of gene functions that potentially underlie climatic adaptation. We were able to match these with functions that are known from phenotypic thermal adaptation (Wollenberg Valero et al., 2014). Interestingly, the products of these genes (Proteins, RNAs) were found to be functionally related with each other thus forming gene networks within the cellular environment.

The Caribbean Anolis cybotes is widely distributed across Hispaniola, and thrives in hot, xeric environments just as well as in cooler and more humid montane environments. The rift valley of Lago Enriquillo heats up to 40.5 °C (104.9 °F), and a few instances of frost were reported at the highest peak (Pico Duarte at 3,098m elevation) – so population survival across these climatic extremes does not seem to be a trivial endeavor.

Populations of this species show pronounced differences between montane and lowland forms in morphology, physiology, behavior, and perch use (Wollenberg et al., 2013Muñoz et al., 2014), which led us to expect that at least some of this variation should have a genetic basis. Thus, we set up to test whether Anolis cybotes displays any signatures of genomic adaptation to the diverse kinds of environments it inhabits, and whether any genes showing evidence for selection can also be subsumed under the candidate functions we defined previously.

We sampled tissue of these lizards from several high and low elevations (the specimens being the same as in Wollenberg et al., 2013), and looked for variation according to climatic differences via RAD sequencing and subsequent analysis with LFMM. RAD sequencing generates a reduced representation of the target genome, producing thousands of short sequences representing the distribution of the restriction enzyme’s cutting sites throughout the genome. Owing to this property, it cannot be expected that this type of data will necessarily contain “the total set of adaptation genes”; to this effect, detailed genome sequencing is required and such studies have been done in some model organisms (stickleback fish, beech mice, Drosophila, etc.).

What Makes Anolis Communities Complete?

One of my favorite graphic representations of a typical anole community is the one where all ecomorphs are hanging out together in a tree and a scrub next to said tree. Each ecomorph has its structural microhabitat place and they are all spaced out evenly across the tree to represent competition. Originally the figure was published by Williams (1983) and then modified later on. Arriving on the Greater Antilles, one thus expects to promptly be able to say hi to all these ecomorphs at the next best tree. Well, from my personal experience, I can tell you that this is unfortunately not the case.

Idealized representation

Localities where all ecomorphs are found together are scarce, and all of them are famous, having served as field sites for the most groundbreaking of anole discoveries. But what about the rest of them? Something must prevent the co-occurrence of ecomorphs in all these other places. This was noted before: Losos (2009) remarked that all utilized structural microhabitats exploited by all ecomorphs are present throughout the islands, so “complete” ecomorph communities should also be able to occur everywhere.

A common explanation for the absence of certain  “functional types” (= Anolis ecomorphs) from local communities is a process that is called “filtering.” Modern community assembly theory distinguishes two such types of filters: 1. Biotic interaction filters and 2. Environmental filters.

 Filters

Biotic filtering involves competitive exclusion: For anoles this phenomenon caused ecological speciation which led to the convergent evolution of the ecomorph communities. But biotic filtering should not be expected to occur at this stage of the radiation: Different ecomorphs are not competing for the same structural microhabitat niche in different localities. This leaves environmental filtering. In our study recently published in Ecology and Evolution, on which I am reporting here, we tested whether environmental filtering could be a possible explanation for the absence of ecomorphs in local communities.

First, we modeled Anolis ecomorph community completeness by constructing environmental niche models for each ecomorph (the sum of species belonging to that ecomorph) on each island. These models were then overlaid for all ecomorphs per island.  ECC map

 The map for ecomorph community completeness shows a very patchy distribution of areas where all ecomorphs are expected to occur. Comparisons of environmental niches among these islands revealed that only Hispaniola and Cuba have their complete Anolis ecomorph communities occurring in a similar bioclimatic parameter space.

This patchiness could be explained by elevation for all islands except Jamaica: the Anolis community completeness map strongly resembles the topographic relief of the Greater Antilles. Looking more closely into the climatic parameters, Jamaica has much lower daily and annual temperature ranges which are also not related to the island’s elevation, whereas in the rest of the Greater Antillean islands, they are. Occurrence probability of ecomorphs seems to be coupled to environmental parameters, which explains why some ecomorphs are “filtered out“ in some locations: they do not encounter a favorable environment there.

Since I mentioned initially that filtering relates to “functional types” (not species), the filtering must be a result of certain functional properties of the Anolis ecomorphs’ phenotype. We wanted to take the study a step further and actually investigate one (among many) possible functional trait: body mass.

Sex

Anolis carolinensis is headlining the new exhibition on animal sex in the Natural History Museum Rosenstein, Stuttgart, Germany. Go check it out if you’re in the area

http://webmuseen.de/sex-stuttgart.html

Great graphic design! Wondered several minutes what the toasted oats were doing in there. Duh, they're eggs! (amphibian)

Gear review: the Fish Pen

Are you sure you don’t want to take a lizard pole?” – “No way, we’re on vacation, not field work”.

teasing me

But once arrived on the lovely Yucatan Peninsula in Mexico I just couldn’t get any of the anoles perching on about every single palm tree to dewlap for me. I’d speculate about their dewlap colours – they did look like A. sagrei, but how could I be sure without flipping out their dewlap? And if I did, would it be red or orange, and how broad would the yellow margin be?

It was as if they were mocking me with their presence, knowing that I was pole-less. On the next trip to the local supermarket, however, I saw and immediately grabbed a small package that read: “Fish pen, as seen on TV.” It was a tiny telescopic fishing pole, complete with hooks, reel and line, that can clip to your shirt like a pen. For MXP 200 (ca. $20), I just had to buy it. Although I wouldn’t recommend to hunt any large or skittish lizards with it (it’s a short pole), it proved to be quite effective to satisfy any spontaneous dewlap-flipping cravings during vacation.

Great Moments in Anolology: Dedication of the MCZ Herp Library in Honor of Ernest Williams

“…On the first weekend of October in 2009, 125 anole biologists traveled from eight countries to Harvard University’s Museum of Comparative Zoology to attend the 6th Anolis Symposium. It had been 10 years since the previous symposium, and a reunion was long past due. In 2008, as we began to consider how to proceed with such an endeavor, a fortunate thing happened: the Herpetology Department at the MCZ renovated its library and teaching space – the famous lair of the late pater anolis, Ernest Williams. The library needed a namesake, and Ernest was under strong consideration (after all, he had been instrumental in filling its shelves!). After a brief period of friendly deliberation, it was decided that the library would be dedicated to Williams, and that the occasion would be the commencement of the 6th Anolis Symposium, held at the Museum of Comparative Zoology…” (From the preface of the Anolis Newsletter VI)

Anoleophobic Golfers, Rejoice

In the light of the recent debate of surfacing Scoliodentosaurophobia, golfers that are scared of anoles can now rejoice:

Galvin Green UK PACLITE® has collaborated with GORE-TEX® to create the first anoleophobic waterproof golfing gear, helping anole-conscious golfers to “reduce the stress on the body, preserving the body’s energy levels, enabling the golfer to focus more on the game” without having to fear unwanted anole encounters.  This product is making waves online with interested parties. People from all walks of life and health should be able to enjoy golfing. Thankfully, this is the kind of future we have in store for us.

anoleproof golfing gear

Phobias

Stumbling over the search terms leading to the Anole Annals blog today I found this interesting bit of information:

…”afraid of anolis”?

Scoliodentosaurophobia, apparently, is the scientific expression for “fear of lizards”. It’s a category to the more general Herpetophobia (fear of amphibians and/or reptiles). These sorts of fears might seem a little bit odd to the herpetologist… after all I have heard of colleagues having bite lists for fun (“what was the coolest species that ever had its fangs in you?”).  But they are surprisingly present amongst laymen and –women out there. Women in Africa would run screaming when they’d see me handling chameleons – fearing that the chameleon’s stare would prevent them from having babies. In the DR, Miguel Landestoy and I were convinced we could help prevent the slaughtering of Haitiophis snakes out of fear by telling farmers that “the girl (me) is not afraid of them either”, appealing to their machismo. The large Dominican green anole Anolis baleatus (and probably some other large crown giants too) has the nickname Salta cocote because it is supposed to jump at people from the trees, trying to suck their blood (“dice la leyenda que le salta a la gente y le muerde el cocote”). An older gentleman seemed very convinced that the Salta cocote had just sucked to death some of his neighbor’s cattle. It even has its own Merengue song (Caco e maco salta cocote, which literally means “you ugly frog head, lizard”).

Phobophobes, by the way, are afraid of phobias.

Do you want to cuddle? It makes me feel safe.

Is this really worth it? I was asking myself while trying to balance my weight on the slanted old tree which I had climbed, the mountain stream beneath me gurgling around glistening rocks in the humid night. I stretched out my left arm as far as possible while clinging onto the tree with my right, to snap a probably completely out-of-focus and missing-the-object-of-focus picture with my trusty waterproof Pentax. While pushing the releaser button, I noticed some parts of the old tree I was holding on to slowly giving away. A flash, a thump, and I found myself suddenly clinging to another part of the tree, while the green power diode of my camera now flickered at me from the bottom of the stream. Great, I thought, you’ve ruined your camera for a picture that won’t even have anything on it and wasn’t that great to begin with either. This is why I want to make it worth it now, a posteriori: worth a blog post. Examining the SD card later on it turned out, that there was indeed a motif on that picture, and even the one I had hoped to catch: Two male Anolis etheridgei sleeping together on a leaf (more like waking up on a leaf due to my intrusion), facing away from each other. What made this observation picture-worthy for me is that these weren’t the only specimens I found like that that night. At least five other pairs of male A. etheridgei were sleeping in the same position, touching each other’s tails. When I approached them, the one that would wake up first would make a jerking movement, then both would simultaneously drop from their sleeping site into the leaf litter. They were way harder to catch than many other sleeping anoles I’ve stalked at night. Four eyes are better than two, as the saying goes, and those little anoles seemed to have realized just that.

Cuddling for safety

Rest in peace, my trusty Pentax Optio WP.

Anole predation, literally

It was just one of these mornings when I found myself in the x-ray imaging facility downstairs, post-coffee, but still mostly functioning vegetatively, scanning my specimens. The most interesting incidences during these sessions usually involve Jon catching me dancing around to the mp3 player while waiting for the machine to finish or finding healed bone fractures and the like on the freshly acquired images. Sometimes I can even see gut contents, like what I think are elytras of coleoptera, or fractured snail shells. Well imagine my surprise when I scanned this massive male Anolis cybotes and found this in its stomach:

Image by K. Wollenberg Valero

It seems like it’s congener didn’t stand a chance – swallowed whole, head-first.

Image by K. Wollenberg Valero


Although the skull is pretty digested already and I can’t make out the shoulder girdle, it looks to me like a distichoid anole – a likely candidate, as these two types are frequently sharing their microhabitat (the trunks of trees and such).

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