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Does Evolution or Ecology of Anolis Lizards Shape the Bacterial Communities Living in their Guts?

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Figure 2 from Ren et al. 2016: “Diversity of Anolis gut microbiota as a function of host phylogeny. Each thin horizontal bar represents an individual lizard, with bacterial diversity (proportion of reads) coded at phylum, family, and genus.”

In recent years, the study of microbiomes – the communities of microorganisms living in certain environments or in association with hosts – has boomed. It’s long been understood that microorganisms (especially bacteria) can play a big role in host health, but recent work has also shown that microbes can have a huge impact on many other important facets of a host’s life, from growth and development to behavior. Despite the importance of these microbiomes, the ecological and evolutionary processes that shape them are still not very well understood.

In a recent study, Ren et al. (2016) decided to use our favorite model system to better understand the relationship between host and microbiome. As a classic example of an adaptive radiation, Anolis lizards provide an opportunity to test both ecological and evolutionary factors that might be influencing their microbiomes. In this study, the authors asked whether the evolutionary and ecological diversification of a host lineage (anoles) has structured the biodiversity of the gut microbiome community.

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A. evermanii and A. gundlachi sharing a perch

The authors used several approaches to address this question. First, they sampled gut microbiomes (using fecal samples) from six Puerto Rican anole species representing three ecomorphs: two trunk-crown sister species (A. evermanii and A. stratulus), two grass-bush sister species (A. pulchellus and A. krugi), and two trunk-ground species (A. cristatellus and A. gundlachi). They predicted that microbiomes of species of the same ecomorph would be more similar to one another than to species of different ecomorphs, reflecting an influence of either ecological similarity or phylogenetic relatedness on gut microbiome composition. Second, they sampled invasive populations of two trunk-ground species in Florida (A. cristatellus and A. sagrei) in sympatry and in allopatry to explore a) whether species that are phylogenetically distinct but ecologically similar have similar gut microbiomes and b) whether gut microbiome is influenced by the local environment. Lastly, they documented individual variation in gut microbiome composition over time by recapturing and resampling marked individuals.

The most striking result of the study was the huge amount of variability in gut microbiome composition between individuals (Fig 2, Ren et al. 2016). For example, on average, any two gut microbiomes only shared 7% of their bacterial OTUs (“Operational Taxonomic Units,” you can think of them as bacterial species). Such high variability from one individual to another is notable, compared to studies of other organisms.

In their analysis of the Puerto Rican anoles, the researchers found that gut microbiomes were more similar between conspecifics than between individuals of different species, but only weakly so. Perhaps more surprisingly, there was no difference in gut microbiome composition based on ecomorph. The authors suggest that this lack of distinction between ecomorphs may stem from the fact that most anoles are dietary generalists; although different ecomorphs do partition habitats, they still overlap in the types of arthropods that they consume, which could impact their gut microbiomes. The authors find further support for this conclusion in their separate analysis of temporal variation in A. sagrei. The composition of an individual’s gut microbial community fluctuated greatly over time, suggesting that transient factors (such as variability in diet) have a significant impact on the gut microbiome.

Interestingly, the two invasive trunk-ground species in Florida showed a much stronger pattern: despite being of the same ecomorph, the gut microbiomes of the two species were significantly different from one another. The authors suggest that the strong signal in these not-so-closely-related invasive anoles along with the weak signal in the closely-related Puerto Rican anoles might indicate that Anolis evolution could have impacted the diversification of the gut microbiome over long evolutionary timescales, but the Puerto Rican radiation just is too young for such microbiome divergence to have occurred. But it’s also possible that the difference in the microbiomes of the two invasive anoles is just a holdover from the source environments (Puerto Rico and Cuba) that has been maintained in their invasive ranges. To throw another wrench into the works, the authors also found that allopatric populations of one of the invasive species (A. cristatellus) were different from one another, while those of the other invasive species (A. sagrei) were not.

So does host ecology impact gut microbiome? Does host phylogeny? Or host environment? Ren et al.’s study suggests possibly yes to all, but with limited (and somewhat conflicting) evidence, it’s hard to draw any certain conclusions. Perhaps more poop from more branches of the Anolis tree will hold the answers.

 

Find the full paper here:
Ren, T. et al., 2016. Does adaptive radiation of a host lineage promote ecological diversity of its bacterial communities? A test using gut microbiota of Anolis lizards. Molecular Ecology.

Praying Mantis Eats Anole

carolinensis eaten by praying mantis

The stuff of science fiction horror stories. We’ve previously reported on spiders eating anoles [e.g., 1, 2 and type “spiders” into search bar for more], but reports of anolivory by other invertebrates are scarce. Some others (from p.141 of Lizards in an Evolutionary Tree): katydids, tarantulas, whip scorpions, and centipedes.

Some Anoles from Cuba – Help for ID

During July-August 2016, I went for a three-weeks holiday trip to Cuba. Being a Ph.D. student at the Lizard Lab, I had to come back with pictures of… lizards of course. This post is dedicated only to the anole species I observed in Cuba. Any help to ID will be greatly appreciated! More of my pictures of the Cuban herpetofauna (anole and non anole) can be found on my website website.

1- Anolis sp (?) from Cienfuegos.

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2- Anolis sagrei – Brown Anole

a) DSC_0307-3

b) DSC_0388-3

c) DSC_0391-3

 

3- Anolis allissoni – Allison’s Anole

a) DSC_0418-2

b) DSC_0483-3

c) DSC_0897-3

 

3- Anolis homolechis – Cuban White-fanned Anole

a) DSC_0515-3

b) DSC_0842-3

4- Anolis porcatus – Cuban Green Anole

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5- Anolis vescus – Purial Bush Anole (??) from Baracoa

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6- Anolis sp (?) from Viñales

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Honduran Anole Identification

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I have been working my way through McCranie and Kohler’s guide to Honduran anoles and thought I would pull out some old photos from when I did some romping about Honduras a decade ago. At the time I had little interest in anoles and barely noticed them on my trips to Honduras (O foolishness of youth!). These photos below, however, represent a species I remember seeing frequently. I believe it is Norops lemurinus but without a specimen in hand it is difficult to use a dichotomous key. I was hoping someone more familiar with this part of the world could offer confirmation or correction. I was on the northern coast a few miles east of Balfate, less than 50 m above sea level.

I took my first trip to Honduras in 2004 at the age of 19 and made six more trips over the next eight years. Unfortunately, what I remember most was how the landscape changed so drastically from one year to the next as more and more people, mostly ‘norteamericanos,’ moved in to extract any and all resources from the land. At 19, I could hardly take one step through the long grasses on my way to the beach without scattering a half dozen lizards. I remember that so vividly! By the time I hit my late 20’s the grasses were replaced with a coconut grove and a size-able complex of condominiums (built by and, I assume, advertised to Canadians).

Of course, there are still plenty of herps around and about: when last I left, the cane toads and hemidactylids were doing just fine.

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A Tale about Two Tails: No Effect of Having a Regrown Tail on Body Condition

A dorsal view of the brown anole male that I collected on the 19th of July 2002.

A dorsal view of the brown anole male that I collected on the 19th of July 2002.

On the 19th of July, 2002, I collected a brown anole (Anolis sagrei) male from the edge of a rice paddy next to a tarred road in Santzepu, Sheishan District, Chiayi County, Taiwan, as part of a diet and reproductive cycle study. As I removed it from the fine-meshed fishing scoop net, which I used for capturing it, I found that it had two tails. I later found that even though the lizard had no abdominal fat bodies the animal was still in a reproductive state, indicating that it was not only able to regenerate a tail twice, but it could also still meet the energetic demands for reproduction.

This finding prompted our study to attempt to address the question of whether there are differences in the abdominal fat body weights and liver weights of A. sagrei specimens that had suffered tail autonomy and conspecifics that had not.

We were surprised when we found no statistically significant variations in the monthly mean abdominal fat-body weight indices or monthly mean liver weight indexes of lizards that had not experienced caudal autotomy and those that had. We hypothesize that A. sagrei specimens that experienced tail autotomy most likely met the energetic demands for regenerating the lost portion of their tail by foraging more.

Editor’s Note: for more on two-tailed anoles, such as the photo below, type “tail” or “tailed” into the search bar on the right.

 

ESA 2016: Top-Down Effects of Brown Anoles on Islands Following Hurricanes

Following up with summaries of anole talks at ESA 2016, Dave Spiller presented a broad summary of his and his colleague’s (Tom Schoener and Jonah Piovia-Scott) research investigating the effects of hurricanes on long term food web dynamics of small Bahamian islands, which has just recently been published in Ecology (see Spiller et al. 2016).

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Spiller opened by explaining some of the patterns of food web dynamics that have been learned from this research. Most notably, that the elimination of brown anoles – which act as top predators in these simple ecosystems – leads to increased levels of herbivory as arthropods experience a relaxation of predation pressure (Spiller and Schoener 1990).Specifically, the presence of a common moth (Achyra rantalis) on islands without brown anoles can lead to extreme levels of herbivory upon a common island plant, Sesuvium portulacastrum (below).

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Spiller and his colleagues began to notice that following hurricanes, one of the most extreme natural disturbance events in this region, islands with lizards experienced a much more rapid recovery of Sesuvium .

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In an attempt to understand how ecosystems may be stable despite experiencing extreme disturbance regimes, Spiller and colleagues measured the percent ground cover of Sesuvium and abundance of Achyra moths on 11 islands with lizards present and 21 islands without lizards annually for 10 years.

Overall abundance of Achyra was 4.6 times higher on no-lizard islands than on lizard islands. The percent cover of Sesuvium exhibited lower temporal variability on lizard islands when the study site was undisturbed by hurricanes, and higher recovery rate on lizard islands following hurricanes.

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Spiller concluded by suggesting that these stabilizing phenomena are linked to a trophic cascade in which predators (brown anoles) control herbivores (Achyra moths), and therefore enhance plant recovery following hurricanes.

Brown Anole Mouthful

Photo by Karen Cusick

It’s amazing the size of prey that some anoles will try to get down their throats (and who could blame them?).  Here’s an example from Daffodil’s Photo Blog. And here’s another example from the same source.

Great Nickname for Jamaican Anole

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Anoles on Exhibit at the Milwaukee Public Museum

 

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AA stalwart Tony Gamble has provided these two photos from exhibits at the Milwaukee Public Museum. The one above is a knight anole, whereas below, an Archaeopteryx appears to be dining on a green anole, significantly increasing our understanding of the age of the anole radiation.

AA’s other Wisconsin stalward, Greg Mayer, provides the low-down: “The equestris  is from the Rain Forest exhibit. This is a fabulous exhibit based mostly on the Costa Rican rain forest, but including some other tropical/rain forest elements. I take my vert. zool. class there every year, and have used it as part of the pre-trip preparation for Costa Rican field classes. It was funded in part by the NSF, and involved lots of field work–they did latex casts of trees to get the bark right for life size models of them! The Milwaukee Public Museum was much involved in making Costa Rica the center of tropical studies for US-based scientists. The MPM was slightly independent of OTS. They had their own field station, La Tirimbina, which is very nice–I’ve taken students there 2 or 3 times.

Allen Young, the MPM lepidopterist, was the driving force for Milwaukee’s tropical studies. He wrote about his work at Tirimbina in Sarapiqui Chronicle (Smithsonian Institution Press, Wash. DC, 1991). Young first went to Costa Rica in 1968 with OTS, then focused his work at Tirimbina. (Bob Hunter, who owned Tirimbina at the time, also owned part of La Selva, and was involved in getting both places established as field stations.) MPM’s stake in Tirimbina was sold off by then Milwaukee county executive (now governor) Scott Walker, who couldn’t imagine why a natural history museum in Wisconsin could be interested in Costa Rica. Fortunately, another conservation organization bought MPM’s share.

Others were involved in the exhibit creation as well, and though I’ve never asked him, I’ve always thought the Anolis equestris behavior display in the rain forest exhibit may have been a contribution of Bob Henderson. There are several males and females (not sure if they’re freeze-dried, or some kind of model), showing various levels of agonistic display– fans, nuchal crests, open mouth, raised posture– set out on vines/branches. A question I ask vert. zool. students about this display case is how could they tell the lizards are arboreal, even if they were not posed on branches.”

And with regard to the photo below: “The other picture is from the Third Planet exhibit (I’m always tempted to write Third Rock!), from a section of that very good exhibit on the Hell Creek Formation and the end Cretaceous vertebrate extinctions. The MPM has two Archaeopteryx models made up with feathers, and the one in the pic has a dried or model Anolis carolinensis in its mouth, painted a fairly bright green. The other Archaeopteryx model is better done, and that one goes out on loan periodically to other museums (I think I’ve seen it at the Field Museum).

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Owls Eat a Lot of Anoles: Data from Dominica

An owl with a green anole.

A recent paper in the Caribbean Journal of Science on the diet of the Lesser Antillean barn owl on Dominica revealed that anoles, specifically the native species A. oculatus, are a very frequent prey item, constituting 193 of the 517 prey items. The authors note that owls are nocturnal and anoles are diurnal and proffer three explanations: 1. the predation occurs at dawn and dusk, when both species are normally active; 2. the anoles are active around lights at night; 3. the owls are catching the anoles while they sleep. We’ve discussed this topic before: owls are known to eat anoles in Cuba and many other places in the neotropics, and there’s the great photo re-posted below (original post here). As far as I’m aware, that’s the only direct observation of an anole being preyed upon by an owl (although a quick search on Google Images will yield many photos like the one at right). We’ve also discussed the parallel  issue of bat predation on anoles in these pages. Clearly, more data are needed!

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