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The Evolution of Variation in Back Patterns in Anolis

Many species of anoles exhibit distinctive dorsal patterns, including spots (e.g. A. sabanus), stripes (A. krugi) or chevrons (A. sagrei) (Figure 1). Dorsal patterns are highly variable in anoles, presenting not only variation across species, but also within species (sexual dimorphism) and within sexes (polymorphism). So why is there such a large variation in dorsal pattern?

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Figure 1. Examples of dorsal pattern in Anolis lizards. A, A. sagrei, B, A. krugi, C, A. sabanus (photograph by B. Falk). D, A. pulchellus. Photographs A, B and D by D. L. Mahler.

Previous posts (1,2) explain the extent of the variation in dorsal pattern within females, a phenomenon known as female-pattern polymorphism (FPP), where females are more likely to present variation in dorsal patterns than males. Other studies have tried to explain within-population variation in dorsal pattern in several Anolis species with montane and xeric distributions. These studies suggest that habitat and crypsis could be an important factor explaining variation in dorsal pattern in Anolis.

Anoles are famous for having evolved convergent ecomorphs in different islands in the Caribbean. Each ecomorph is associated with a suit of adaptive traits that has evolved in response to their ecology. Some years ago, I went to the Losos Lab to explore, using several species of Anolis and hundreds of museum species, whether ecomorphs could explain variation in dorsal pattern. Namely, we wanted to know whether differences between ecomorphs could explain the degree of sexual dimorphism in dorsal pattern and female polymorphism, using 36 species of Anolis from the Greater Antilles.

In our paper, published on early view in the Biological Journal of the Linnean Society, we built a matrix with 11 different characters that described dorsal pattern. We used this matrix to construct a principal coordinate space, and in this space we calculated distances between male and female dorsal pattern for each species  (amount of dorsal pattern sexual dimorphism) and the variation in dorsal pattern within each sex (amount of polymorphism within sex).

We found that species perching closer to the ground have higher degrees of sexual dimorphism, and males and females from these species usually present different patterns (Figure 2). For example, in A. bahorucoensis, a grass-bush species, females present a dorsal stripe, while males have chevrons. We also found that size dimorphism is correlated to dorsal pattern dimorphism, and species perching closer to the ground have larger differences in size and dorsal pattern between sexes, suggesting that both types of dimorphism are evolving together. We suspect that larger differences in habitat use between males and females in low-perching species may explain why some species are more dimorphic in dorsal pattern that others.

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Figure 2. Association between sexual dimorphism in dorsal pattern and ecomorph in 36 species of Anolis. A, Phylogenetic tree with coloured branches representing values of dimorphism in dorsal pattern (Euclidean distance). Circles at tips represent ecomorph and the colour legend is the same as in (B). B, Values of dorsal pattern dimorphism according to ecomorph class.

On the other hand, ecomorph could not explain why some in some species there is higher variation in dorsal pattern in females (FPP). In our study, 44% of the species presented significantly higher female polymorphism than male polymorphism, reflecting how widespread is this phenomenon, but this was not related to ecomorph type. However, species with higher female polymorphism also had males that were more variable, suggesting that they might be under similar selective pressures. More precise information on habitat preferences within sexes, especially in  females, will be required in order to fully understand the mystery of female-biased polymorphism.

Reference

Medina, I., Losos, J.B. & Mahler, D.L. 2016. Evolution of dorsal pattern variation in greater Antillean Anolis lizards. Early view, Biological Journal of the Linnean Society.

Rodolfo Ruibal, R.I.P.

AA is sorry to learn of the passing of Rodolfo Ruibal, an eminent Cuban herpetologist based at UC-Riverside for many years. Rodolfo did important early work on thermal biology andsocial behavior of Caribbean anoles. For example, 1961 paper showed thermoconformity in some lizards (when everyone though that lizards always thermoregulate carefully), it showed that physiology can evolve faster than morphology, and it proposed that only thermoregulators (not thermoconformers) could invade the temp zone.

You can find transcripts from a 1998 interview with Rodolfo as part of a UC-Riverside history project. Here’s the obituary that recently appeared in UCR Today:

Professor Emeritus Rodolfo “Rudy” Ruibal, a founding member of UC Riverside’s Biology department whose passions included lizards, frogs and making beautiful jewelry, died Aug. 30 at the age of 88, just six months after the death of his wife of 68 years, Irene Shamu Ruibal.

“He was instrumental in forging the department in the directions and expertise that form its center now,” said Professor Michael Allen, chair of UCR’s biology department.

Ruibal was a native of Cuba who conducted research in several parts of South America with fellowships from the National Science Foundation and the John Simon Guggenheim Memorial Foundation. He was an early student of temperature regulation in reptiles and amphibians, said friend and colleague Professor Mark Chappell, and was also known for his work with water loss in amphibians and their ability to waterproof their skin by using waxy glandular secretions the animals wipe over themselves.

“He taught the Biology 161 course, on functional vertebrate morphology, or ‘Vert’ to generations of premeds and other life science students, and was renowned for both the clarity of his lectures and for his skill in drawing structures on the blackboard,” said Chappell.

During Ruibal’s 42 years at UCR, he helped establish the Philip Boyd Desert Research Center and spent a year as the acting director of UC MEXUS, created to stimulate teaching and research between California and Mexico. Ruibal also spent a year advising a man he much admired—UC President Clark Kerr—about faculty requests and concerns.

“He always had one faculty member in his office,” Ruibal said during an oral history interview in 1998. “It was his way of simply making sure his faculty were being treated by an academic who knew what the score was, rather than somebody who was just a bureaucrat.”

Ruibal’s life read like a novel. He was born in Cuba on Oct. 27, 1927, an only child who attended the same Jesuit school as Fidel Castro. The budding scientist had an early fascination for animals, said his son, Claude Ruibal of Zurich, Switzerland. Rudy Ruibal’s earliest memories were of watching fish swimming in the waters of Cuba, and chasing lizards in his yard, something his aunt remembered years later, when he returned to Cuba for research on an NSF grant project.

Reptiles and research always fascinated Ruibal, and he excelled at an early age. He enrolled in Harvard when he was just 16 years old, after completing high school at the prestigious McBurney School in Manhattan.

Ruibal took a break from Harvard when he was 18, to serve in the military at the tail end of World War II. But he returned to school a year later and married his wife, Irene, a secretary in the Department of Herpetology in the American Museum of Natural History.

By the time he was 21, Ruibal had finished his BA at Harvard and enrolled at Columbia University for graduate studies in biology. At 26, Ruibal completed his PhD and accepted a position at a new liberal arts college called UC Riverside, where Howard Spieth, one of his former professors at Columbia, had become the chair of the life science’s department, and would later become the university’s first chancellor.

Ruibal began teaching in the fall of 1954, the second semester for a school so new that it had no landscaping or trees. Their son was born the following year, in 1955. Claude Ruibal said his parents were loving but not overbearing. His father, he said, “was a thoughtful guy, a moral guy—very rational and not very emotional. I don’t think I ever heard my parents argue.”

His mother loved to cook and throw dinner parties, and they cultivated a diverse group of close friends—artists, business people, even the publisher of the newspaper. His father loved tennis, playing into his 80s, and did a lot of reading about history and politics.

Ruibal also was a noted local artist. Shortly after he arrived in Riverside, he successfully lobbied the Riverside Art Museum to have real nude models available for sketching (instead of women in bathing suits). He later branched into candle making, ceramics —complete with his own kiln—and finally, making brass and silver jewelry, which were top sellers at the Riverside Art Museum, Mission Inn Museum and other locations.

Anole Fashion: Dorsal Crests and Curlicue Tails

Daffodil’s Photo Blog has some nice photos of stylish anoles. Some anoles–the festive anole (A. sagrei) being a prime example, seem to have a penchant for sitting with their tails hanging in a lovely. Why do they do it? Got me.

We do know why they raise their dorsal crests–to look fearsome, as this mini-dinosaur does. How they do it, though, is another matter, when discussed previously in these pages (1,2).

Best Anole Dewlap of All Time?

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There are many contenders, but my favorite is Anolis sericeus, seen above from the Kanahau research station on the Honduran island of Utila, and another photo below from Chiapas, Mexico.

Lizards Running (and Slipping) in Ultra-Slo-Mo!

Day’s Edge Productions has done it again (again? see here and here).

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.

 

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