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Vasotocin and Chemical Communication in Anolis carolinensis

 

A male green anole basking on my porch in Atlanta, Georgia. (Photo source S. M. Campos)

Growing up in Texas, I often found Anolis carolinensis green anoles (my first love) basking on my front porch and developed an early obsession with studying their natural behavior. Green anoles are the only anole endemic to North America (but see Wegener et al. (2019) suggesting the Cuban green anole, Anolis porcatus, is the same species). Anolis carolinensis are often referred to as American Chameleons due to their ability to switch between green and brown skin colors, despite being a completely different family than true chameleons. In graduate school, I worked with a different lizard genus, Sceloporus (from Greek “skelos” meaning leg, “poros” meaning hole), named for the scent producing glands on their inner thighs called femoral glands. The realization that some lizards modulate their social behavior based on chemical information that is deposited by other lizards was pivotal in my research career. Here, I’ll discuss chemical communication in A. carolinensis and the serendipitous discovery that the neuropeptide arginine vasotocin (AVT) plays some role in stimulating this chemical communication.

Anolis is an important animal model for studying the neuroendocrine control of visual communication due to their hormonal modulation of  vibrant color displays and conspicuous push up displays. Large eyes and brain areas dedicated to processing visual information suggest that detecting and responding to the visual environment is very important to anole survival and fitness. In contrast, anoles do not have the femoral or precloacal glands described in other lizards, which are used to deposit scent marks. Their olfactory bulbs (the portion of their brains that responds to volatile and non-volatile chemical signals) are tiny structures that are nestled in front of their eyes and behind their nares, attached to the rest of the brain by a long narrow nerve tract. Therefore, it is not all that surprising that anoles have long been considered microsmatic, relying very little on their sense of smell.

A CT scan of Anolis sagrei showing the main and accessory olfactory bulbs (yellow and blue arrows, respectively). The main olfactory bulb responds to volatile chemicals detected by the olfactory epithelium in the nose (such as odors in the air) and the accessory olfactory bulb responds to non-volatile chemicals detected by the vomeronasal organ. (Source Photo by Ed Stanley, arrows added by S. M. Campos)

So what is the deal with this peptide hormone, AVT? AVT and its mammalian homologue vasopressin (AVP) regulate social behavior in animals and decades of research has shown that AVT works within the visual sensory system of green anoles to modulate competitive and reproductive interactions. In non-reptilian animals like fish and mammals, AVT/AVP plays a similar role in modulating social interactions through the chemosensory system. Whether AVT influences chemosensory behavior in reptiles is unknown, representing an important gap in our understanding of the evolution of social behavior.

Now, the serendipitous part of the story. My postdoc advisor, Walter Wilczynski, built his career studying how AVT impacts visual communication in social interactions of frogs and green anoles. Previous work showed that green anoles can differentiate between AVT-treated and saline-treated males during live social interactions, but found no obvious differences in visual display rates between AVT-treated and saline-treated males, suggesting differences in behavior may be due to available chemical information. In the present study, we asked  whether an untreated lizard responds to a live AVT-treated male by altering its rate of chemosensory behavior, which we would expect if AVT-males and saline-males emit different chemical signals.

From left to right: Study authors Stephanie M. Campos, Walter Wilczynski, and Valentina Rojas. (Photo source S. M. Campos)

While lizards breathe in odors in a manner similar to humans (olfaction), they also have a secondary sense of “smell” called vomerolfaction. The latter involves using their tongues to bring chemicals from the outside environment into their mouths and deliver those chemicals to the vomerolfactory organ (often referred to as Jacobson’s organ in snakes) located in the roof of their mouths. We can easily quantify chemosensory behavior involving the tongue by counting the number of licks (tongue touches to a substrate, such as a rock), tongue flicks (tongue extrusions into the air), and lip smacks (draws odors into the mouth) a lizard performs. Use of these behaviors give us an estimate of a lizard’s level of interest in the chemical information available in their immediate environment. Chin wiping, or jaw rubbing, is another chemosensory behavior that may either deposit chemical signals or help to detect chemical signals already on a substrate. We provide short video clips in the online version of our article to show each of these behaviors.

In our experiment, we gave adult male green anoles an intraperitoneal injection of either an AVT or saline (control) solution, then introduced an untreated lizard (male or female) into the home tank of the treated lizard for a filmed 30-minute interaction. We measured rates of chemosensory behavior and the latency to perform these different behaviors. Since lizards tend to use higher rates of tongue flick behavior for exploratory purposes as they move around their environments (Cooper et al. 1994; Mason 1992), we also counted short bouts of locomotion.

Untreated males that interacted with AVT-males performed more tongue flicks and lip smacks compared to males that interacted with saline-males. Interestingly, lizards that interacted with AVT-males tended to move around less compared to lizards that interacted with saline-males. This suggests that the higher rates of chemosensory behavior by untreated males that interacted with AVT-males was not simply due to an increase in locomotion. We also found that untreated males moved around more than untreated females, regardless of treatment, demonstrating a general sex difference in locomotion among green anoles. We found no significant differences between treatments in chemosensory behavior performed by untreated females.

Lizards in their home tanks. (Photo source S. M. Campos)

When we examined the behavior of treatment males (which received injections), we found that AVT-males were faster than saline-males to perform a chemical display and, more specifically, a tongue flick toward untreated males. This suggests that AVT increases the level of initial interest in chemical information that is available during asocial encounters.

What about visual displays? We found no significant differences in visual display rates of untreated lizards, but did find that as treatment males performed more visual displays, untreated lizards moved around more (Supplementary Materials).

These results collectively suggest that AVT impacts chemosensory behavior during social interactions in green anoles, even in untreated social partners. More broadly, the mechanisms used by AVT to impact chemosensory behavior may be evolutionarily conserved. Our results are consistent with previous work linking AVP in mammals and AVT in fish to chemosensory-mediated interactions, such that AVT in reptiles deserves more research attention in the future. Furthermore, even in microsmatic lizards like Anolis, the impact of chemical communication on social dynamics should not be ignored. This study examined social dynamics between two live lizards and did not isolate the chemical signal. Thus, further work is necessary to determine whether similar changes in chemosensory displays occur when isolated chemical stimuli are presented to untreated lizards.

Aruba Anole on “Banknote of the Year”

According to no less authoritative a source than Coin World, the most fabulous new currency for 2019 is the 100-florin bill (about $56 US) from the island of Aruba. You can read all about it in CW‘s article below, but let me highlight the important point that our very own Anolis lineatus is featured prominently on the bill (as well it should be). Clearly, the message here is that if you (you being a country) want to gain accolades for your currency, putting an anole on the note is a wise move. Perhaps some of our more artistically gifted readers can mock up some examples?

Those of you in the anole-know will recall that A. lineatus is distinctive as being the only anole in which the two sides of the dewlap are different.

h/t George Gorman

 

Paper Money

Aruba 100-florin note named Banknote of the Year for 2019

By Arthur L. Friedberg , Special to Coin World

Published: Apr 20, 2020, 8 AM

Aruba’s new 100-florin note was named Banknote of the Year for 2019 by the voting membership of the International Bank Note Society. The winner bested 21 other contenders selected from among the over 100 new notes issued last year. The finalists were the only ones considered new enough in design to be considered for the award.

The IBNS said that Aruba’s entry led almost from the start of balloting. While every nominee received at least some votes, immediately behind Aruba were the Eastern Caribbean States $10 bank note with multiple motifs, the Ulster Bank of Northern Ireland’s £5 note showing flying geese with people on the shoreline, and Switzerland’s 1,000-franc bank note with human hands in the main design. Norway’s 1,000-kroner note with a cascading wave design was in fifth place.

The IBNS competition began in 2004, but this was Aruba’s first entry.

Canada’s $10 bank note won for 2018, breaking a two-year run by Switzerland with its 10- and 50-franc notes.

Aruba issued a new five-note series of 1-, 5-, 10-, 25-, 100- and 200-florin notes at one time on June 30, 2019. (The florin is pegged to the U.S. dollar at a rate of 1.79:1.)

The series, called the “Stars of Aruba,” was the first redesign in 30 years. Their vertical format draws on artistic elements from Aruba’s culture, flora, and fauna. They were jointly developed with Crane Currency, who also did the printing. Given Aruba’s small population of 120,000, the central bank needed to balance anti-counterfeit technology with production costs, and did so utilizing high-relief printing, watermarks, color-changing ink, the Omron Rings, and Motion Surface, Crane’s 3D moving stripe with miniaturized micro-optics.

The face of the 100-florin note is predominantly emerald green in color with a large iguana in its center and an indigenous lizard, the striped anole (Anolis lineatus) on the left. The green and blue back features women in native dress dancing and leaves from the aloe plant, an economic mainstay.

Jane Semeleer, president of the Central Bank of Aruba, said, “It is very clear that we have managed to create a beautiful family of bank notes. We have one of the most innovative and modern banknote series in the world. And we’re very proud that our vision — to make Arubans proud of their country and to show the world the rich life of Aruba — has led to an award winning 100 florin banknote.”

Semeleer added, “We had to present a better product that the public could fall in love with — and we succeeded. The reactions since the launch have been very positive. Shortly after the co-circulation started, 80 percent of the old banknotes where exchanged.”

About the award

Among the criteria for the nominated notes, according to the IBNS, “Banknotes nominated must have been issued to the public (specimens and non-circulating currencies are inelligble) for the first time during the year of the award, and must have artistic merit and/or innovative security features, and be in general circulation.”

Notes were judged and “the winner [was] decided by a vote of the IBNS, who will consider the artistic merit, design, use of colour, contrast, balance, and security features of each nomination,” according to the IBNS.

“The IBNS Banknote of the Year award is an initiative of the IBNS to recognize an exceptional banknote issued each year,” according to the organization.

Do Bigger Anoles Have More Diverse Parasites? Not in Brazilian Anolis fuscoauratus

Anolis fuscoauratus. Photo by Roberto Langstroth

New literature alert!

In Journal of Helminthology
Helminths associated with Norops fuscoauratus (Squamata, Dactyloidae) in highland marshes of the Brazilian semi-arid
J.M. dos Santos Mesquita, S.S. de Oliveira, R. Perez, R.W. Ávila

Summary

Helminthological studies may contribute with valuable information on host biology and conservation. Herein, we provide new data on helminths infecting the lizard Norops fuscoauratus, testing one of the factors considered most important in parasitic ecology: host size. We analysed 25 specimens of N. fuscoauratus from three highland marshes in the Brazilian semi-arid. Eight taxa of helminths belonging to Nematoda, Trematoda and Acanthocephala were found. Physaloptera sp. showed the higher prevalence (40%), with a mean intensity of infection of 3.3 ± 1.46 (1–16) and mean abundance 1.32 ± 0.65 (0–16). Norops fuscoauratus represents four new host records for the helminths Cyrtosomum sp., Pharyngodon travassosi, Strongyloides sp. and Centrorhynchus sp. There is no relationship of host body size (P = 0.79) and mass (P = 0.50) with parasite richness. In addition, the present study contributes to the knowledge of the parasitic fauna of N. fuscoauratus and the Neotropical region.

Read the full paper here!

Anoles among the Most Endangered Species in Dominican Republic

Anolis marcanoi. Photo by Rich Glor

reprinted from Dominican Today

The global prayer that motivates the celebration of Biodiversity Day today is a call to stop the loss of biological diversity, that is, the variety of species of plants, animals, and microorganisms that inhabit the planet in its various ecosystems.

Why is this biological variety important? For the United Nations, “biological resources are the pillars that sustain civilizations.” For example?

“Fish provide 20% of animal protein to some 3 billion people. More than 80% of the human diet is made up of plants. Approximately 80% of people living in rural areas of developing countries depend on traditional plant-based medicines for basic health care,” says the agency.

However, an estimated one million animal and plant species are currently endangered.

FLORA IN DANGER

In the DR, for 2011, the List of Endangered, Threatened or Protected Species of the Dominican Republic (Red List) published by the Ministry of the Environment indicated that “of the approximately 6,000 vascular plant species reported for the Dominican Republic, 547 were found to have some category of threat.”

Later, updated data collected in the Red List of Vascular Flora in the Dominican Republic (2016) indicate that some 1,388 plant species present some degree of threat. Some 841 more species than those registered in 2011.

Which of these species are the ones with the highest degree of vulnerability and critical status?

Research indicates that among the families with the highest percentage of their species under some degree of threat are those of orchids (Orchidaceae), palms (Arecaceae), and cacti (Cactaceae).

Indeed, of the orchid family, 145 of the 268 species studied are critically endangered, including the cacatica ( Tolumnia henekenii ) and the Quisqueya rosea.

25 species were included from the palm family (Arecaceae). Of these, there are 13 critically endangered: the red Manacla, Calyptronoma plumeriana; guano: Coccothrinax boschiana; the lake guano: Coccothrinax jimenezii; the guano de costa:Coccothrinax montana Burret; the palm Coccothrinax scoparia Becc; the tame guano: Coccothrinax spissa LH Bailey; el yarey: Copernicia berteroana Becc; the rain palm: Gaussia attenuata; the search Pseudophoenix sargentii H. Wendl; the frisk Pseudophoenix vinífera; the wild coquito: Reinhardtia paiewonskiana; the Thrinax radiata palm  and the guaney: Zombia antillarum. 

Of the cacti, eight species are critically endangered: the Bánica rose ( Pereskia marcanoi Areces ), the Bayahibe rose ( Pereskia Quisqueyana Alain), the spiny melon ( Melocactus lemairei and Melocactus pedernalensis ), the rose ( Pereskia portulacifolia ), the Melocactus praerupticola Arece s; the pitajaya ( Harrisia nashii Briton ) and the cagüey or avocado ( Dendrocereus undulosus ).

Within the families of compound flowers (Asteráceas), of the 99 analyzed there are 76 in critical condition, among them the Salcedoa mirabaliarum.

Other plants that are listed as critically endangered are three species of conifers (juniper): Juniperus gracilior var. ekmanii, Juniperus gracilior var. gracilior and Juniperus gracilior var. urbaniana and the cross stick (Podocarpus hispaniolensis laubenfels ).

You can see images of species of Dominican flora that is critically endangered in the following gallery: https://listindiario.com/la-vida/2017/08/03/476648/galeria-de-la-flora-dominicana

AND ANIMALS?

The distribution of local fauna is as follows: 483 species of amphibians, reptiles, birds and mammals; 527 species of marine and freshwater fish and 8,529 species of invertebrates (6,833 terrestrial and 1,696 marine). In total, 9,539 species, according to the 2011 List of Endangered, Threatened or Protected Species of the Dominican Republic (Red List) .

Which are in the worst state of conservation?

Among the critically endangered fish are two types of native grouper, Epinephelus itajara and Epinephelus striatus, and the endemic fish Cyprinodon higuey and Cyprinodon nicholsi.

Amphibians and lizards are among the most vulnerable. About to disappear are the endemic species of the Hispaniola crested toad ( Peltophryne fluviatica ); the Jarabacoa burrowing frog ( Eleutherodactylus bothroboans ); the red-legged frog of La Selle ( Eleutherodactylus furcyensis ); the La Selle brown frog ( Eleutherodactylus jugans ); the southern pastel frog ( Eleutherodactylus leoncei ) and the green spiny frog ( Eleutherodactylus nortoni ).

Also the Neiba telegraph frog ( Eleutherodactylus notidodes ); Neiba’s whistling frog ( Eleutherodactylus parabates ); the Rucilla stream frog ( Eleutherodactylus rucillensis), the Bahoruco red-legged frog ( Eleutherodactylus rufifemoralis ); the northern stream frog ( Eleutherodactylus schmidti ); the Massif du Nord’s whistling frog ( Eleutherodactylus sommeri ) and the Vallejuelo burrowing frog ( Eleutherodactylus tychathrous ).

Among the reptiles, the most threatened are the hawksbill turtle, Eretmochelys imbricata; the giant lucia of Villa Altagracia, Celestus anelpistus; the lucia of Pico Duarte, Celestus marcanoi; the slender Alto Velo anolis (lizard), Anolis altavelensis; the green-banded lizard, Anolis fowleri; the long-nosed lizard from La Selle, Anolis hendersoni; the sturdy red fan lizard, Anolis marcanoi; the Neiba twig lizard, Anolis placidus; the ricord iguana, Cyclura ricordii and the lizard Leiocephalus altavelensis.

Two species of skid lizards also appear in critical condition, Mabuya lineolata (striped skink from Hispaniola) and Mabuya sloanii (greater skink from the Antilles) and thirteen species of geckos or geckos (spherodactyls), all endemic.

Running snakes Haitiophis anomalus, Hypsirhynchus melanichnus,  Laltris agyrtes and laltris haetianus; the snakes Mitophis absolepisMitophis calypso , Mitophis pyrites and Typhlops syntherus are also almost in critical condition, as is the American crocodile, Crocodylus acutus.

Of the birds, the diablotín ( Pterodroma hasitata ), the Spanish sparrowhawk ( Buteo ridgwayi ), the barb ( Coccyzus rufigularis ) and the owls Asio flammeus and Asio stygius are critically endangered.

The manatee ( Trichechus manatus ) is among the most threatened marine species and, as a curious fact, the solenodon ( Solenodon paradoxus) does not appear in the category of critical danger, but “endangered.”

Article on St. John Lizards

Getting To Know Your Virgin Island Lizards

Crested anoles are curious and not shy. (Source photo by Gail Karlsson)

During the Virgin Islands ‘safer at home’ phase, I have found myself engaging more frequently with my non-human housemates – especially the lizards.

Most days I’ll be working at a table on our screened ground-level porch. The screen door is loose along the bottom, which has allowed a small lizard to come inside and share my work space. It is a Crested Anole (Anolis cristatellus), which has a permanent ridge along its back and tail. (Smaller crested anoles with light stripes on their back are either young, or female.)

Anoles are quiet and mostly eat bugs, which I appreciate. (The name rhymes with ravioli.) They are curious, and not scary or threatening. However, this one sometimes shows aggressive behavior if another anole enters its territory – even if it is on the outside of the screen – by doing push-ups and extending the dewlap under its chin.

Anoles are quite plentiful, and a favorite food for the American Kestrels, and Great Egrets living in the neighborhood. Recently I saw a kestrel blast over and snatch an anole up from the ground just outside the porch in a split-second attack. It definitely would have been safer inside the house.

Kestrels in the Virgin Islands seem to mostly eat anoles. (Source photo by Gail Karlsson)

Outside the front door is a small entry deck, where my husband puts a bowl of kibbles for the neighborhood cats. If they don’t finish it, a Ground Lizard (Ameiva exsul) might stop by to grab a bite. This lizard is sometimes called a ‘skink’ in the Virgin Islands, although that name generally refers to a different, rarer species. The ground lizard is larger and beefier than the anoles, with a snake-like body. It moves very quickly, swinging from side to side, more like a ‘slink’.

A ground lizard came by to eat a few kibbles from the cats’ dish. (Source photo by Gail Karlsson)

There is an old teak chair by the door, which for some reason recently attracted a bright, young Green Iguana. They don’t usually come into the house, though there was that time when my son’s girlfriend came to visit and reached into her suitcase to find an iguana sitting in there. Someone must have left the door open.

A juvenile green iguana came to sit on the outdoor chair. (Source photo by Gail Karlsson)

These iguanas get darker, spiky-backed, and considerably less attractive when they get larger – especially when one decides to take a dip in the pool.

An adult green iguana decided to cool off in the pool. (Source photo by Gail Karlsson)

I had another eek! moment recently when I got out the large pasta pot and something dark was crawling around in it. After I jumped, I realized it was not a gross roach, but a Dwarf Gecko (Sphaerodactylus macrolepus), which some people call a ‘wood slave’. They are nocturnal, and I only seen them occasionally, like when I move a picture frame on the wall and one is sleeping behind there and quickly runs off.

I have never been able to get a good look at one, so I grabbed my camera and took a few shots of this one before it crawled up the side of the pot and hopped out.

The photos turned out to have a surprisingly existential quality, I thought, capturing the general feeling of safer-at-home isolation, confinement and vertigo.

A dwarf gecko was quarantining in the pasta pot. (Source photo by Gail Karlsson)

Gail Karlsson is an environmental lawyer, writer and photographer – author of The Wild Life in an Island House, plus the guide book Learning About Trees and Plants – A Project of the Unitarian Universalist Fellowship of St. John. See uufstjohn.com/treeproject and gvkarlsson.blogspot.com. Follow her on Instagram @gailkarlsson

Sneaking into SoCal: the Brown Anole’s Rapid invasion of Orange County, USA

By Lelani Del Pinto & Samuel Fisher 

Southern California has remained relatively unaffected by invasive reptiles for the past few decades. While there have been few invasive species noted, Californians use of citizen science tools has made it easier to detect novel invasive species.  One source of invasive species passage is plant nurseries. Multiple sources studying invasive species across the world have noted they have played a major role in various A. sagrei invasions.

At our sites we found plant nurseries at three out of the five survey locations. Anolis sagrei was first detected during an invasive lizard survey in which we (Lelani Del Pinto and Samuel Fisher) were determining the spread of parthenogenetic whiptails (Aspidoscelis sonorae) from Arizona, when we stumbled upon the unexpected A. sagrei population.  A new survey began immediately among a tiny strip mall and not one but approximately 30 A. sagrei were seen.

With a new mission in hand, we next turned to iNaturalist which showed a few scattered records of A. sagrei across Orange County. None of the citizen records were from the strip mall at which we conducted our first survey. Doing a literature search, we found one short note about A. sagrei in California, but no other publications for the state. We established five separate sites based on iNaturalist records as well as the other population we found. After that we surveyed all of the sites and accounted for all of the lizard species seen.

Each site with citizen records proved to have at least a couple of hectares of invaded A. sagrei land. Our methodology was focused on trying to understand the total distance the separate A. sagrei populations had spread; by trying to create a minimum convex polygon, we hoped to get an idea about the minimum size of each of these disjunct populations.

As we were already keeping track of all lizard species we found, we quickly noticed a somewhat problematic trend. It seemed that in localities where A. sagrei was present, the native Sceloporus occidentalis was nowhere to be found. Due to the lack of presence of S. occidentalis in the surveyed sites in which A. sagrei was observed, we think there is reason to pursue further surveying to ensure our native western fence lizard is not threatened by this invader.

While the full extent of the invasion is yet to be determined, further studies could prove the issue is more problematic than anticipated, especially if more A. sagrei come into California and eventually establish through the help of the nursery trade. Secondly any downstream effects caused by invasive A. sagrei should be closely watched because extirpations of S. occidentalis may prove troublesome. Sceloporus occidentalis is known to have an important role in our ecosystem and reduces lyme disease.

The results of our study help to show that within southern California, A. sagrei has the potential to become an invader as it has in many other places such as Florida, Hawaii, and Texas. The impact of the potential A. sagrei invasion in southern California will hopefully be further studied and handled appropriately.  We hope you check our paper out to learn the details about where brown anoles have recently spread!

References                                

Fisher SR, Del Pinto LA, Fisher RN. 2020. Establishment of brown anoles (Anolis sagrei) across a southern California county and potential interactions with a native lizard species. PeerJ 8:e8937 https://doi.org/10.7717/peerj.8937

Mahrdt CR, Ervin EL, Nafis G. 2014. Geographic distribution: Anolis sagrei (Cuban Brown Anole). Herpetological Review 45:658–659.

 

Hurricane-blown Anoles are a NY Times Cartoon!

Communicating anole science to the public recently reached dizzy new heights as anoles were immortalized in a New York Times cartoon!

Scientists studying lizards in the Americas found that populations in regions battered by hurricanes have larger toe pads that help them hang on in high wind. It’s proof that extreme weather events can alter the course of a species.” Artist: James Yang

 

The cartoon was published in relation to a recent study in PNAS investigating how hurricanes may drive the evolution of anole toepads by Colin Donihue et al.

Dewlap Size and Seasonality in Mexican Anoles

Figure 1. Some examples of “typical” species found in seasonal and aseasonal environments in Mexico. Please forgive the terrible lighting of the Seasonal photos.

Reprinted from the pages of BioMH: Biology of Mexican Herps:

In 1984, Henry Fitch and David Hillis published a paper on mainland anoles that grabbed my attention decades later as I began my graduate research. In that paper, they described a number of dewlap traits and found that many dewlap scale traits were useful for species identification. They also found an interesting correlation between male dewlap size and habitat type. Species with large male dewlaps were associated with habitats in highly seasonal environments such as deserts and thorn-scrub, while those with small male dewlaps inhabited cloud forests and tropical rainforests (Fig. 1). Why might such an association exist?

Fitch and Hillis proposed a sexual selection hypothesis to explain the pattern. After all, Fitch had previously found decreased sexual size dimorphism (SVL) in anole species associated with stable environments such as cloud forests and rainforests (1976). One interpretation of this pattern is that the intensity of sexual selection is reduced in species that can breed throughout the year, decreasing body size dimorphism between the sexes. Fitch and Hillis also found increased body size dimorphism in species that had large dewlaps and lived in seasonal environments (1984). Since anoles living in highly seasonal environments can have shortened breeding seasons linked to precipitation (Fleming & Hooker 1973), the Fitch-Hillis Hypothesis posits that constraints in length of the breeding season increases male dewlap size due to strengthened sexual selection (1984).

Using new datasets for Mexican anoles, we re-investigated support for the Fitch-Hillis Hypothesis at two scales. We performed “macro” analyses across over 40 Mexican anole species and also looked at the Anolis sericeus group, the only group that occurs broadly throughout seasonal and aseasonal habitat types. In our study, we were able to do two important things differently than the original study. The first is that we were able to treat seasonality as a continuous variable thanks to modern GIS tools and environmental data (Hijmans et al. 2005), enabling a finer-scale look at the link between male dewlap size and seasonality. The original study treated seasonality as a categorical variable (“seasonal” vs “aseasonal”). The second difference is that we were able to correct for phylogenetic non-independence of species. To put it simply, species may be similar in dewlap size due to relatedness to other species (evolutionary history) rather than to the seasonality environment they inhabit. To do this, we used a recently-published phylogeny (Poe et al. 2017) and phylogenetic regression (PGLS) to verify the results of the previous study.

Interestingly enough, our standard ordinary least squares (OLS) regression analyses duplicated results from the original study; without accounting for evolutionary history, there is indeed a strong correlation between male dewlap size and seasonality in Mexican anoles (Fig. 2A, black line). Being able to replicate results using different datasets and approaches is very important and not as common as many of us scientists would like. However, as reflected in the more flattened red dotted line in the figure below, the correlation is weakened substantially after accounting for phylogeny. We therefore cannot say with confidence that seasonality affects male dewlap size in Mexican anoles.

Figure 2. Regression results from Gray et al. (2020). (A) Results from our “macro” analyses, with black line representing standard OLS regression results and red dotted line representing the PGLS results. (B) Results for the Anolis sericeus complex, with black line representing results for all three major lineages and red dotted line representing results of the Pacific and Caribbean lineages. See paper for further details or please ask questions in the comment section below!

We were not able to perform phylogenetic regressions on the Anolis sericeus complex, unfortunately. Though several of us published a phylogeographic study on the silky anoles, many populations represented in the dewlap dataset were not included in that work (Gray et al. 2019). Therefore we had to come up with another way to investigate a correlation in silky anoles. Our phylogeographic work discovered three clades which we assigned Pacific, Caribbean, and Yucatan. Incidentally, the Yucatan lineage is diagnosed in part by small male dewlap size (Lara-Tufiño et al. 2016). The Yucatan lineage also occurs in relatively aseasonal environments that fall within the conditions inhabited by the Caribbean lineage (Gray et al. 2020). So after running regressions on all populations (Fig. 2B, black line), we also ran regressions on only the Pacific and Caribbean lineages, which collectively experience the broadest range of seasonality environments (Gray et al. 2020). As you can see in the figure above, removing the Yucatan lineage flattens the regression line and makes it clear the correlation between male dewlap size and seasonality in silky anoles is influenced by phylogenetic history (Fig. 2B, red dotted line).

Does this mean seasonality is not a driver of male dewlap size? Not necessarily. We discuss other possibilities in the paper, including that anole lineages in Mexico may not have “switched” environments enough for us to be able to detect an effect. We found strong phylogenetic signal for seasonality in Mexican anoles, suggesting species from lineages preferring seasonal environments do not often switch to aseasonal environments and vice versa. As an example, one lineage of 14 west Mexican anoles consists of species that tend to have large dewlaps and live in seasonal environments. In that clade, having a large dewlap might be traceable to one evolutionary event when the most recent common ancestor of the clade evolved a large dewlap. Sexual selection and a truncated breeding season might have had something to do with that event…or the ancestor may have evolved a large dewlap for other reasons and extant species maintained the trait.

While the final result may not be super exciting, I enjoyed working on this project. Collectively, I spent about one year in Mexico catching lizards during grad school and our sample size for some species still left a lot to be desired. Datasets like this take a lot of time and effort to generate! A lot of friends and collaborators helped find and photograph animals through the years. I want to thank Adam Clause, Luke Mahler, Eric Schaad, and Britt White for taking some of the best dewlap photos in our collection.

If anyone wants to play around with the data, they are available at Dryad. And the paper is open access and short, so check it out!

References

Fitch HS (1976) Sexual differences in the mainland anoles. Occasional papers of the Museum of Natural History, the University of Kansas, 50:1-21.

Fitch HS, DM Hillis (1984) The Anolis dewlap: Interspecific variability and morphological associations with habitat. Copeia, 1984:315-323.

Fleming TH, RS Hooker (1973) Anolis cupreus: the response of a lizard to tropical seasonality. Ecology, 56:1243-1261.

Gray LN, AJ Barley, S Poe, RC Thomson, A Nieto-Montes de Oca, IJ Wang (2019) Phylogeography of a widespread lizard complex reflects patterns of both geographic and ecological isolation. Molecular Ecology, 28:644-657.

Gray LN, AJ Barley, DM Hillis, CJ Pavón-Vázquez, S Poe, BA White (2020) Does breeding season variation affect evolution of a sexual signaling trait in a tropical lizard clade? Ecology and Evolution, 10:3738-3746.

Hijmans RJ, SE Cameron, JL Parra, PG Jones, A Jarvis (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25:1965-1978.

Lara-Tufiño JD, A Nieto-Montes de Oca, A Ramírez-Bautista, LN Gray (2016) Resurrection of Anolis ustus Hallowell, 1856 (Squamata, Dactyloidae). Zookeys, 2016:147-162.

Poe S, A Nieto-Montes de Oca, O Torres-Carvajal, K de Queiroz, JA Velasco, B Truett, LN Gray, MJ Ryan, G Kohler, F Ayala-Varela, I Latella (2017) A phylogenetic, biogeographic, and taxonomic study of all extant species of Anolis (Squamata: Iguanidae). Systematic Biology, 66:663-697.

Free Online Course: Landscaping for Lizards

On Wednesday, May 20 at 4:00PM EDT, the University of Florida IFAS Extension Service is hosting a free online course! Here’s the event description from the website.

Learn about how you can landscape for lizards! We will cover many of the species you may see in Northeast Florida, the many benefits to having them around, and what you can do you in landscape and garden to support and protect them.

This is a free online course but registration through Eventbrite is required and the class is limited in size to 80 participants.

The cover photo for the event features a green anole (Anolis carolinensis, also pictured above), so expect some discussion of our beloved anoles. If you attend, please comment below and let us know what you learned!

You can register for the course here.

Anoles Love It When Ant and Termite Nests Get Opened

Lepidoterist and keen naturalist Andrei Sourakov from the Florida State Museum posted this photo on Twitter.

This is actually an effective, if somewhat mean to the little insects, way of watching anoles, as Stan Rand noted in his 1975 paper of A. agassizi: “In the West Indies, a well-established method for attracting large numbers of anoles is to break open a termite nest. Under such conditions, large numbers will often gather and feed actively with little aggressive interaction.”

 

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