Author: Travis Hagey

Evolution 2019: How Many Species of Anolis distichus?

Anolis distichus is a highly variable species from Hispaniola. It’s especially variable in its dewlap color, ranging from white, to orange, to red. In the past, A. distichus has been broken up into 16 subspecies based on its dewlap variation! Previous work by Rich Glor and his students used genetic data to identify six candidate species, although these six candidate species didn’t correspond well with the 16 dewlap-based subspecies.  In order to get a better handle on how justified these candidate species are, undergraduate Tanner Myers, working with Pietro Longo Hollanda de Mello and Rich Glor, from the University of Kansas, presented a poster titled Identifying species when boundaries are blurred.

Myers collected morphological data from populations of A. distichus from across Hispaniola. The authors expected their morphological data to also partition along with the previously identified genetic candidate species. They found this to not be the case!  When the authors looked at their morphological data (linear body, limb, and head measurements), to see if these 6 candidate species had any morphological divergence, they found no strong pattern. All of the candidate species clustered together to support one morphological group. In the end, the authors suggest that Anolis distichus may represent a highly variable group in in the early stages of speciation, but at this point, they do not support any taxonomic revisions of the species.

Tanner Myers will be starting graduate school with Jamie Oaks at Auburn University in the fall.

SICB 2019: Anole Setal Morphological Diversity

An anole toepad imaged with a scanning electron microscope.

In the endless comparison between the adhesive systems of geckos and anoles, today we learned a bit more about anole toe pads. University of Akron grad student Austin Garner, from the Peter Niewiarowski and Ali Dhinojwala labs, presented a poster on setal morphology across the toe of Anolis (Deiroptyx) equestris or the Cuban Knight anole. Like a lot of studies on toe pads, the inspiration for this work can be traced back to a previous study by Tony Russell (Johnson and Russell. 2009. Journal of Anatomy). In their 2009 study, Johnson and Russell found that the more distal lamellae of Rhoptropus geckos were more narrow and that their distal setae were longer, lower in diameter, and more densely packed within and across lamellae. This study came to shape our knowledge of within-toe gecko setal morphology.

Today Garner presented preliminary data evaluating the same patterns in an anole. Although their numbers are very preliminary (N=2), it suggests some interesting deviations from Rhoptropus. The more distal lamellae of equestris are narrower, similar to Rhoptropus. Distal setae are also more densely packed, but setae seem to be the longest and have the widest diameter in the middle of the lamellae, and in the middle of the toe, which is very different than what was observed in Rhoptropus. 

If this pattern holds as Garner et al. increase their sample size, it will have interesting implications for how we think about toe detachment in geckos and anoles and well as how the two groups navigate rough and smooth surfaces. I am really excited to see what patterns emerge from the study and so stay tuned to see how their results shake out!

SICB 2019: Sexual Differences in Relative Lengths of Toes

Today I had the pleasure of attending an excellent talk by University of Florida undergraduate Griffin McNamara. I was really impressed with the work he presented, especially for an undergraduate.

McNamara was investigating the ratio in digit length between the 2nd and 4th digits. This is interesting because in mammals, especially humans, this ratio is sex specific, with men typically having longer ring fingers than pointer fingers. A lot of research has looked into the developmental reasons for this, with a likely relationship to hormone exposure of the developing fetus. Applying these ideas to anoles makes sense because the toe of anoles are somewhat unique in lizards, as we all know here. McNamara is looking into if sexual dimorphism in 2nd and 4th digit length was also present for anoles.

McNamara wasn’t the first person to measure this in anoles, but he was the first to use cleared and stained specimens, which likely greatly improved his ability to accurately measure digit length. Interestingly, he found that the pattern was reversed, with males having longer 2nd digits, not longer 4th digits as in mammals. In addition, this pattern didn’t show up until a lizard’s teenage years, with juvenile anoles not showing a difference between the sexes. Using cell staining to visualize dividing cells, he was able to narrow down the digit discrepancy to growth in the 2nd phalanx during sexual maturity.

Suspecting that this late onset dimorphism might still be related to hormone exposure, McNamara got his fingers on some testosterone-treated female anoles from collaborators and found that they had “masculinized” digit ratios, although not as much as true males.

I thought this was a great study, combining old school cleared-and-stained approaches with cell biology and experimental endocrinology. It also opens up lots of interesting questions. Is there an adaptive reason that mammals and lizards have sexually dimorphic digit lengths? Is it just a quirk of development? Does this digit length reversal have anything to do with the fact that the shape of anoles’ rear feet is already kind of mirrored as compared to our hands?

Anoles versus Geckos: The Ultimate Showdown

Two green lizards in Miami, one of each variety.

Two green lizards in Miami, one of each variety.

History is rich with great rivalries; David versus Goliath, Red Sox versus Yankees, Alien versus Predator, but one of the greatest match ups of our time is anole lizards versus gecko lizards. For readers of this blog that are unfamiliar, for which I assume there are few, geckos and anoles are well matched competitors because of their morphological and ecological similarities. Geckos (infraorder Gekkota) are the earliest branch on the squamate tree (sister to all other lizards and snakes) with over 1500 species around the globe, whereas anoles (genus Anolis) appeared roughly 150 million year after the origin of geckos (nested within the Iguania infraorder). The roughly 400 species of anoles can be found primarily in Central and South America. Geckos and anoles both independently evolved very similar hairy adhesive toe pads that help them adhere to and navigate vertical and inverted surfaces. While anoles can likely trace their toe pads to a single origin (and one loss in A. onca), toe pads likely arose and were lost multiple times within Gekkota, although we are still sorting out the exact details (Gamble et al., 2017). Nearly all anoles are arboreal and diurnal, with only a handful of terrestrial or rock dwelling species. Conversely, geckos can be found thriving in arboreal as well as rocky and terrestrial microhabitats day and night.

While anoles tend to get all of the attention from evolutionary ecologists, with decades of amazing research quantifying their habitat use in the Caribbean, geckos are actually older, with more ecological and morphological diversity. As my prior PhD advisor Luke Harmon can surely confirm, I have been interested in knowing how or if insights from Caribbean anole ecomorphology can be applied to geckos. How similar is the evolution and diversification of geckos and anoles? Do geckos partition their habitat along similar dimensions as Caribbean anoles?

In this post, I’d like to share some of my previous work comparing and contrasting gecko and anole diversification and habitat use and then solicit information and opinions from the anole community for an upcoming field trip in which we will be looking at habitat use of sympatric introduced geckos and anoles.

figures

Fig 1. Our reconstruction of gecko (blue) and anole (green) ancestral toe pad performance based on our best fitting weak OU model of trait evolution. Horizontal bars below the X-axis represent the region in which we constrained the origin of toe pads for each clade. Detachment angle (y-axis) represents our measure toe pad performance (the maximum ratio of adhesion and friction a species can generate). The generation of more adhesion for a given amount of friction results in a higher detachment angle. Shaded bands represent our estimated OU optimum value for each clade. Figure modified from Hagey et al. (2017b).

In 2017, we had two great papers come out investigating the diversification of toe pad adhesive performance in geckos and anoles, and the ecomorphology of Queensland geckos. In our diversification paper (Hagey et al., 2017b), we found that while geckos are an older and larger group than anoles, their toe pad performance does not appear to be evolving towards a single evolutionary optimum. Instead, we found that Brownian motion with a trend (or a very weak Ornstein-Uhlenbeck model) best modeled our data, suggesting geckos have been slowly evolving more and more diverse performance capabilities since their origin approximately 200 million years ago (Fig 1). These results assume a single evolutionary origin of Gekkota toe pads, which was supported by our ancestral state reconstructions, but ancestral state reconstructions are far from a perfect way to infer the history of a trait. And so for now, the true history of the gecko toe pad’s origin(s) remains a ‘sticky’ issue. Conversely, adhesive performance in anoles appears to be pinned to a single optima in which anoles quickly reached after their split from their padless sister group (i.e. a strong Ornstein-Uhlenbeck model, Fig 1).

Given these results and the fact that geckos are such a morphologically diverse group, living on multiple continents in many different microhabitats, our results suggest the adhesive performance of geckos may be tracking multiple optima, and when pad-bearing geckos are considered together as a single large group, could produce the general drifting pattern we observed when we assume their ancestor started without little to very poor adhesive capabilities. On the flip side, we can imagine multiple reasons why anoles appear to be limited in their toe pad performance. Perhaps anoles lack the genetic diversity to produce more variable toe pads or they are mechanically or developmentally constrained to a limited area of performance space. Alternatively, since anoles are nearly all arboreal and diurnal in new world tropical environments, it is possible that they are all succeeding in the same adaptive zone and there isn’t the evolutionary pressure or opportunity to evolve more diverse performance capabilities. Closer studies of the adhesive performance capabilities of the few anoles species that have branched out from arboreal microhabitats, such as the rock dwelling aquatic species would be really interesting!

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Fig 2. Our gecko and anole residual limb length calculations suggest geckos (grey triangles) generally have shorter limbs then anoles (black circles). Figure modified from Hagey et al. (2017a).

In our second paper from 2017 (Hagey et al., 2017a), we quantified microhabitat use and limb lengths of geckos across Queensland, Australia and compared these patterns to those known from Caribbean anoles. We found some interesting differences and similarities. Our first result arose as we tried to calculate residual limb lengths and realized that geckos, as a group, have shorter limbs than anoles, which resulted in us calculating residual limb lengths for geckos and anoles separately (Fig 2). We then compared microhabitat use and limb length patterns and found that Strophurus geckos may be similar to grass-bush anoles. Both groups have long limbs for their body lengths and use narrow perches close to the ground. We also found other general similarities such as large bodied canopy dwelling crown-giant anoles and large bodied canopy dwelling Pseudothecadactylus geckos. Unfortunately, we didn’t focus on sympatric Australian geckos and so we couldn’t make direct habitat partitioning comparisons to anoles. We hope to fix that in our next project and would really love to hear from you, the anole community.

Later this spring, I am planning a fieldtrip with John Phillips and Eben Gering, both fellow researchers here at Michigan State University, to Hawai’i (Kaua’i and O’ahu) to investigate habitat partitioning of invasive geckos and anoles, specifically A. carolinensis, A. sagrei, and Phelsuma laticauda. Jonathan Losos one claimed that Phelsuma are honorary anoles! These three species are all diurnal, arboreal, have adhesive toe pads, and are commonly seen in Hawai’i and so we expect them to be competing for perch space. This has been on some of the greatest anole minds since at least 2011 with Jonathan wondering which group would win when the two clades collide in the Pacific. Previous studies of anole ecomorphs across the Greater Antilles and invasive A. sageri in the southeastern US give us a good expectation of how the trunk-crown A. carolinensis and the trunk dwelling A. sagrei should interact and partition their arboreal microhabitat, with A. sagrei pushing A. carolinensis up the trunk. The wild card is P. laticauda. There hasn’t been much microhabitat use work done with Malagasy geckos, and definitely nothing compared to the extensive work with Caribbean anoles. As a result, I don’t know much about exactly what part of the arboreal environment P. laticauda uses in its natural range or how it will fit in with its new pad-bearing brethren in Hawai’i. The best information we have to my knowledge is a study of other arboreal Phelsuma by Luke Harmon in Mauritius (Harmon et al., 2007). He found that while the Phelsuma geckos of Mauritius also partition their arboreal habitat by perch height and somewhat by diameter, they also partition by palm-like or non-palm-like perches. I’m not aware of any anole observations suggesting a palm/non-palm axis of partitioning and so this may be a novel axis that P. laticauda is using in Hawai’i to live in amongst the anoles.

Anoles, geckos, and Hawai’i have come up repeatedly here on Anole Annals

Reproductive Biology of Introduced Green Anoles in Hawaii

JMIH 2016: Anolis vs. Phelsuma in Hawaii

Amazing Green Anole Battle In Hawaii

More On Anoles And Day Geckos In Hawaii

Anoles And Banana Flowers In Hawaii

Fighting Hawaiian Anoles

Brown Anoles on Hawaii and Battle of the Intercontinental Convergents

Many Hawaiians Don’t Like Brown Anoles

SICB 2018: Unraveling Natural and Human-Mediated Founder Events in Anolis carolinensis

Factors Restricting Range Expansion for the Invasive Green Anole Anolis carolinensis on Okinawa Island, Japan

Anole Watercolor Available on Etsy

A Failed Anole Predation Attempt

This Is Not A Madagascan Day Gecko

Battle of the Diurnal, Arboreal Exotics in Florida (the Anole Loses)

Strange perch mate

Green Anole Mayhem

and so we know folks have been thinking about these species and specifically this invasive set of species for a while. We are especially excited to see Amber Wright’s research suggesting P. laticauda was perching above A. carolinensis in her enclosures. We want to know what the anole community has to say. We also don’t want to duplicate or intrude on any projects that are already under way.. If this is something you’ve already started, or started to wonder about… let us know! We would love to collaborate, partitioning interesting questions, if there are already labs working in this arena. We would also be grateful for suggestions, field site recommendations, or relevant publications we may have missed.

 

JMIH 2016: Genetic Evidence of Hybridization between the Native Green Anole (Anolis carolinensis) and the Invasive Cuban Green Anole (A. porcatus)

Photo by James Stroud

Photo by James Stroud

At JMIH 2016, I chatted with Johanna Wegener, a graduate student at the University of Rhode Island in Jason Kolbe’s lab, about her poster detailing her work identifying hybridization between Anolis carolinensis and A. porcatus in southern Florida.

Interspecific hybridization in anoles is thought to be fairly rare, with the best-known example being hybridization between Anolis carolinensis (native to the southeastern U.S.) and A. porcatus (native to Cuba) in southern Florida. I was surprised to learn how little we know about this rumored hybrid zone.

A. porcatus was likely introduced into Florida within the last few decades, but the striking morphological similarities between A. carolinesis and A. porcatus make anecdotal reports of hybridization hard to confirm. Wegener conducted the first genetic analyses of hybridization between A. carolinesis and A. porcatus. She genotyped 18 nuclear microsatellites from green anoles in Florida (Palm Beach and South Miami) and western Cuba and conducted a STRUCTURE analysis and found support for three genetic clusters consisting of Cuban A. porcatus, and two Floridian groups (one from Palm Beach and one from South Miami). With the addition of the mitochondrial ND2 marker, she found that the South Miami population had both A. carolinensis and A. porcatus haplotypes. Interestingly, there appeared to be very few recent hybrids; instead, the hybrid group appeared distinct from either parent group, suggesting that hybridization has been occurring for several generations.

In addition, Wegener looked at the variation in A. porcatus and A. carolinensis markers in each hybrid individual and found examples of some parent markers being retained at high proportions in the hybrids, possibly suggesting the retention of beneficial parent alleles in the hybrids.

Given that this study was only conducted at two sites in Florida, the exciting next step of this study is to better quantify the genetic makeup of hybrids across southern Florida and map out the hybrid zone.

Temporal Variation in Structural Microhabitat Use of Phelsuma Geckos in Mauritius

Phelsuma ornata

I want to start by thanking Anole Annals for the offer to write a post not about anoles, but about a group of honorary anoles, Phelsuma geckos (Losos, pers. comm.). Our recent publication (Hagey et al. 2016) looked at how Phelsuma ornata, P. guimbeaui, and P. cepediana use their environment in Mauritius over the course of the day.

Understanding how species use their environments is a fundamental step to understanding how they’ve evolved and adapted. Extensive previous work has been collecting observations and quantifying the microhabitat use of anoles and other lizards. As we all know on this blog, Caribbean anoles can be organized into ecomorphs, species with convergent morphologies and microhabitat preferences. The microhabitat use patterns of these species are so critical that the names of the ecomorphs represent their habitat preferences. After quantifying the habitat preferences of a set of species, however, often little thought is then given to how this preference may vary seasonally or over the course of a day.

Back in 2002, Luke and Lisa Harmon collected observations of Phelsuma geckos on the island of Mauritius to investigate how these “pseudo-anoles” may be partitioning their microhabitat. They found that Phelsuma partition their habitat structurally, with species using palm or non-palm vegetation (Harmon et al. 2007). In addition, Luke and Lisa collected temporal information, observing the perches that Phelsuma use over the course of the day. With these data, we hypothesized that sympatric species would have complementary activity patterns, reducing the time in which species overlap using the same perches.

We did find that Phelsuma vary their microhabitats, moving to larger diameter and lower perches later in the day, but these changes don’t reduce microhabitat use overlap between sympatric species. Alternatively, species may be moving to track sunlight for thermoregulation, following prey, or avoiding predators. These temporal microhabitat changes are likely to be important for how Phelsuma interact with their environment. We therefore feel that temporal microhabitat and activity variation should be considered more often when quantifying a species’ microhabitat preferences, as it may be an important aspect of a species’ niche (see Pianka 1973; Schoener 1974).

Hagey, T. J., N. Cole, D. Davidson, A. Henricks, L. L. Harmon, and L. J. Harmon. 2016. Temporal Variation in Structural Microhabitat Use of Phelsuma Geckos in Mauritius. J Herpetol 50:102-107.
Harmon, L. J., L. L. Harmon, and C. G. Jones. 2007. Competition and community structure in diurnal arboreal geckos (genus Phelsuma) in the Indian Ocean. Oikos 116:1863-1878.
Pianka, E. R. 1973. The Structure of Lizard Communities. Annual Review of Ecology and Systematics 4:53-74.
Schoener, T. W. 1974. Resource Partitioning in Ecological Communities. Science 185:27-39.

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