Miami Exotic Lizard Safari

A very ambitious brown anole

A very ambitious brown anole

I arrived a day early for the 2018 Anolis Symposium. When it became clear I was not needed to help get things ready, I did what any red-blooded anolologist would do: I headed off for All-America Park, the hottest of hotspots for Miami anoles.

And what a day it was. Two minutes after leaving my hotel, I saw what I’m pretty sure was an Ameiva, though I didn’t get a good look. Then red-headed agamas underneath the monorail on the Dixie Highway.

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Plenty o’ iguanas. How many can you find?

How many green iguanas can you find?

How many green iguanas can you find?

And curly-tailed lizards!

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Along the way, I also saw three introduced anoles: (A. sagrei, A. cristatellus and A. distichus).

Anolis distichus

Anolis distichus

Finally, I got to All-America Park and immediately met five-term South Miami mayor Phil Stoddard, who doubles as a crackerjack neuroethologist at Florida International University, and is a great naturalist to boot. We walked around the park looking for Anolis garmani, the Jamaican giant anole, but without success. There were plenty of other anoles at the Park, all the same ones I’d already seen, but also a knight anole and 13 green anoles–they definitely are doing just fine despite all the invasives. The lizard search was conducted to a soundtrack of screeching peacocks and the occasional flock of parrots flying back. I love Miami! Sadly, no Jamaican giant anoles, A. garmani. That’ll have to wait for a return visit.

Anolis equestris at All-America Park

Anolis equestris at All-America Park

Anolis Symposium Tomorrow!!!

Fairchild Botanical Gardens, site of the 2018 Anolis Symposium

It’s not to late to hop on a plane and get to beautiful Fairchilds Botanical Garden! Abstracts are posted. Here’s the schedule:

9:00 – 9:30 James Stroud Florida International University
Introduction and Welcome

9:30 – 9:45 Michele A. Johnson Trinity University
Physiological mechanisms underlying behavioral convergence in Caribbean anoles

9:45 – 10:00 Tony Gamble Marquette University
Anolis sex chromosomes, past, present, and future

10:00 – 10:15 Rosario Castañeda Universidad Icesi
When did anoles diverge? An analysis of multiple dating strategies

10:15 – 10:30 Colin Donihue Harvard University
Hurricane-induced adaptive shifts in the morphology of an island lizard

10:30 – 10:45 Leo J. Fleishman Union College
Why are there so many yellow dewlaps?

10:45 – 11:30 Coffee Break

11:30 – 11:45 Graham Reynolds University of North Carolina Asheville
Genetic and Morphometric Diversification in the Brown Anole Suggest Early Pathways of Anole Colonization and Evolution in the Caribbean

11:45 – 12:00 Nathalie Feiner Lund University
Transposable elements, Hox gene clusters and genome evolution– How special are Anolis lizards?

12:00 – 12:15 Thomas J. Sanger Loyola University Chicago
The Mechanisms of Thermal Stress Induced Craniofacial Malformation in Lizards Developmental biology

12:15 – 12:30 Sozos N. Michaelides University of Rhode Island
Invasion history of four Anolis lizard species introduced to Bermuda Invasion biology

12:30 – 14:00 Lunch

14:00 – 14:15 Kristin M. Winchell University of Massachusetts Boston
Performance Consequences of Urban Morphological Shifts

14:15 – 14:30 Kenro Kusumi Arizona State University
Comparative Genomics Reveals Accelerated Evolution in Conserved Pathways during Anolis Diversification

14:30 – 14:45 Sean Giery University of Connecticut
Some thoughts on the trophic ecology of Anolis lizards

14:45 – 15:00 D. Luke Mahler University of Toronto
Land use and the restructuring of anole communities across an elevational gradient

15:00 – 15:45 Coffee Break

15:45 – 16:00 Ivan Prates Smithsonian Museum of Natural History
Genomic signatures of adaptation associated with a history of range expansions in South American anoles

16:00 – 16:15 Oriol Lapiedra Harvard University / CREAF
Predator-induced natural selection in behavior Behaviour

16:15 – 16:30 Caitlin C. Mothes University of Miami
Using South Florida’s exotic lizard community to evaluate the use of ecological niche models in predicting biotic invasions

16:30 – 17:00 Neil Losin Day’s Edge Productions
The Lizard’s Tale and Anole Annals v2.0: An enhanced platform for Anolis outreach

17:00
Social & Poster Session

Saturday, 17 March 2018
9:30 – 9:45 Douglas B. Menke University of Georgia
Genome editing methods for the production of genetically modified anoles

9:45 – 10:00 Sarin Tiatragul Auburn University
A shady way to beat the Miami heat

10:00 – 10:15 Joanna O. Palade Arizona State University
Anolis carolinensis satellite cells have expanded musculoskeletal potential

10:15 – 10:30 Gregory C. Mayer University of Wisconsin-
Parkside Using archival DNA to elucidate anole phylogeny Systematics and/or taxonomy

10:30 – 10:45 Liam J. Revell Universidad del Rosario and UMass Boston
Can we detect differences in the rate of discrete character evolution between clades of anoles?

10:45 – 11:30 Coffee Break

11:30 – 11:45 Amber N. Wright University of Hawaii
Predicting the outcome of species interactions in a novel species assemblage: Anolis vs. Phelsuma in Hawaii

11:45 – 12:00 Andrew C. Battles University of Rhode Island
The other Miami Heat: Urban areas alter thermal biology and influence persistence and spread of two invasive Anolis species.

12:00 – 12:15 Nathan W. Turnbough I
Covariation in arthropod community composition and dominant anole identity on dredge spoils islands in Florida

12:15 – 12:30 Cindy Xu Arizona State University
Tail Regeneration in Anole Lizards: Insights from Comparative Genomic Analysis and Reformation of the Peripheral Motor Nervous System

12:30 – 14:00 Lunch

14:00 – 14:15 Michael L. Logan Smithsonian Tropical Research Institute
Using experimental islands to explore evolutionary dynamics under climate change Thermal biology, ecology, or evolution

14:15 – 14:30 Christine Rose-Smyth Verdant Isle Orchids
Role of a sweet-toothed anole in orchid pollination Species interactions

14:30 – 14:45 Christopher J. Thawley University of Rhode Island
Let There Be Light: Widespread Use of Human-Produced Light at Night by Anoles and Its Consequences

14:45 – 15:00 Sean Doody USF St. Petersburg Environmentally Cued Hatching in Anoles Behaviour

15:00 – 15:45 Coffee Break

15:45 – 16:00 Winter A. Beckles University of Miami Signal divergence and habitat partitioning among non-native bark anoles in South Florida

16:00 – 16:15 Stephanie L. Clements University of Miami
Non-native species dominate herpetofaunal community composition in both native and non-native habitat patches in Miami-Dade County

16:15 – 16:30 Zachary A. Chejanovski University of Rhode Island
Predators influence prey body size variation in an urban landscape

16:30 – 16:45 Joshua M. Hall Auburn University
Does season-dependent reproductive value of offspring drive the evolution of life-history traits in Anolis lizards?

16:45 – 17:00 Jonathan Losos Washington University in St. Louis
Concluding Remarks

A New View on Anole Territoriality and Social Structure

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One of our marked lizards for this study. Photo by Jon Suh.

Ambika Kamath has written a synthesis of her two recent papers in territoriality in anoles. It appeared on March 12, 2018 on her blog, Behavioral Ecology, Natural History, Science and Society and is reprinted below:

In my major Ph.D. project, I questioned the idea that territoriality is a good or useful description of Anolis lizards’ mating systems. When I began working on this question, I planned to primarily use an empirical approach, measuring the movement patterns and mating patterns of a population of Anolis sagrei in a way that didn’t depend on territoriality. But anticipating future criticism, I realised that because I’d be working in one population of one species, my empirical work could readily and reasonably be dismissed as an aberration without a broader foundation on which to place it.

This realization led to the historical review in which my Ph.D. advisor Jonathan Losos and I examined the history of research on Anolis territoriality. I’ve written about this historical research quite a bit before, but haven’t said much about the empirical work, leaving the two complementary halves of this project unintegrated. That’s partly been because the empirical work wasn’t published until recently. But it’s also because in contextualizing the problem tackled by the empirical paper, I have to basically recount the whole of the historical review. There really hasn’t been room to talk about both in a single venue, and there still isn’t, but I’m going to tell you a bit more about the empirical paper to balance things out. You’ve heard a little about it before–I wrote field notes about one of the males in this study (interesting addendum: U131 fathered none of the offspring of the females he encountered!) and about a tiny survey of green anoles that we conducted concurrently.

The empirical paper is now published, in the Proceedings of the Royal Society B! Here’s an awesome press release about the study from UCSB that will give you the gist of it, but in short what we did was:

  • Catch and mark almost every lizard we saw, and then measure the spatial locations of as many lizards as we could by repeatedly surveying as big an area as we could.
  • Make a map of all the trees within our sampling area.
  • Measure the body size and estimate the population-level growth rate of males
  • Collect a subset of the females, bring them into the lab, and collect the DNA of their offspring.
  • Devise a mathematical approach to estimating encounters between males and females from data on their spatial locations. Combined this with the growth-rate estimate to calculate the size of males at their encounters with females.
  • Use DNA sequencing to figure out the likely fathers of the females’ offspring; we leaned on the estimates of male-female encounters to do so.
  • Use a clever and (I think!) pretty original approach to quantifying sexual selection on body size and movement patterns by comparing the traits of males that encountered females to the traits of the subset of those males that actually fathered offspring.

In sum what we found was that male and female movement patterns spanned larger areas and were more dynamic than many of us had previously imagined, that females encounter multiple potential mates, that at least 60% and possibly up to 80% of females  mate with multiple males, and that sexual selection acts on male body size as well as males’ spatial extent and the timing of male-female encounters. I’ll let you read the press release and the paper itself to learn more about what we found (here it is on BioRxiv, essentially the same paper but freely accessible)!

Viewed together, I hope the historical and empirical papers make a convincing case that we’ve been looking at Anolis mating systems in a limited way for a long time, and that other, newer ways of quantifying mating systems in ways that don’t depend on territoriality can yield both interesting and sensible results. I see this work as opening up an arena of questions, both in Anolis and in other taxa where mating systems have been described in a static way for a long period of time.

I’m very proud of this paper. I remember a phase of grad school when I found it impossible to convince people that this work would turn out interesting, or maybe it was just that my own self-doubt prevented me from seeing others’ interest and support for this research. It remains true that this is one study of one population of one species, and it may well be that I turn out to be all wrong. Perhaps new explorations of Anolis mating systems will eventually lead us back to territoriality. But even if that’s the case, I feel confident that, thanks to this work, we’ll be able to approach that or any description of Anolis mating systems with clearer, more skeptical, and more discerning eyes.

This won’t be the last you’ll be hearing from me on this subject of lizard mating systems; for one, there are responses to our historical review that are in the process of being published, and we’ll have a chance to respond to them. I’m very excited to engage in an actual scientific dispute, and will do my best to do so respectfully and productively, especially since I have on-the-record views about what makes such disputes annoying. But in terms of research, I seem to be heading in other directions, which I think will be related to this work but maybe not directly. So I wanted to make sure that I put down here, all in one place, what I see this project as and what I hope it will achieve. Let me know what you think!

A Case of Matestaken Identity: Hybrid Mating between Crested and Brown Anoles!

Somebody needs to work on their anole species identification skills.

Somebody needs to work on their anole species identification skills.

Breeding season is heating up for anoles in Miami, and at least one male crested anole (A. cristatellus) is a little…confused. While collecting some baseline data for my post-doc work looking at impacts of artificial light at night (ALAN) on brown and crested anoles, I noticed a commotion on a nearby cycad. Upon closer inspection, I realized that a male crested anole was pursuing and subsequently mating with a female brown anole (A. sagrei) who was decidedly unhappy about the situation.

In case you’re wondering about the colorful jewelry at the base of their tails, both of the anoles in the photo/video are bead-tagged to allow me to reidentify them from a distance. The copulation here lasted 3-4 minutes a portion of which I managed to capture on video.

While previous reports on AA have documented coupling between A. carolinensis and A. sagrei, I haven’t seen any reports of interspecific mating between A. cristatellus and A. sagrei. Has anyone else observed this phenomenon? The two species do encounter each other quite frequently in the Miami area, so this might not be a rare occurrence. Hybridization seems unlikely given the divergence between these two species, but you never know!

Congratulations Dr. Kristin Winchell!

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Yesterday afternoon Kristin Winchell successfully defended her Ph.D. dissertation at UMass Boston…during a nor’easter! The university was officially closed due to the inclement weather (I myself got stuck in a stairwell for several minutes because I didn’t have card swipe access), but that didn’t stop Kristin from delivering a fabulous talk about her work on urban evolution in anoles.

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Congratulations Kristin!! And can you believe this cake?!?!

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James T. Stroud, PhD!

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The latest Dr. Anole…but not for long! Stroud wowed a packed house at Florida, regaling the audience with four chapters of research, two of which are already published in Annual Review of Ecology, Evolution & Systematics and Invasion Biology (2 of the ca. 40 papers he published during his time at FIU. The self-proclaimed highlight of his work? Publishing on T. rex!

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Congratulations, James!

Big Day Tomorrow: Two New Anole Doctors!

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In an event probably unprecedented in anole history, two new anole doctors will emerge tomorrow. After a multi-year incubation, AA stalwarts Kristin Winchell and James Stroud will hatch tomorrow almost simultaneously. James will get the festivities rolling at 11 a.m. eastern time in Miami: 

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Kristin follows shortly thereafter at 1 p.m. in Boston:

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By this time tomorrow, the ranks of Dr. Anolis will be increased by two. Congratulations Kristin and James!

Reproductive Biology of Introduced Green Anoles in Hawaii

Anolis carolinensis on Kauai. Photo by Jonathan Losos.

Anolis carolinensis on Kauai. Photo by Jonathan Losos.

Green anoles (A. carolinensis) have been introduced to a number of Pacific islands, including Hawaii. In a recent paper in Current Herpetology (published by the Herpetological Society of Japan), Goldberg and Kraus examine the reproductive cycle of Hawaiian green anoles and find it very similar to what occurs in their native range.

Here’s the abstract of the paper:

Reproduction was studied in an invasive population of Anolis carolinensis in the Hawaiian Islands, USA. Timing of events in the reproductive cycle was similar between A. carolinensis populations in Hawaii and native populations of the species in the southeastern United States. In Hawaii, males of A. carolinensisundergo a prolonged period of spermiogenesis (sperm formation) starting in November (n=1) and December (n=1) and continuing into August. Gravid A. carolinensis females in Hawaii (n=40) produce one egg in continuous succession from March into August. Reproductive activity in A. carolinensis in Hawaii ceased prior to the colder, wetter, winter months.

Invasive Lizard Meets Native Lizard: the Cartoon!

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Our article was recently published in BJLS (Dufour, Herrel and Losos 2017)!

For the occasion, I made this short comic to pique your curiosity!

Will Chris’ (Anolis cristatellus) and Z’Andy (Anolis oculatus) endure the pressure of a new cohabitation?

Find out more here: https://academic.oup.com/biolinnean/article-abstract/123/1/43/4627047

Ecological character displacement between a native and an introduced species: the invasion of Anolis cristatellus in Dominica.

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Swimming Across the Ocean: Sperm Morphology Differs between Native and Introduced Anoles

Sperm of Anolis sagrei. Picture by Ariel Kahrl.

Caribbean anoles are making their way to Florida in all sorts of ways. Swimming across the sea is not one of them; however, once they arrive, some consistent and interesting patterns begin to emerge for something that swims inside them.

Sperm morphology can vary widely among individuals and between species, and this variation can be due to both intrinsic (genetic) and environmental factors. Large genetic variation in a trait means that the raw materials for evolution are abundant, and populations can diverge over space and time in relatively few generations. Much of this variation, however, could also be the result phenotypic plasticity since the environment that males experience during their lifetime can impact the shape and size of their sperm. Although previous studies have documented how sperm morphology can differ among populations, no studies have determined how introduction into novel habitats might influence this morphology.

Novel environments can influence traits through adaptive evolution, plastic responses to new conditions, or through random changes in gene frequencies (genetic drift and/or founder effects). Random changes in gene frequencies are likely to occur when populations expand into a new range because the founding population tends to be small and thus the gene pool is limited. By studying independent evolutionary trajectories (e.g. multiple species, or independent populations of the same species), we can rule out random changes in gene frequencies if the patterns we find are consistent among groups. As usual, anoles make excellent models for this work.

Ariel Kahrl and Bob Cox examined testis size and sperm morphology (head length, midpiece length, and tail length) for three species of Caribbean anoles (A. cristatellus, A. distichus, and A. sagrei) in their native ranges (Puerto Rico, Dominican Republic, Bahamas, respectively) as well as in Florida where each species is naturalized.

Although the results differed among species for some measures of sperm morphology, they found a few consistent patterns: sperm from introduced anoles had shorter tails and longer midpieces than those collected from native congeners (Figure 1). Furthermore, introduced populations had smaller testes than those from the native range.

Anolis spermatozoa (A). Population means 6 SE calculated from individual mean values (across 15 cells per male) for length of the sperm head, midpiece, and tail in native (black symbols) and introduced (white symbols) populations of three species of Anolis lizards. Significant differences between populations (P < 0.05) were determined using Tukey’s HSD test and are noted with an asterisk.

Figure 1. Anolis spermatozoa (A). Population means +/- SE calculated from individual mean values (across 15 cells per male) for length of the sperm head, midpiece, and tail in native (black symbols) and introduced (white symbols) populations of three species of Anolis lizards. Significant differences between populations (P < 0.05) were determined using Tukey’s HSD test and are noted with an asterisk.

There are two main reasons that differences in sperm morphology between native and introduced populations are probably not the result of random genetic shifts. First, the size of the midpiece and tail correlate with swimming speed in sperm. The midpiece of the sperm is the housing unit for the mitochondria which powers the cell as it moves, and the length of the tail can directly influence the speed at which the sperm swims (longer tail = greater speed). Because the observed changes in morphology likely impact function, adaptive evolution may be the source of these population differences. Second, the observed differences between the native and introduced populations are fairly consistent among species. Were these changes due to genetic drift or founder effects, it is unlikely that all three species would demonstrate similar changes in morphology. This pattern is more indicative of convergent evolution or phenotypic  plasticity because the south Florida environment may generate similar plastic responses in all three species.

What is left to be determined are the proximate causes of these changes in sperm morphology. The observed changes could be due to the process of introduction per se, or they could be caused by unique features of the south Florida environment. Conveniently, many anole species have been introduced to new areas on multiple, independent occasions.  Adding more species from other introductions (e.g. green anoles in Hawaii; brown anoles in California or Taiwan) would provide further insight.

Kahrl, A.F. and Cox, R.M., 2017. Consistent Differences in Sperm Morphology and Testis Size between Native and Introduced Populations of Three Anolis Lizard Species. Journal of Herpetology51(4), pp.532-537. http://www.bioone.org/doi/abs/10.1670/16-184

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