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

New Research on How Lizards Regrow Their Tails

A press release from Arizona State University:

A tale of two studies: ASU researchers uncover mechanisms of lizard tail regeneration

Findings on stem cells, nerve regrowth offer intriguing clues that may one day translate to human therapy


January 30, 2018With the hope that someday scientists will advance regenerative therapy in humans, an interdisciplinary team of researchers from Arizona State University and two other institutions has discovered important new clues in exactly how lizards regenerate their tails.

The findings appear in a pair of studies published in a Jan. 15 special issue of the journal Developmental Biology that focused on regeneration. The University of Arizona College of Medicine-Phoenix and Victor Chang Cardiac Research Institute also participated in the studies.

A green anole lizard (Anolis carolinensis). Photo: Kenro Kusumi.

In one paper, scientists from ASU investigated the role of a muscle stem cell population called “satellite” cells. Regeneration involves making new muscle, cartilage and tendons and requires cells that will become these tissues in a regrown tail.

The researchers found that the muscle satellite cells in green anole lizards (Anolis carolinensis) do double duty and can become cartilage as well. This study provides the first functional description of this stem cell population in lizards.

“Satellite cells are a unique stem cell population that allows humans to grow and repair muscle tissue,” said senior author Jeanne Wilson-Rawls, associate professor with ASU School of Life Sciences. “Mammals, including mice and humans, have muscles that contain these cells. After an injury, these satellite cells can repair the remaining muscle, but they cannot replace lost muscle in humans, unlike in lizards.”

“Using cell culture techniques, we found that lizard satellite cells behave the same as mouse satellite cells,” said Joanna Palade, lead author of the first paper and graduate student in the ASU molecular and cellular biology graduate program. “However, while both cell types can differentiate into muscle, only lizard satellite cells can turn on the genes and proteins required to make cartilage.”

By studying the genetic programming in mice and lizards, the researchers hope to find the differences between them that make the lizard more capable of regeneration.

“Lizards and humans have most of the same genes,” said Kenro Kusumi, co-author of the study and professor with the school. “Working with expert computer scientists, we found the genes that control cartilage formation were turned on in lizard but not mouse satellite cells, pointing to the existence of a possible switch that must be activated for regenerative therapies.”

A green anole lizard (Anolis carolinensis) with a regenerated tail. Photo: Joel Robertson

In a second study, the scientists found that nerve regeneration in particular, is a critical part of the tail regeneration process.

“Nerve regrowth is immediate in the regenerated lizard tail,” said Cindy Xu, co-author of the paper and also a graduate student in the program. “Regenerating nerves quickly repopulate the tail as muscle begins to form. As the neuromuscular junction matures, the nerves are pruned back but remain more numerous when compared to the original tail.”

In this study, the researchers allowed lizards to regenerate their tails up to 250 days and then studied the neuromuscular junctions — the connections between nerve and muscle — at different stages. Coordinated tail movements require effective communication between neurons and tail muscles through these neuromuscular junctions resulting in muscle contraction.

“Overall, we found that the regeneration of neuromuscular junctions in the lizard followed a pattern similar to development in mice and humans,” said Minami Tokuyama, co-author of the paper and former research technician in Kusumi’s lab. “However, the regenerated muscle ends up with a greater density of neuromuscular junctions, and studying these differences may be important in developing future therapies for humans.”

Together, these findings may bring researchers closer to solving the challenge of creating the capability for limb or organ regeneration in humans.

The research team included Kusumi, Palade, Tokuyama, Wilson-Rawls and Xu, as well as Jason Newbern and Alan Rawls, who are faculty with ASU’s School of Life Sciences; Rebecca Fisher with ASU School of Life Sciences and the University of Arizona College of Medicine-Phoenix; and Joshua Ho and Djordje Djordjevic from Victor Chang Cardiac Research Institute. The National Institutes of Health funded this research through grants.

Fabric Poster!

poster

For those who travel with posters to conferences, here is a neat idea… have your poster printed on fabric. This one turned out really nice! Was done using Spoonflower in North Carolina (www.spoonflower.com). The cost is around $22.00 + shipping, but not having to travel with a poster tube is pretty enticing. I have no affiliation with company, just wanted to share. 

Colonization and Adaptation of Japanese Island Green Anoles

A female green anole from Hahajima in the Osagawara Islands.

We’ve had a series of posts about the anoles of the Osagawara Islands, of Japan, the “Galápagos of the Orient” [1, 2]. Now a new paper (pdf here) from Masakado Kawata’s lab has resequenced genomes of multiple individuals and measured morphology to assess how large the founding population was and what sorts of morphological changes have occurred since colonization, as well as identifying some genes potentially under selection.

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Here’s the abstract:

Invaded species often can rapidly expand and establish in novel environments through adaptive evolution, resulting in devastating effects on native communities. However, it is unclear if genetic variation at whole-genomic levels is actually reduced in the introduced populations and which genetic changes have occurred responding to adaptation to new environments. In the 1960s, Anolis carolinensis was introduced onto one of the Ogasawara Islands, Japan, and subsequently expanded its range rapidly throughout two of the islands. Morphological comparison showed that lower hindlimb length in the introduced populations tended to be longer than those in its native Florida populations. Using re-sequenced whole genomic data, we estimated that the effective population size at the time of introduction was actually small (less than 50). We also inferred putative genomic regions subject to natural selection after this introduction event using SweeD and a method based on Tajima’s D, π and FST. Five candidate genes that were potentially subject to selection were estimated by both methods.The results suggest that there were standing variations that could potentially contribute to adaptation to nonnative environments despite the founder population being small.

Last Call for Anole Symposium Registration

The Seventh Anole Symposium is now only two months away (17-18th March 2018), so we are making a last call for registration for the meeting. If you want to attend please follow the link below to submit your registration by 11:59 EST January 31st to secure your spot. We will send out a payment link to registrants the following week.

Winning Symposium t-shirt design by Eric-Alain ParkerWinning Symposium t-shirt design by Eric-Alain Parker

Click HERE to register

Another Great Anole Journal Cover

mesoamerican herpetology cover photo copy

Looks like it’s time for an updated compilation of anole covers! This one’s from the December 2017 issue of Mesoamerican Herpetology. Here’s what they have to say:

Javier Sunyer is a Spanish herpetologist who has lived in the Neotropics for the last 20 years. His work includes over 80 scientific papers and notes, dealing mostly with the distribution, natural history, and conservation of the Nicaraguan herpetofauna. Currently, he is a Research Associate at the Universidad Nacional Autónoma de Nicaragua-León (UNAN-León) and an Associate Editor/Section Editor for Mesoamerican Herpetology. Pictured on our cover is an image of Kempton’s Anole (Norops kemptoni), photographed in January 2006 at Alto Chiquero, Parque Nacional Volcán Barú, Provincia de Chiriquí, Panama. Adult males are territorial, and often display their colorful dewlap to intruders.

Green Anoles in Pennsylvania?!

A few days ago, I received an intriguing comment on my lizardsandfriends.org blog:

Hello Michele;

My name is Steve and I found a family of Green Anoles living in my shed this past summer.  The interesting thing about this is that I live in Pennsylvania.  As far as I understand, they should not be this far north.

At first I only saw the one and would see him every now and again on hot days.  Then I saw two at once and then later I saw three at once.  So I assume I have a family taking shelter in my shed.

My daughter had a couple of anoles as pets back in 2002.  One escaped and the other eventually died.  I can’t help but wonder if the one that escaped was pregnant and happened to find my shed and the smorgasbord of insects that also take up residence there and started a family.

Thing is that there have been many winters between then and now and it is often in the single digits here during the winter.  We just went through over a week where the temps didn’t get out of the single digits much.  Do you think these little guys will be OK?  I mean I assume they have been dealing with these conditions for many years but I don’t really know.  The three I saw together were of different sizes which makes me think they’ve been there long enough to raise a family.

I am reluctant to change anything regarding how I keep the shed as I assume it has been agreeable enough in previous winters but can’t help wondering how they are doing…

I was, of course, skeptical that there could really be green anoles living outdoors in Pennsylvania – it’s just too cold in the winter.  I wrote back:

Hi Steve,

This is indeed unexpected! I assume you know exactly what green anoles look like, having had them as pets. The scenario you suggest is possible, that the escaped lizard was gravid and managed to reproduce and they survived, but is not “supposed” to happen with the kind of weather you experience in PA. Also, anoles don’t usually hang out together, as they defend territories from one another (and have no parental care), so it’s also a little curious that you saw them in a group. In any case, I wouldn’t suggest changing anything about the shed, but I agree it seems unlikely that these guys (if they are anoles) would make it through the winter. Feel free to send me a photo to confirm what they are, if you’d like.

And Steve replied, with photos that make it clear that yes, there are indeed green anoles living in his shed!

I am pretty sure these are green anoles.  They at least look exactly like the ones my daughter kept.  Also when I saw the first one, he was initially green and then turned brown as I moved closer to check him out.  Below is an image of that guy when I first saw him.

 anole

I never saw the anoles hanging out together in a group.  They were just out in the shed at the same time.  They do all seem to have their favorite areas.  One hung out above a window with a southern exposure where there was a large spider in a web below (the spider and the web eventually disappeared).  I would often see this one basking in that window.  The smaller one hung out around the side door of the shed and would often be poking out from around the side door jam.  The third one I saw on the chicken wire.  I did see one on the vent screen once but I’m not sure which one that was.  They all seemed to like the chicken wire though.  I also grow Mission Figs here and I use the chicken wire and plastic sheeting, tar paper and burlap to wrap the figs for winter.  All this stuff is piled up on the side of the shed where I always saw the anoles.

 I have been affectionately calling them Shed Lizards since they can’t be your standard variety anole this far north and I have never seen them outside the shed …

One at the roof vent:

A Clouded Anole Male during a nocturnal walk through the jungle

The Lonely Clouded Anole on a Pacific Island

Anolis nebulosus

Anolis nebulosus. Photo by Hugo Siliceo-Cantero.

By H. Hugo Siliceo-Cantero and A. Garcia

In the late 1980´s, the scientists Bradford C. Lister and Andrés García discovered an interesting population of clouded anoles inhabiting the small 3.3 ha island of San Agustin located just off the Pacific coast of Jalisco, Mexico. This island was also close to the actual protected area of tropical dry forest on the mainland in the Chamela-Cuixmala Biosphere Reserve. Lister and García reported that the abundant anole population on San Agustin was maintained a decade later at much higher densities than the mainland population. We began to study this population in 2007 as a graduate student. Since then, we have studied several aspects of the ecology of this island population comparing this with the ecology of anoles on the mainland.

The existence of such island populations enables scientists to carry out natural experiments that provide invaluable information helping us to understand ecological and evolutionary processes.

This Clouded Anole (Anolis nebulosus) species that is on San Agustin Island is endemic to Mexico, and is of particular interest as this population has evolved in the absence of similar species of the same genus, or congeners. The species on the island also occupies a broad niche of perch height and a low number of lamellae, and is one of the most sedentary anoles known. Our work demonstrated that San Agustin population of the Clouded Anole has distinct morphological and genetic traits compared to conspecifics on the mainland.

Recently, we found that the insular population also presents distinct ecologic traits compared to those of the mainland population. In our manuscript “Assessing the relative importance of intra- and interspecific interactions on the ecology of Anolis nebulosus lizards from an island vs. a mainland population”, we suggest that the processes that drives the ecology and evolution of this insular population (intraspecific competition) differs from those that are important in the mainland (interspecific competition).

We believe that the results of our research on the insular population of anoles on San Agustin Island complement the scenario of Caribbean anoles, where congeneric competition is the key evolutionary driver. Furthermore, in our study, we used video cameras to provide direct evidence of predation, interspecific and intraspecific encounters and aggression, which was possible because the Clouded Anole is a sedentary lizard.

It has been a pleasant and rewarding experience for me to study the Clouded Anole. Although spending hours in the field observing a largely sedentary lizard may seem a little boring and tedious, the data from our studies have revealed a fascinating adaptation to the natural and social environment with unique physical, genetic, and ecological characteristics.

Currently, the population of Clouded Anoles on San Agustin has been dramatically reduced, almost to the point of extirpation. We think that two natural events, the hurricanes Jova in 2011 and Patricia in 2015, as well as invasive studies such as Hernández-Salinas et al. (2016) where they extracted 77 anoles from this small island, are the cause of the dramatic reduction in the Clouded Anole of San Agustin Island. As ecologists, we believe that research should not be done at the expense of the species or population under study, but should ensure that the population remains intact to continue along its evolutionary path, and further elucidate our understanding of the natural world around us.

We are currently monitoring both insular and mainland populations in order to understand and evidence the ecological implications of such natural and anthropogenic reduction on anole populations.

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