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.

SICB 2018: Heat Stress and Deformed Faces

EmbryosIncubation temperature is an important factor in development for anoles (and other ectotherms). Thom Sanger, a professor at Loyola University in Chicago, IL, presented his research on how high temperatures affect brain formation in developing anole embyros. With the help of undergraduates and a high school summer intern, Dr. Sanger found that when developing eggs were heat-shocked, many embryos were lost (75%), but for those that survived, forebrains became smaller (In the figure, A is normal and B is deformed). Interestingly, malformation of the forebrain affects the size and shape of the face, and so surviving heat-shocked embryos exhibit cranial malformations. As Sanger continues his research, he will follow a neural degeneration hypothesis, which boils down to (no pun intended) the idea that thermal stress increases the rate of cell death, and the amount of cell death affects facial shape. While the effects of high temperature may seem alarming, Sanger notes that this does not happen very often in nature; females are generally pretty good at selecting suitable nest sites. But, because development is similar across reptile taxa, anoles can be an excellent model system to inform predictions about what may happen to species that are in danger.

Origins and Biogeography of the Anolis crassulus Subgroup

Anolis morazani. Photo by Josiah Townsend from iNaturalist.

The Anolis crassulus subgroup contains ten morphologically-conserved highland anole species found throughout Nuclear Central America. Its members have long been a source of headache for region’s systematists. To quote Meyer & Wilson (1971): “…specimens of the crassulus group from Guatemala and Mexico have a bewildering array of admixtures of the distinctive characters observed in Honduras… The inter-relationships of the populations… [of the crassulus group] are exceedingly complex, and… we are unable to suggest a satisfactory arrangement.” This was followed up 21 years later by McCranie, Wilson, & Williams (1992): “Clearly, a thorough analysis of crassulus-like specimens from throughout their range… is sorely needed”, and repeated by McCranie & Köhler (2015) 13 years after that.

Despite the need for a thorough investigation into this group, our understanding of the relationships and validity of these taxa has not improved much. This is partly because this subgroup has been poorly represented without broad sampling in larger-scale molecular phylogenies. Two samples in particular, an A. crassulus (from Chiapas, Mexico) and an A. sminthus (from Olancho, Honduras), have been continuously utilized, without additional samples from these species. Most recently, Nicholson et al. (2017; six species) and Poe et al. (2017; three) expanded the molecular sampling for this group, using single exemplars as part of broader analyses.

In a study published last month in BMC Evolutionary Biology, Josiah Townsend and I examined the evolutionary relationships of the majority of this subgroup, in order to provide a starting point for resolving some of the confusion surrounding these taxa.

Figure 4 from Hofmann & Townsend, 2017. Species tree of the Anolis crassulus subgroup. Inset photo: Anolis heteropholidotus (2) by JHT.

Fig. 4 from Hofmann & Townsend, 2017: Species tree of the Anolis crassulus subgroup. Black nodes indicate PP > 0.95; PP < 50 not shown. Inset photo: Anolis heteropholidotus (2) by JHT.

The results of our multilocus phylogenetic investigation gave us some interesting new insights into the subgroup. We found support for the monophyly of the A. crassulus subgroup relative to other Anolis (as opposed to its paraphyly, as recovered in Poe et al. 2017), and the validity of all of its species (excepting the two we could not sample). Additionally, we recovered considerable overlooked diversity within this subgroup. Anolis crassulus itself represents at least four lineages corresponding to distribution: the Chortis Highlands of Honduras, the Salvadoran Cordillera, Guatemala, and Chiapas, Mexico. Surprisingly, the sample from Chiapas previously used in many phylogenies was recovered as an undescribed lineage sister to A. anisolepis, not conspecific with any of the four A. crassulus lineages, including another Chiapan lineage. We also recovered the widely-used “A. sminthus” sample (which was previously hypothesized by McCranie and Kohler (2015) as representing an undescribed lineage more closely related to A. crassulus) as an undescribed lineage sister to A. morazani, and found additional mitochondrial lineages within A. heteropholidotus and A. rubribarbaris. Diversification within the group was estimated to have started in the early Miocene in the Chortis Highlands (supporting the results of Nicholson et al. 2017), with the Honduran population of A. crassulus diverging from the other three lineages approximately 13 MYA.

Figure 5 from Hofmann & Townsend, 2017. Chronogram showing results from divergence dating and ancestral area reconstruction analyses. PP shown when < 1.

Fig. 5 from Hofmann & Townsend, 2017: Chronogram showing results from divergence dating and ancestral area reconstruction analyses. PP shown when < 1.

Given the relatively deep divergence times within this group when compared with the apparent lack ecological and morphological diversification, we hypothesized that this subgroup represents a non-adaptive radiation, though extensive study is necessary to determine if these traits are as conserved as they appear. A taxonomic revision of the Chortis Highland population of Anolis crassulus is being finalized, but a great deal of work remains in order to improve our understanding of these highland anoles.

SICB 2018: Evo-Devo of Anole Digits

Griffin

One more update from the SICB conference in San Francisco last week!

Across vertebrates, the ratio of lengths of the second and fourth digits of the hand are influenced by testosterone and estrogen. This could be of particular importance in species such as anoles, in which the fourth digits of the hindlimbs are extremely long and critically important in locomotion, but previous studies of the 2D:4D ratio in anoles have produced varying results. In the final poster session at SICB, undergraduate Griffin McNamara, working with Bonnie Kircher in Marty Cohn’s lab at the University of Florida, presented preliminary results from a study of cleared and stained brown anole (Anolis sagrei) hind feet. Griffin has big plans for continuing this work, so watch for future publications with these findings!

Anolis wattsi Expanding its Range in Trinidad

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A, wattsi is one of five introduced species on the islands. A new report in Living World: the Journal of the Trinidad and Tobago Field Naturalists’ Clubindicates that it’s on the move.

SICB2018: Density and Timing of Hatching Impact Survival and Growth in Anolis sagrei

Dan Warner (left) and Tim Mitchell (right) beside their poster on impacts of population density and time of hatching on survival and early life phenotypes of Anolis sagrei

Dan Warner (left) and Tim Mitchell (right) beside their poster on impacts of population density and time of hatching on survival and early life phenotypes of Anolis sagrei

Tim Mitchell a post-doctoral researcher at University of Minnesota with Emilie Snell-Rood presented his work from his prerious post doc in Dan Warner’s lab where he investigated the impacts of density and timing of hatching on the survival and growth of Anolis sagrei hatchings. Seeking to specifically address these questions:

How does investment in offspring size and number shift seasonally?

Does the timing of hatching influence survival or growth in the field?

And does adult density influence survival or growth of hatchlings in the field?

Adult anoles were brought into the lab on three different dates and breeding was split into three corresponding windows of time: Cohort 1 (February 23rd – April 27th), Cohort 2 (June 18th – July 30th), and Cohort 3 (September 5th – October 15th).  On experimental islands, adult densities were manipulated to create high and low lizard densities. Hatchlings from cohorts 1, 2, and 3 were released onto high and low adult density islands in June, August, and October, respectively, and researchers returned the following spring to recapture the marked lizards.

Breeding in the lab revealed a seasonal shift from producing more smaller offspring early to producing fewer larger offspring later in the season. Adult densities on the islands did not affect hatchling survival, but there was a substantial survival advantage to being an early-hatched lizard. Size and growth of hatchlings were influenced both by timing of hatching and the adult densities. So happy to catch up with my academic family and see the cool research they are doing!

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