Author: Masakado Kawata

Anolis allisoni. Photo by Masakado Kawata

Cuba is a fascinating country and the largest island in the Caribbean. Cuba has the highest diversity of Anolis lizards, including more than 60 species (see my Instagram page for photos of Cuban anoles and landscapes). Antonio Cádiz, Luis M. Díaz (National Museum of Natural History of Cuba) and a member of my lab published a paper comparing genetic divergence of Anolis species within Cuba (Cádiz et al. 2018, Zoological Letters, 4:21). The study was conducted when Tony was a PhD student at Tohoku University and lecturer at Havana University.

We constructed a phylogeny using nuclear and mitochondrial genes of 303 individuals from 33 Cuban Anolis species (Fig.2) . The phylogeny presented in this study follows the most comprehensive sampling of Cuban Anolis species to date. We added five species which had not been sequenced previously. We also estimated another phylogeny using mitochondrial genes of 51 Cuban and 47 non-Cuban Anolis species for estimated relative species ages (Fig.S3).

Map of Cuba showing our sampling locations.

Then, we tried to estimate factors affecting interspecific (or interclade) differences in genetic divergence among populations of Cuban Anolis species. We considered species age, environmental heterogeneity within species ranges, and ecomorph type as putative factors. For this purpose, we examined genetic divergence within species by using 177 populations of 26 species.The sampling locations of these species were selected for the best feasible coverage of known geographic ranges of each species. Phylogenetic Generalized Least Squares (PGLS) analyses showed that species age was positively correlated with species’ average genetic divergence among populations.

Previous studies have indicated deep interpopulation genetic divergence found in several Anolis species. Our results showed that relavie differences in genetic divergence was largely affected by species age and geographic distances within species (Fig. 3). This indicates that older species could have more divergent populations within species.

Phylogeny of Cuban anoles.

Cádiz, A., N. Nagata, L. Díaz, Y. Suzuki-Ohno, L.Echenique-Díaz, H. Akashi, T. Makino and M. Kawata. (2018) Factors affecting interspecific differences in genetic divergence among populations of Anolis lizards in Cuba. Zoological Letters 4:21 [Open Access] https://doi.org/10.1186/s40851-018-0107-x

Behavioral and TRPA1 Heat Sensitivities in Three Sympatric Cuban Anolis Lizards

By Masakado Kawata

On April 1, 2018

In New Research

I would like to introduce our recently published paper on Comparison of Behavioral and TRPA1 heat sensitivities in Cuban Anolis lizards. In Cuba, three sympatric species of Anolis lizards (Anolis allogus, A. homolechis, and A. sagrei) inhabit different thermal microhabitats (above). Different thermal habitats, that is shade, edges of forests and cleared forests, are occupied by A. allogus, A. homolechis and A. sagrei, respectively. Anolis allogus is non-heliothermic, while A. homolechis and A. sagrei are heliothermic species. Our previous study found that these species showed distinct gene expression patterns in response to temperature stimuli, suggesting the genetically distinct thermal physiology among species (Akashi et al. 2016. Mol.Ecol.).

For lizards, heat avoidance behavior is crucial for limiting their body temperatures within thermally safe margins. We predict that the temperature that elicits heat avoidance behavior would differ between these three Anolis species, and the differences might be related to different heat sensors among the species. Organisms perceive various temperatures via biological temperature sensors, such as thermosensitive transient receptor potential ion channels (thermo-TRPs). Among known thermo-TRPs, transient receptor potential ion channel ankyrin 1 (TRPA1) in non-mammalian species has been reportedly heat sensitive (Saito et al. 2012).

In our paper, we first conducted behavioral experiments to analyze the temperatures at which the three Anolis species escape from heat source (i.e., hotplate; Fig. 1) to examine whether the Anolis species inhabiting locally distinct thermal habitats diverge their thermal tolerances.

Then, for each of the three species, we isolated cDNA encoding of TRPA1, and performed electrophysiological analysis to quantify activation temperature of Anolis TRPA1. We found that temperatures triggering behavioral and TRPA1 responses were significantly lower for the shade-dwelling, non-heliothermic species (A. allogus) than for sun-dwelling heliothermic species (A. homolechis and A. sagrei).

The ambient temperature of shade habitats where A. allogus occurs stays relatively cool compared to that of open habitats where A. homolechis and A. sagrei occur and bask. The high temperature thresholds of A. homolechis and A. sagrei may reflect their heat tolerances that would benefit these species to inhabit the open habitats.

Akashi, H., S. Saito, A. Cádiz , T. Makino, M .Tominaga, M. Kawata. (2018) Comparisons of behavioral and TRPA1 heat sensitivities in three sympatric Cuban Anolis lizards. Molecular Ecology https://doi.org/10.1111/mec.14572

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

By Masakado Kawata

On May 19, 2017

In All Posts, Introduced Anoles

Photograph was taken in Hahashima, Ogasawara Islands, by Hideaki Mori.

We would like to introduce our recent paper on the invasive green anole (Suzuki-Ohno et al. 2017). In Japan, the green anole Anolis carolinensis invaded the Ogasawara Islands in 1960’s and Okinawa Island in 1980’s. In Ogasawara Islands, A. carolinensis expanded its range and had a significant negative impact on native species and the ecosystem. This becomes a big problem since Ogasawara Islands are designated as a natural heritage.

On Okinawa Island, A. carolinensis was first captured in 1989 and it did not expand its distribution until more than 25 years later, although its density is extremely high in the southern region. In the northern region of Okinawa Island, Yambaru area, native forests are preserved so that it is important to avoid the invasive effects of A. carolinensis. Thus, It is important to determine whether A. carolinensis has the potential to expand its distribution on Okinawa Island.

Phylogenetic analysis shows that the invader A. carolinensis originated in the western part of the Gulf Coast and inland areas of the United States. Interestingly, all of the invaded A. carolinensis in Ogasawara, Okinawa and Hawaii originated from the Gulf Coast and inland areas of the United States.

ND2 phylogeny using Okinawan, Ogasawaran, and Hawaiian populations in addition to haplotypes used by Campbell- Staton et al. (2012) and Hayashi et al. (2009).The major branches with high posterior probabilities of the Bayesian inference method (>0.99) are indicated in bold. The map was redrawn from Campbell-Staton et al. (2012). Cited from Suzuki-Ohno et al. (2017). Figure 2 of Suzuki-Ohno et al. (2017) lacks bold lines in error.

We used a species distribution model (MaxEnt) based on the distribution of native populations in North America to identify ecologically suitable areas on Okinawa Island. The MaxEnt predictions indicate that most areas in Okinawa Island are suitable for A. carolinensis. Therefore, A. carolinensis may have the potential to expand its distribution in Okinawa Island.

MaxEnt prediction of suitable areas for A. carolinensis in Okinawa Island according to the presence data for North America. Lighter and darker areas indicate high or low suitability, respectively. Points indicate the presence distribution of A. carolinensis. (a) prediction using all parameters, (b) prediction omitting mean diurnal range and precipitation of warmest quarter. Cited from Suzuki-Ohno et al. 2017.

The predictions indicate that habitat suitability is high in areas of high annual mean temperature and urbanized areas. The values of precipitation in summer in the northern region of Okinawa Island were higher compared with those of North America, which reduced the habitat suitability in Okinawa Island. Adaptation to low temperatures, an increase in the mean temperature through global warming, and an increase in open environments through land development will likely expand the distribution of A. carolinensis in Okinawa Island. We think that invasive anoles (A. calrolinensis and A. sageri) prefer open habitats.

Therefore, we suggest that A. carolinensis should be removed by using traps and/or chemicals. In addition, we must continue to be alert to the possibility that city planning that increases open environments may cause their range to expand.

These results were published as Suzuki-Ohno et al. (2017) Factors restricting the range expansion of the invasive green anole Anolis carolinensis on Okinawa Island, Japan. Ecology and Evolution

Research Projects Of Anolis lizards In Cuba

By Masakado Kawata

On May 2, 2013

In New Research

Anolis homolechis

From 2009, we have investigated the evolution and ecology of Anolis lizards in Cuba, collaborating with Habana University and The National Museum and Natural History of Cuba. Prof. Losos asked us to describe our research projects in Cuba for communication among anole biologists. Thus, we would like to inform our ongoing projects on Anolis lizards in Cuba, and we are very grateful if you have any suggestions and comments on our projects. Also, your suggestion of collaborating research projects will be welcome.

1. Searching for the genetic basis determining differences in hindlimb length between the trunk-ground anole A. sagrei and the twig anole A. angusticeps. Similar to Sanger et al. (2012), we have tried to determine the developmental timing for divergence of hindlimb length between twig and trunk-ground anoles. The manuscript on this subject was submitted and is now under review.

2. The effects of microhabitat use, range expansion and the number of speciation events on local species richness of trunk-ground Anolis lizards in Cuba. We examined the species richness and thermal microhabitat partitioning (considered to be a measure of ecological interaction) of 12 trunk-ground anole species in 11 local assemblages in Cuba, covering nearly the entire geographic range of all these species. Our results suggest that the species composition and richness in local assemblages could be explained by both evolutionary history (the number of speciation events and limits to range expansion) and ecological processes (habitat partitioning). This research is a part of Ph.D. thesis of Antonio Cadiz (Tohoku University and Havana University). The manuscript on this subject was accepted by Ecosphere and will be available soon.

3. We reconstructed a phylogeny using almost all Cuban Anolis lizards and also analyzed the genetic distances between populations within Cuban islands for these species. This project aims not only to construct the comprehensive phylogeny, but to understand ecomorph evolution within Cuban island.

4. Genetic basis for adaptation to different thermal environments. Multiple trunk-ground species can coexist since they inhabit different thermal environments. Anolis sagrei was found in open locations with high levels of light intensity and temperature. In contrast, A. allogus was found in shaded locations within forests with low levels of both light and temperature. Anolis homolechis was typically found at the edges of forests or in open locations in forests with intermediate environmental conditions. We try to examine genetic basis for these different thermal adaptation by using both a candidate gene approach and whole transcriptome analysis.

5. Other research projects will be started this year, although we do not specify the detailed plan.

In addition to Cuban Anoles, we are investigating the evolution of Anolis carolinensis introduced into the Bonin islands (Ogasawara islands) about 50 years ago (from either Guam, Hawaii or Florida).

Masakado Kawata, Graduate School of Life Sciences, Tohoku University, Sendai, Japan (kawata ‘at’ m.tohoku.ac.jp)