All posts by Ivan Prates

About Ivan Prates

My PhD research focuses on South American anoles to help uncover how changes in climate and landscape over time (thousands or millions of years) and space (across regions) have contributed to the geographic distribution of evolutionary lineages, alleles, and traits. I also use genetic and phenotypic data to assess the geographic distribution, phylogenetic relationships, and taxonomic status of poorly-known mainland anoles.

Legendary Brazilian Anoles Rediscovered

Several anole species are known from a single remote locality or only a few individuals, sometimes collected long ago. Because sampling these species is hard, we have a limited understanding about their biology and evolution. In a recent paper, we report on the rediscovery of Anolis nasofrontalis and Anolis pseudotigrinus, two mainland species from the Brazilian Atlantic Forest that were not reported for more than 40 years. Based on DNA sequence data, we examine their placement in the Anolis tree of life and estimate divergence times from their closest relatives. Moreover, based on the morphological attributes of newly and previously collected specimens (some of which were overlooked due to misidentification), we provide much needed taxonomic re-descriptions.

Fig. 1. Coloration in life of Anolis nasofrontalis (A, B) and A. pseudotigrinus (C, D). In A, inset shows the black throat lining of A. nasofrontalis, an uncommon trait that may be indicative of close relationships with Andean anoles (such as A. williamsmittermeierorum). Photographed specimens are females.

Coloration in life of Anolis nasofrontalis (A, B) and A. pseudotigrinus (C, D). In A, inset shows the black throat lining of A. nasofrontalis. Photographed specimens are females.

This study starts with efforts by collaborator Dr. Miguel T. Rodrigues (Universidade de São Paulo) to investigate reptiles and amphibians that have been undetected for years – a gap that could indicate human-driven extinctions. On late 2014, Dr. Rodrigues and his students (including co-author Mauro Teixeira Jr.) launched an expedition to the mountains of Santa Teresa (state of Espírito Santo, Brazil), the type locality of both A. nasofrontalis and A. pseudotigrinus. After a few days (and nights) of search, the team spotted the first A. pseudotigrinus in decades. The adult female was found sleeping on a narrow branch, (probably) unaware of its significance for South American biogeography (so were we). No signs, however, of A. nasofrontalis.

Shortly after, PhD students Paulo R. Melo-Sampaio (Museu Nacional) and Leandro O. Drummond (Universidade Federal do Rio de Janeiro) decided to visit Santa Teresa, inspired by conversations with Dr. Rodrigues. At this point, Dr. Rodrigues, my supervisor Dr. Ana C. Carnaval (City University of New York), and I had agreed that a phylogenetic study of A. pseudotigrinus would fit my PhD research well. Then, on early 2016, we got an unexpected email from Paulo and Leandro, with the first picture ever taken of an A. nasofrontalis in life. Both legendary anoles were real!

Back to the lab, we generated DNA sequence data and performed phylogenetic analyses, with completely unexpected results. First, A. nasofrontalis and A. pseudotigrinus are not closely related to the other (confirmed) Atlantic Forest species (A. fuscoauratus, A. ortonii, and A. punctatus); instead, they are close relatives of a species from western Amazonia, the “odd anole” Anolis dissimilis. These three species were found to compose a clade with A. calimae from the western cordillera of the Colombian Andes, A. neblininus from a Guiana Shield tepui on the Brazil-Venezuela border, and two undescribed Andean species (Anolis sp. R and Anolis sp. W from Poe et al. 2015 Copeia). This clade falls outside of the five major clades previously recovered within the Dactyloa radiation of Anolis, which have been referred to as species series (aequatorialis, heterodermus, latifrons, punctatus, roquet). Based on these results, we define the neblininus species series of Anolis.

Fig. 2. Phylogenetic relationships and divergence times between species in the Dactyloa clade of Anolis inferred using BEAST. Asterisks denote posterior probabilities > 0.95.

Phylogenetic relationships and divergence times between species in the Dactyloa clade of Anolis inferred using BEAST. Asterisks denote posterior probabilities > 0.95.

The neblininus series is composed of narrowly-distributed species that occur in mid-elevation sites (or adjacent habitats in the case of A. dissimilis) separated by large geographic distances. This pattern suggests a complex biogeographic history involving former patches of suitable habitat between regions, followed by habitat retraction and extinction in the intervening areas. In the case of A. nasofrontalis and A. pseudotigrinus, for instance, past forest corridors may explain a close relationship with the western Amazonian A. dissimilis. Atlantic and Amazonian rainforests are presently separated by open savannas and shrublands, yet geochemical records suggest that former pulses of increased precipitation and wet forest expansion have favored intermittent connections between them. These connections may have also been favored by major landscape shifts as a result of Andean orogeny, such as the establishment of the Chapare buttress, a land bridge that connected the central Andes to the western edge of the Brazilian Shield during the Miocene.

Fig. 3. Geographic distribution of confirmed and purported members of the neblininus species series. The inset presents a schematic map of South America around 10-12 mya, when the ancestor of A. nasofrontalis and A. pseudotigrinus diverged from its sister, the western Amazonian A. dissimilis. The approximate locality of the Chapare buttress, a land bridge that connected the central Andes to the western edge of the Brazilian Shield, is indicated.

Geographic distribution of confirmed and purported members of the neblininus species series. The inset presents a schematic map of South America around 10-12 mya, when the ancestor of A. nasofrontalis and A. pseudotigrinus diverged from its sister, the western Amazonian A. dissimilis. The approximate locality of the Chapare buttress, a land bridge that connected the central Andes to the western edge of the Brazilian Shield, is indicated.

During our morphological examinations of A. nasofrontalis and A. pseudotigrinus, it became apparent that these two species are not very different from Caribbean twig anoles, with whom they share short limbs and cryptic coloration. We learned that these features are also present in other, distantly-related mainland anoles, such as A. euskalerriari, A. orcesi, A. proboscis, and A. tigrinus. Phylogenetic relationships support that a twig anole-like phenotype was acquired (or lost) independently within Dactyloa, perhaps as a result of adaptive convergence. Alternatively, this pattern may reflect the conservation of an ancestral phenotype. In the former case, an apparent association with South American mountains is intriguing.

Unfortunately, natural history data from A. nasofrontalis and A. pseudotigrinus are lacking. It is currently unclear whether they  exhibit the typical ecological and behavioral traits that characterize the Caribbean twig anole ecomorph, such as active foraging, slow movements, infrequent running or jumping, and preference for narrow perching surfaces.

Fig. 4. Anolis dissimilis, the 'odd anole'.

Anolis dissimilis, the ‘odd anole’.

It has become increasingly clear that broader sampling of genetic variation is key to advance studies of mainland anole taxonomy and evolution. This significant challenge also provides exciting opportunities for complementary sampling efforts, exchange of information, and new collaborations between research groups working in different South American countries.

To learn more:

Prates I, Melo-Sampaio PR, Drummond LO, Teixeira Jr M, Rodrigues MT, Carnaval AC. 2017. Biogeographic links between southern Atlantic Forest and western South America: rediscovery, re-description, and phylogenetic relationships of two rare montane anole lizards from Brazil. Molecular Phylogenetics and Evolution, available online 11 May 2017.

Cuban Anolis porcatus introduced to Brazil (perhaps through Florida?)

Several anole species have become established outside of their native ranges as a result of human-mediated transportation, being introduced to Japan, Singapore, Taiwan, Hawaii, the continental U.S., and beyond. Alien anoles can have major impacts on the ecological communities that they invade, for instance leading to local extinction of arthropod taxa and displacing native anole species. It is therefore key to detect and report instances of introduction by these potentially aggressive invaders, as well as to document their geographic spread in colonized regions. In a recent paper, we report on the presence of Anolis porcatus, a species native from Cuba, in coastal southeastern Brazil, using DNA sequence data to support species identification and examine the geographic source of introduction.

Anolis porcatus collected in Brazil, and comparison with the native anole A. punctatus. A, male A. porcatus showing green coloration. B, male A. porcatus showing brown coloration. C, the pink dewlap of male A. porcatus. D, female A. porcatus. E, male A. punctatus, a native anole species. F, the yellow dewlap of male A. punctatus. Picture credits: A–D, Mauro Teixeira Jr.; E, Renato Recoder.

Anolis porcatus collected in Brazil, and comparison with the native anole A. punctatus. A, male A. porcatus showing green coloration. B, male A. porcatus showing brown coloration. C, the pink dewlap of male A. porcatus. D, female A. porcatus. E, male A. punctatus, a native anole species. F, the yellow dewlap of male A. punctatus. Picture credits: A–D, Mauro Teixeira Jr.; E, Renato Recoder.

Perhaps embarrassingly, this study started with Facebook. On August 2015, Ricardo Samelo, an undergraduate Biology student at the Universidade Paulista in Santos, posted a few pictures of an unknown green lizard in the group ‘Herpetologia Brasileira.’ A heated debate about the animal’s identity took place, with people eventually agreeing on Anolis carolinensis. On my way to Brazil to join the Brazilian Congress of Herpetology, I contacted Ricardo (but only after properly hitting the ‘like’ button) and proposed to examine whether the exotic anole was established more broadly in the Baixada Santista region.

To our surprise, local residents knew the lizards well, with some people quite fond of the ‘lagartixas’ due to their pink dewlap displays. People could often tell when the anoles were first noticed in the vicinities – ‘six months’, ‘nine months’, ‘one year ago’ –, suggesting a rather recent presence. Guided by these informal reports, we sampled sites in the municipalities of Santos, São Vicente and Guarujá, where we found dozens of lizards occupying building walls, light posts, fences, debris, trees, shrubs, and lawn in residential yards, abandoned lots, and alongside streets and sewage canals. It was clear that the alien anoles are doing great in human-modified areas; the high density of individuals across multiple sites, as well as the presence of juveniles with various body sizes, seem to suggest a well-established reproductive population.

Sites in the Baixada Santista in southeastern coastal Brazil where introduced A. porcatus were detected. 1, Guarujá. 2, Santos. 3, São Vicente. Green indicates Atlantic Forest cover; gray indicates urban areas; black indicates water bodies.

Sites in the Baixada Santista in southeastern coastal Brazil where introduced A. porcatus were detected. 1, Guarujá. 2, Santos. 3, São Vicente. Green indicates Atlantic Forest cover; gray indicates urban areas; black indicates water bodies.

By reading and bugging experienced anole researchers about the Anolis carolinensis species group, I learned about paraphyly among species, hybridization, and unclear species diagnosis based on external morphology. As a result, my PhD supervisor, Dr. Ana Carnaval, and I decided to recruit Leyla Hernandez, by the time an undergraduate student in the Carnaval Lab at the City University of New York, to help generate DNA sequences to clarify the species identity, and perhaps track the geographic source of introduction in Brazil. To our surprise, a phylogenetic analysis found Brazilian samples to nest within Anolis porcatus, a Cuban species that has also been introduced to Florida and the Dominican Republic. Brazilian A. porcatus clustered with samples from La Habana, Matanzas, and Pinar del Río, which may suggest a western Cuban source of colonization. Nevertheless, Brazilian specimens are also closely related to a sample from Coral Gables in Florida, which may suggest that the Brazilian population originated from lizards that are exotic elsewhere.

Phylogenetic relationships of A. porcatus introduced into Brazil (indicated in red), inferred using MrBayes based on a mitochondrial DNA locus. Purple indicates samples of A. porcatus invasive elsewhere (Florida and the Dominican Republic). Blue indicates native Atlantic Forest anole species. Asterisks indicate posterior probability >0.95. Picture depicts a male A. porcatus collected in São Vicente, Brazil.

Phylogenetic relationships of A. porcatus introduced into Brazil (indicated in red), inferred using MrBayes based on a mitochondrial DNA locus. Purple indicates samples of A. porcatus invasive elsewhere (Florida and the Dominican Republic). Blue indicates native Atlantic Forest anole species. Asterisks indicate posterior probability >0.95. Picture depicts a male A. porcatus collected in São Vicente, Brazil.

The presence of A. porcatus in the Baixada Santista may be related to the country’s largest seaport complex, the Porto de Santos, in this region. Numerous storage lots for intermodal shipping containers were situated near sites where the lizards were detected, and in one instance we found the animals sheltered inside an open container. An exotic green anole (identified as A. carolinensis) was previously found in Salvador in Brazil’s northeast; like Santos, Salvador hosts a major seaport complex, which may indicate that the exotic anoles reached Brazil after being unintentionally transported by ships bringing goods from overseas perhaps twice independently.

It is currently unclear whether A. porcatus will be able to expand into the surrounding coastal Atlantic Rainforest, or into more open natural settings such as shrublands in the Cerrado domain. It is also unknown whether this species will have negative impacts on the local ecological communities. In Brazil, introduced A. porcatus may potentially compete with other diurnal arboreal lizards, such as Enyalius, Polychrus, Urostrophus, and the native Anolis. Five native anoles inhabit the Atlantic Forest (for sure): A. fuscoauratus, A. nasofrontalis, A. ortonii, A. pseudotigrinus, and A. punctatus. While none of them is currently known to occur in sympatry with A. porcatus, the worryingly similar A. punctatus has been reported for a site in Bertioga located only 50 kilometers from the site in Guarujá where we found the exotic anoles.

To properly evaluate the potentially invasive status of A. porcatus in Brazil, we hope to continue assessing the extent of its distribution and potential for future spread, as well as to gather data about whether and how A. porcatus will interact with the local species – especially native Brazilian anoles. This seemingly recent, currently expanding colonization also represents an exciting opportunity for comparisons with other instances of introduction of A. porcatus, as well as the closely-related A. carolinensis, based on ecological and phenotypic data.

Studying such mysterious alien anoles in Brazil was made much more tractable through advice from Jonathan Losos and Richard Glor. Thank you!

To learn more: Prates I., Hernandez L., Samelo R.R., Carnaval, A.C. (2016). Molecular identification and geographic origin of an exotic anole lizard introduced to Brazil, with remarks on its natural history. South American Journal of Herpetology, 11(3): 220-227.