Category: New Research Page 16 of 66

Monkey lizards (Polychrus) are unique among Neotropical arboreal lizards in having strikingly long whip-like tails, as well as long limbs and digits. Interestingly, they resemble Old World chameleons in both morphology and behavior: slow-moving lizards with a laterally compressed body and cone-shaped eyes with partially fused eyelids. Although their phylogenetic position in the iguanid tree of life remains controversial, many authors argue that monkey lizards are the living sister taxon of anoles.

In a study published last week in PlosONE, we present a molecular phylogeny of all eight currently recognized species of Polychrus based on the largest geographic sampling to date. Our species tree places P. acutirostris as sister to all other species of Polychrus. While the phylogenetic position of P. gutturosus and P. peruvianus is poorly resolved, P. marmoratus and P. femoralis are strongly supported as sister to P. liogaster and P. jacquelinae, respectively. Moreover, recognition of the recently described P. auduboni and P. marmoratus sensu stricto as distinct species suggests that the populations of “P. marmoratus” from the Amazon and the Atlantic coast in Brazil represent separate species. Finally, species delimitation analyses suggest, among other things, that the populations of P. femoralis from the Tumbes region (southwestern Ecuador and northwestern Peru) might belong to a cryptic undescribed species.

Uracentron flaviceps (upper photo) and Microlophus thoracicus (lower photo), two tropidurine lizards adapted to rainforests and deserts, respectively.

I was lucky enough to spend some months working at the Museum of Comparative Zoology of Harvard as part of the Losos lab. There I learned a good deal about anoles and got to meet anole-loving people face to face. Even though this atmosphere tempted me to develop a project related to one of the greatest examples of adaptive radiation, I had other plans in mind involving some of their distant cousins: tropidurine lizards! The results of this study are already published (Toyama, 2017) and I will describe a bit of what I found.

Tropidurinae is a group of lizards whose representatives have diversified across South America. They come in different shapes, colors and sizes, as you would expect from any group of organisms spreading in a diverse territory in terms of habitats, climates and altitudes. Rainforests, deserts, mountains and dry forests are just some examples of the different ecosystems where you can find these lizards. Given this scenario, I wondered if the morphological diversity observed in this clade could be linked to the challenges imposed by the different habitats types found in the continent.

Inspired by similar studies that focused on other lizard radiations, I took measurements of functional morphological traits of several species of lizards coming from 10 out of the 12 genera comprising the Tropidurinae. These traits would allow me to look for a possible correspondence between morphology and habitat.

However, as I was not only interested in the link between morphology and habitat use, but also in the morphological diversity itself, I started looking at purely morphological information. The next figure shows the illustrative results of a Principal Component Analysis (PCA), which tries to separate the species as much as possible based on the morphological measurements. In the figure, we can observe how the dots of each color (representing species of the same genus) occupy a particular zone in the graph. This means that, in general, species of the same genus are, as expected, morphologically more similar between them than to species of other genera (exceptions aside, given the overlaps between some genera).

Scatter plot showing the morphological space defined by PC1 and PC2. Each dot represents the average values for a species, and species are grouped in genera (colors). Abbreviations are shown for some traits as HL (head length), HW (head width), HH (head height), BW (body width), BH (body height), Dist (distance between limbs), Htoe (longest toe of the hind limb), and Ftoe (longest toe of the forelimb).

Going a bit farther in respect to morphological diversity,

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Anolis oxylophus at La Selva Biological Station (left, photo by Christian Perez) and Anolis aquaticus at Las Cruces Biological Station (right, posed).

Among anoles, West Indian ecomorphs are the best known microhabitat specialists, but they are not the only ones. Semiaquatic anoles, of which there are 11 described species, live exclusively near streams and will sometimes enter water to feed or to escape a threat. The Central American species Anolis aquaticus appears to be specialized for climbing on rocks, particularly relative to other Central American semiaquatic anoles (Muñoz et al. 2015). Recent posts on A. aquaticus have addressed sleep site fidelity, dewlaps and trait scaling, and underwater foraging.

During a field ecology course with the Organization for Tropical Studies last winter, I compared patterns of substrate use between A. aquaticus and another Central American semiaquatic anole, Anolis oxylophus. Unlike A. aquaticus, A. oxylophus perches predominantly on woody and leafy substrates (Table 1). I wondered what was driving the differences in substrate use between these two species that appear broadly similar in morphology and lifestyle. Some Caribbean anoles alter their behavior to use only a narrow subset of available substrates in their habitat, whereas others have a greater breadth of substrate use that more closely reflects habitat-wide availability (Irschick and Losos, 1999; Mattingly and Jayne, 2004; Johnson et al., 2006). To evaluate whether substrate use differences between A. aquaticus and A. oxylophus are driven by substrate availability, species-specific selectivity, or both, I simultaneously quantified lizard substrate use and substrate availability within their streamside habitats.

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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.

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.

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.

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.

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.

The adult sex ratio is an important characteristic of a population, influencing the number of available mates in an area, the strength of sexual selection, and the evolution of mating systems. In our new paper in the Journal of Zoology, Michele Johnson and I use anoles to look at variation in sex ratios within and across species within a clade.

Photo by Michele A. Johnson

This paper had its roots when Jonathan Losos put me in touch with Michele in my first semester of grad school. Michele had compiled a massive database of detailed behavioral observations for Anolis populations and species across the Greater Antilles during her PhD on territoriality and habitat use (see Johnson et al. 2010 for more details!). While still trying to familiarize myself with the data set, I came across papers by Bob Trivers on sexual selection in anoles and his publication on the name-sake Trivers-Willard hypothesis; the combination of these topics made me curious about sex ratios and their role in sexual selection. I decided to quickly calculate the sex ratios of our localities, and given their distribution, realized that we should definitely look into this more.

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Sex ratios are generally very hard to measure in the field. You need to be certain that you haven’t had any biased sampling, or in other words, that you’ve made a fair attempt at censusing the population. This is quite difficult during short sampling periods! However, Michele conducted extended behavioral observations, and carefully tagged and monitored every individual in large habitat areas for ~3 weeks in each locality. This meant that we could be fairly confident that she had captured every individual in the population during her sampling periods, and her total counts of male and females in the population would be accurate. Even more, she had these adult sex ratios for 14 species, with some of those species being sampled at multiple localities. Given these data, we could actually both look at sex ratios across the Anolis clade, and within multiple anole species, for the first time.

We had two main questions: 1) were the sex ratios of these anole populations significantly skewed (i.e., were they very far off  from a 50:50 male-to-female ratio?) and 2) did the adult sex ratio of a population correlate with the strength of sexual selection in that population? For question 2, we used two measurements of sexual size dimorphism as a proxy for the strength of sexual selection. Sexual selection generally drives an increase in sexual size dimorphism (i.e., the difference between males and females in body size), but is also thought to be related to sex ratio skew (as the more skewed a population sex ratio, the more competition for mates or mating opportunities). We predicted that species with more skewed sex ratios would show an increase in sexual size dimorphism. Given that ecomorphs are an important component of evolution in anoles, and are commonly associated with varying levels of sexual size dimorphism, we also decided to test for a correlation between sex ratio skew and ecomorph type.

We found that sex ratios varied widely across and within anoles, ranging from a very female biased 0.32 in Anolis krugi to a male biased 0.61 in Anolis smaragdinus (sex ratios are expressed as the total number of adult males divided by the total number of both adult males and females in the population). Adult sex ratios also varied between different localities within a species (we had six species with multiple localities). We found two populations with significantly skewed sex ratios (Anolis krugi and Anolis valencienni) but based on Fisher’s test of combined probabilities, the sex ratios of anoles overall are not skewed away from 50:50.

I should note, however, that it is intrinsically extremely difficult to detect a skewed sex ratio in a natural population. We’re trying to measure deviations from a 50:50 sex ratio, and this requires surprisingly high population sizes since the binomial distribution has a broad center. For instance, to detect a true underlying sex ratio of 0.4 or 0.6 (away from our null of 0.5), we would need population sizes of >780 lizards to detect a significant skew 80% of the time. This is just an illustration, but the main point is that these population sizes might not exist for a given species – and so detecting significantly skewed sex ratios might not be possible at all. This is especially difficult when looking at small or endangered populations – there sex ratio skew might be a big problem, but impossible to demonstrate statistically. The general takeaway here is that sex ratio skew in a population can be biologically important, but not statistically significant.

We then used both the categorization of the anole species by sexual size dimorphism (low or high SSD) and the measured sexual size dimorphism of each population (calculated by average male SVL divided by average female SVL, minus 1). We used both of these estimates of SSD to test whether the sex ratio of a population correlated with the sexual size dimorphism of that population, as predicted by sexual selection theory. Turns out we were completely off – there was really no correlation between sex ratio skew and measured SSD, categorical SSD, or ecomorph (see figure 1, posted below,  for a visual of this lack of correlation!).

Figure 1 (from the paper) : Sex ratio versus sexual size dimorphism. Sex ratio is represented as the proportion of males among adults in the population, while sexual size dimorphism was calculated dividing the average SVL of the larger sex by the average SVL of the smaller sex, and subtracting 1 for each population. Each circle represents 1 of the 21 localities sampled in this study. The dashed line represents an equal sex ratio of 0.5. We found no relationship between sexual size dimorphism and sex ratio across the 21 localities (PGLS: adjusted R2 = −0.08, P = 0.86).

So what’s the general message here? Sexual size dimorphism does not correlate with adult sex ratios across anole species, and so the relationship between strength of sexual selection, sex ratio bias, and sexual size dimorphism may be more complicated than we initially assumed. However, anole sex ratios can range widely between species, and within populations. Given the variance within anole species, the adult sex ratio is probably a better description of a locality, or population, than an intrinsic quality of an entire species. We also think that the influence of various localized environmental factors may impact sex-specific mortality or dispersal, which in turn which cause differences between localities in adult sex ratio skew.

This is my first anole paper, and it’s really nice to see all the brainstorming and discussions put into print. It was also great to get to know and work with Michele, and learn more about her research and behavioral work in anoles (we even got to meet in person at the Evolution conference last year!). This paper was also my first small step into the world of sex ratio and sex determination theory which now forms a large part of my PhD work, so I’m very grateful for the introduction to the subject. Anyway, feel free to email us with any questions and we hope you enjoy the paper!

Paper here: Sexual selection and sex ratios in Anolis lizards

Figure 1. Anolis cristatellus male in survey position.

Foraging behavior reflects a trade-off between the benefits of obtaining vital resources and the potential costs of energy expenditure, missed mating opportunities, and predation. Through time, selection should canalize foraging behaviors that optimize fitness within a given environment, but novel habitats, like urban landscapes, may require behavior to change. For example, human-landscape modification often results in significant reductions in structural complexity of habitat as compared to natural areas, potentially leaving individuals with a greater sense of perceived vulnerability as they venture out to feed. Moreover, these landscapes can alter the diversity and density of predators in ways that might leave prey with a greater sense of perceived predation risk.

In a recent paper in Urban Ecosystems, Chejanovski et al (2017) sought to quantify differences in foraging behavior between anoles from urban areas and those from more natural, forested locations. They utilized two trunk-ground anoles: Anolis sagrei in Florida and A. cristatellus in Puerto Rico. In both urban and natural habitats, they located male lizards in survey posture (Fig 1), which indicates an individual is likely searching for food, and placed a tray with mealworms on the ground at a fixed distance from the perch. They measured each lizard’s latency to feed which was the time it took to the lizard to descend from its perch and capture a mealworm.

Because the availability of complex habitat structure and the proximity of predators might both influence foraging behavior, they experimentally manipulated perch availability for A. sagrei and predator presence for A. cristatellus in both urban and natural habitats. For A. sagrei, they provided half the individuals with two extra perches between the lizard’s original position and the food tray. For A. cristatellus, they manipulated perceived predation risk by placing a static bird model on the opposite side of the feeding tray from half the lizards.

Additionally, they measured several other factors that might influence foraging behavior: the number of available perches within a fixed radius of each lizard – increased habitat complexity might result in lower perceived predation risk; perch height of each individual – those that perch lower to the ground may be more motivated to feed and those that perch higher may be satiated; estimates of body temperature by placing a copper model at the original position of each lizard – body temperature can influence locomotor function and this may have consequences for how easily a lizard can escape predation and play a role in its perceived risk. They also measured the density of conspecifics in the immediate vicinity and noted when conspecific individuals captured mealworms from the feeding tray.

Finally, they measured SVL and mass for a representative sample of each population (urban and natural) in order to calculate body condition. Trade-offs between costs and benefits of foraging decisions can be influenced by satiation of hunger, and body condition, which increases with food consumption, may indicate the extent to which individuals are well-fed.

For both species, lizards from urban areas had a longer latency to feed and demonstrated lower overall response rates to food trays; many individuals never attempted to capture a mealworm in the allotted time (20 minutes). For A. sagrei, habitat (urban vs. natural) best explained feeding latency, but perch height and the presence of conspecifics were also important determinants of feeding latency for A. cristatellus. Individuals perching lower had shorter latency, and latency was shorter when a conspecific attempted to feed from the tray. Neither experimental perch availability nor perceived predation risk (bird model) had any influence on foraging behavior. In both species, individuals from the forest were smaller (SVL) and less massive than those from the city. Body condition was higher for urban A. sagrei but did not differ between natural and urban habitats for A. cristatellus.  

Differences in foraging behavior for male A. cristatellus between natural and urban habitats.

Because of the reduced availability of perches and structural complexity in urban habitats, urban lizards could have generally higher perceived predation risk and this might explain their reluctance to feed; however, experimental perch availability did not influence foraging behavior for A. sagrei and an artificial predator had no effect on A. cristatellis. The latter may simply reflect that the experimental predator was stationary and a moving predator may have elicited different results.

It is possible that foraging differences reflect food availability in urban vs natural habitats, and thus motivation to forage. Urban anoles had higher body condition and may be generally better fed than those from the forest; however, the authors found no significant correlation between individual body condition and latency to feed. It is also possible that mealworms represent a novel food source for urban anoles, and this resulted in a hesitance to initiate feeding since many animals are reluctant to approach novel objects/ food (neophobia).

In summary, this study demonstrates that differences do exist in foraging behavior for two distantly related species of anoles between urban and forested habitats. The increased latency to feed observed in urban anoles could be due to perceived predation risk, foraging motivation, neophobia, or some combination. What is left to be determined is the extent to which these behavioral differences might be adaptive in their respective habitats.