I'm a Ph.D. candidate at UMass Boston in the Revell lab. I am interested in how animals respond to urbanization from an ecological and evolutionary perspective. My dissertation research has focused on adaptive shifts in the Puerto Rican crested anole, Anolis cristatellus, in response to urbanization.
View all posts by Kristin Winchell →
Late Breaking: one last Evolution 2017 post! Last weekend during the Evolution meeting, I had a chance to chat with Iris Holmes (Ph.D. student, University of Michigan) about the poster she presented. Initially not on our watch list because of the lack of “anole” in the description, my eye caught the dewlapping lizard perched at the top of her poster from across the room.
Iris presented her work on gut microbiomes of two groups of lizards: anoles and ameivas. She wanted to know if different taxa have different gut microbiomes and to what extent diet influences bacterial composition of gut microbiomes. Her collaborator (Ivan Monagan) collected scat samples from 22 Anolis dollfusianus and 9 Ameiva from an agricultural area in the Soconosco region of Chiapas, Mexico. Together, they then sequenced both the gut bacteria and the digesting prey with two 16S primers. Iris chose to target the prey as well because she wanted to know if they were eating different things and how different stages of digestion influence gut bacteria communities.
Iris found that there were no clear differences between the gut microbiomes of anoles and ameivas. Both species had gut microbiomes dominated by three main phyla: Proteobacteria, Firmicutes, and Bacteroidetes. Little is currently known about how these bacteria relate to digestion and health in reptiles, but Iris commented that we can make some guesses based on studies in other taxa. Proteobacteria are a disease indicator in mammals, but appear to be normal in reptiles and birds. Firmicutes and Bacteroidetes are both important for digestion of carbohydrates and fats (respectively) in mammals. Iris found that there was a loose correlation between the amount of prey consumed and the abundance of Bacteroidetes, suggesting these bacteria also play a role in digestion in lizards. She also found that there was an apparent tradeoff between the Proteobacteria and the two other groups – sequence abundance of proteobacteria was negatively correlated with abundance of Bacteroidetes and Firmicutes. Overall, this is an interesting first step in understanding the gut microbiomes of reptiles and how they differ (or don’t) between groups.
Bright and early on the last day of the annual Evolution meeting, James Stroud (Florida International University) presented his work on character displacement in novel communities of introduced anoles in Miami. In this elegant use of a natural experiment, James looked at the novel co-existence of two anoles in their introduced range and wondered if character displacement was occurring as predicted when two ecologically similar species are found in sympatry. Specifically, James wanted to know if Anolis cristatellus and Anolis sagrei would shift their habitat use when in sympatry, resulting in correlated shifts in morphology. These species are both trunk-ground anoles of roughly the same body size. They are native to Cuba/Bahamas and Puerto Rico (respectively) and are diverged by ~50 million years.
James hypothesized that in their introduced range in Florida, these two species would diverge ecologically in sympatry but be more similar in allopatry. He found that in allopatry, both speciesattained similar relative abundances and perched at similar heights. However, in sympatry, both decline in relative abundance suggesting that these species are interacting strongly with one another. Even more interesting, in sympatry A. sagrei perches lower and spends more time on the ground than it does in allopatry, while A. cristatellus perches higher!
Next James hypothesized that these ecological shifts could lead to shifts in morphology. If A. sagrei is spending more time on the ground, perhaps longer limbs would be favored. Similarly, if A. cristatellus is spending more time higher up in the trees, perhaps there would be selection for stickier toepads. As predicted, A. sagrei had longer forelimbs and hindlimbs in sympatry. However, he did not find any difference in toepad morphology between sympatric and allopatric populations of A. cristatellus. Instead, he observed that A. cristatellus in sympatry with A. sagrei had significantly smaller heads.
James ended by wondering if alternative behavioral and social mechanisms may drive these observed shifts in head morphology. Either way, this case study provides an interesting insight into how a complex range of adaptive responses can result from a seemingly simple ecological interaction.
At last night’s poster session, undergraduate Derek Briggs (U. Mass. Boston) presented findings from his senior capstone project in which he looked at several traits related to dominance and health. Using a dataset of x-rays and dewlap photos collected over a 4 year period from various urban and forest sites across Puerto Rico (by Kristin Winchell), Derek looked at body size, body condition, dewlap size, and injury rates (broken bones and missing digits) to see if there was a difference in frequency between urban and forest habitats.
Derek and his co-authors chose these traits because they thought they might be impacted by shifts in lizard density and distribution in the urban habitat which may lead to increased male-male competition. Specifically, in urban habitats, lizards tend to perch closer to one another because the potential perches are more clustered. This increase in local density could lead to increased encounter rates and fights over optimal perch sites, food resources, or mates. Derek hypothesized that this shift in distribution should lead to shifts in these traits, although he did not have a prediction about the direction of these shifts.
Derek Briggs with his poster.
Derek found that urban lizards were consistently larger than forest lizards in terms of snout-vent-length (SVL) but that body condition (mass~SVL) did not consistently differ between sites. Although all paired populations had significant differences in body condition, in some municipalities lizards were fatter in urban habitats and in some they were fatter in forests. In terms of dewlap size, Derek did not find any significant trends, although he still has quite a few dewlap photos to analyze still, so stay tuned!
In terms of injuries, Derek did not find significant differences between forest and urban animals for bone breaks or missing digits. However, these are rare events to begin with, so it is possible that a much larger sample size is needed to detect a difference. His findings do suggest a trend of more bone breaks in urban populations, and more missing digits in forest populations. He attributes this trend to either elevated male-male competition in urban habitats or differences in predator communities.
We look forward to seeing the full results from Derek’s honors thesis.
With summer just around the corner (any day now, Boston!) that can only mean one thing – the annual ASN/SSE/SSB sponsored Evolution meeting is almost here! This year the anole community is attending in full force with 2 posters, 11 regular talks, and 2 symposium talks.
We regularly cover this meeting here at Anole Annals, and once again we are asking for YOU to help us out. If you will be attending Evolution and are interested in writing a short blog post about one or more of the talks or posters, send me an email (email@example.com) or comment below. I will give you all the information you need to get started and a little help on how to write a blog post for us if you haven’t done so before. We always appreciate the extra help and fresh perspectives.
For those of you not attending the meeting (or maybe still debating attending), here’s the current list of anole talks in the schedule. Are you particularly excited about a talk at Evolution this year? Did we miss a talk that should be on our list? Let us know in the comments!
Are we wrong about territoriality in Anolis lizards?
Evolutionary analysis of viral strains infecting a single anole species
Deeply conserved genetic constraints influence adaptive radiation of Anolis lizards
Macroevolution of the dewlap and diversification of Anolis lizards
Using sexually antagonistic skewers to explore the genetic architecture of sexual dimorphism in Anolis lizards
Evaluating the evidence for protein coding convergence in phenotypically convergent anoles
Variation in dominance traits and body condition in urban Anolis cristatellus
Population trascriptomic analysis of ecologically differentiated, partially reproductively isolated Anolis lizards
Natural selection in behavior? A field experiment with Anolis lizards from the Caribbean
Temporal variation of anthropogenic perch use by populations of forest and urban lizards
The influence of relatedness and size on spatial structure in an urban population of Anolis carolinensis lizards
Urban adaptation in Lizards: Connecting phenotypic shifts with performance and survival
Character displacement in evolutionary-novel Anolis lizards
Does competition between the Dominican native Anolis oculatus and the invasive Anolis cristatellus drive changes in ecological, agonistic and reproductive traits?
Population genomics of Anolis carolinensis transposable elements: insertion polymorphisms are abundant but rarely approach fixation
Urbanization creates drastic changes to habitats leading to differences in microclimate, perch characteristics and distribution, and ecological communities (competitors, prey, and predators) when compared to natural (forest) habitats. Studies have found increased rates of mortality of many urban species due to generalist urban-tolerant predators such as raccoons, feral cats, and domestic animals (Ditchkoff 2006). Anolis lizards are able to voluntarily drop their tails (“autotomize”) when challenged by a predator, enabling their escape in many instances. The maimed lizards are able to regenerate their lost tails, though the replacement tail is a rod of cartilage and not the original bony vertebrae. The regenerated tail portions are often a different color and texture, and the lack of vertebrae / cartilage rod are clearly visible in X-rays.
We hypothesized that autotomy rates would be more similar between urban areas in different municipalities than to natural areas in the same municipality due to similar predator regimes in urban sites across the island. We compared the frequency and pattern (number of caudal vertebrae remaining) of caudal autotomy of A. cristatellus between urban and natural areas in Puerto Rico.
X-rays of our samples with an intact tail (A) and an autotomized tail (B).
We sampled A. cristatellus from paired natural and urban sites in four Puerto Rican municipalities: San Juan, Mayagüez, Ponce, and Arecibo. The natural sites were high quality natural forests and the urban sites were high-density residential areas. Urban sites were dominated by asphalt and other impervious surfaces, had sparse tree cover, and a large fraction of potential perches were manmade surfaces such as walls and fences. We scored 967 X-rays from these eight sites for caudal autotomy and counted the number of remaining tail vertebrae. We tested for an effect of urbanization on caudal autotomy by fitting a logistic regression model with municipality (San Juan, Mayagüez, Ponce, Arecibo) and site type (urban, natural), and their interactions, as model factors, and body size as a covariate.
Our data shows that lizards found in urban sites have a larger probability of having autotomized tails.
Interestingly, we found higher rates of autotomy in all urban populations compared to nearby natural areas. Differences in autotomy might be explained by differences in predator density and efficiency (Bateman 2011). For example, inefficient predators (those that more often than not fail to capture their prey) tend to leave behind more lizards with broken and regenerated tails (Schoener 1979). In addition, a greater abundance of predators could result in more predation attempts. Unfortunately, we did not collect data on predator abundances or community composition, so we cannot distinguish between these (non-mutually exclusive) explanations. Higher rates of autotomy in urban areas could thus reflect any of a variety of factors, including (but not restricted to) inefficient predators in urban areas, a shortage of refuges offering protection from predators, or an increase in predator density.
For lizards with autotomized tails, we found no significant difference in caudal vertebrae number between urban and natural sites.
Lastly, we did not find that lizards with autotomized tails in urban areas had lost more (or less) of their original tail to caudal autotomy. Since regenerated tails cannot be autotomized past the original break point (i.e. cartilage cannot autotomize), this suggests that lizards in urban areas are no more likely to be subject to multiple unsuccessful predation attempts (resulting in caudal autotomy) than lizards in natural forest. Future investigation quantifying predation attempts or predator community composition in urban and forest habitats could help us better understand the source of this intriguing pattern.
BATEMAN, P. W., AND P. A. FLEMING. 2011. Frequency of tail loss reflects variation in predation levels, predator efficiency, and the behaviour of three populations of brown anoles. Biological Journal of the Linnean Society 103:648–656.
DITCHKOFF, S. T. 2006. Animal behavior in urban ecosystems: modifica- tions due to human-induced stress. Urban Ecosystems 9:5–12.
SCHOENER, T. W. 1979. Inferring the properties of predation and other injury-producing agents from injury frequencies. Ecology 60:1110–1115.
In this outreach project, James and colleagues had 101 schools participate in collecting data. Armed with a handy anole ID guide created by Jason Kolbe and a video by James explaining anole biology and species differences, students and teachers set out to conduct 15 minute visual surveys. On these surveys, they recorded how many animals they encountered, the species ID, and the approximate body size using a provided standardized collection protocol and entering data into a Google forms site.
The results were overwhelming: more than 1,000 students conducted a total of 1,356 surveys resulting in 12,000+ lizard observations! This project produced massive amounts of data on very short time frames. In general, distribution patterns fell as they were expected to, although some records certainly hint at some mis-identification (e.g. some A. cristatellus locations). Unsurprisingly, the least abundant lizards were those that were hardest to detect: the species typically found high in trees.
While the resulting dataset is impressively large, James admits that there are data quality issues with collecting data in this manner and asked for input on how to improve data collection. Specifically, he suggested that in the future they would like to incorporate photographic and smartphone GPS information, perhaps via an app. Does anyone have any suggestions for James on implementing such an app or otherwise improving the design?
James emphasized that providing meaningful natural experiences with wildlife for kids is good for conservation, fosters an appreciation for nature and helps inspire the next generation of scientists. Many of our readers may find inspiration from the success of this program and we would love to hear about it if you implement similar types of citizen science projects with anoles!
Travis Hagey presented some new results from his ongoing research on the evolution of functional traits in lizards. Travis normally works on geckos, but frequently includes Anolis species in his studies. Last year at Evolution, Travis told us about toepad evolution by comparing gecko toepads to those of anoles and skinks. Along the same vein, this year at JMIH Travis talked about patterns of limb-length across different lizard groups.
Travis started with anoles as an example of morphology being correlated with habitat use. As we all know, anole limb length is associated with structural habitat. Lizards like Anolis occultus (a twig anole) use thin perches and have very short legs. Other species that perch on broader substrates tend to have longer legs. Travis is interested in finding out if this pattern holds for other groups of lizards.
He started by comparing anoles to geckos to see if relative limb length differed between the groups. He accumulated an impressive database of hindlimb lengths from many gecko and anole species and when he looked at the relationship between hindlimb length and body size (SVL), he found that for a given body size anoles tended to have longer limbs than equivalently sized geckos. He then added in data for a number of species from Liolaemus, Tropidurus, and Phrynosomatidae. Interestingly, he found that these other groups all clustered with the anoles. This suggests that there are possibly two relationships between limb-length and body size across lizards.
Travis ended by commenting on how this might relate to habitat use. He analyzed hindlimb length by perch diameter for anoles (red line) and geckos (black line). Geckos, it turns out, have a different relationship between perch use and limb length than anoles: geckos with shorter limbs tend to use broader diameter perches! Travis is still working on this research and is looking for data on limb length for many groups. If you have hindlimb length data from lizards you should email Travis to help out!
Kevin Aviles-Rodriguez, from the Revell lab at U. Mass. Boston, gave the second urban anole-themed talk of the meeting. Kevin presented his Master’s thesis work that he conducted with the Kolbe lab at U. Rhode Island in a talk titled, “Structural habitat alterations caused by urbanization influence escape behavior of a common lizard.”
Urban habitats are drastically modified and present novel resources and threats for animals that persist and utilize these spaces. Structurally, urban habitats have different types of surfaces that are smoother, broader in diameter, and often more vertically oriented (90° angle). Urban habitats also present abundant and novel food resources in terms of human food and insects attracted to lights and garbage. But with the abundance of food and novel niche space also comes an abundance of novel predators such as cats and dogs kept as pets.
Kevin wanted to know how Anolis cristatellus from San Juan, Puerto Rico and South Miami behaved in urban habitats compared to forest habitats when perceiving a predation threat. Although there are obvious costs of not escaping a predator successfully, there are also costs of fleeing when not necessary in terms of lost feeding opportunities and disrupted social interactions (mating, territory defense). Kevin wanted to know if the urban environment influenced escape behavior decisions. Specifically, he had two objectives: (1) To quantify escape behavior (squirreling, jumping, or sprinting) and how this relates to different types of perches found in urban areas. (2) To measure flight-initiation distance (FID), or how close one can approach an animal before it flees, to see if there are differences between forest lizards and urban lizards.
Kevin found that as perch diameter increases, the probability that a lizard will squirrel around a perch or sprint up the perch increased and the probability of jumping decreased. Interestingly, when he also looked at perch use, he found that the majority of lizards were using perches of thinner diameter where the probability of jumping was highest. Urban lizards also tended to use more isolated perches, which he defined as the number of nearby potential perches within 1 meter. When nearby perch density was lower, lizards tended to jump less – perhaps not all that surprising since they have fewer places to jump to. Kevin also found that escape strategy differed based on the type of perch used. In urban habitats, on trees and on metal posts lizards squirreled more frequently than they did in forest habitats. Interestingly, on cement walls (e.g. buildings) lizards did not jump at all and mainly sprinted to escape. Kevin offered a few possible explanations for this trend. For one, building perches tend to be more isolated than trees and so it may simply be that lizards on these substrates have nowhere to jump to. A second possibility is that the lizards have trouble jumping from these perches since they are more vertical than the optimal angle for jumping (39-42°, Toro et al. 2003).
In his final analysis, Kevin found that flight initiation distance (how close you can get to the animal before it flees) was very short for animals perched on urban trees and metal posts. In fact, he commented that on some occasions he was able to get close enough to touch the lizard before it fled! This difference was significantly shorter than for animals perched on trees in the forest and for animals perched on painted concrete walls in the city.
Bright and early this morning, Christopher Peterson kicked off the anole talks of the day on the topic “Intraspecific color and habitat use variation in Anolis conspersus.” Christopher noted that on Grand Cayman there appear to be three color morphs for A. conspersus: brown, blue, and green and asked if color morph was correlated with habitat use. Christopher captured 309 lizards across the island, photographed them for color analysis, and took a large number of habitat measurements plus basic morphology of the lizards (mass, SVL). When analyzing the color data, however, he noticed that the picture was not so clear: many of the lizards had both blue and green coloration. Since these were not discrete groups, instead he analyzed body pattern, which appeared to be more discrete and showed the same geographical variation. In general, lizards on the East of the island were brown and spotted while the lizards on the West of the island were green/blue with vermiculated pattern.
Using a complex logistic regression, Christopher analyzed the discretized character state with his habitat and morphological measurements. Disappointingly, he found no associations between morphology or habitat use with body patterns. He concluded that the variation in pattern and coloration is probably best explained by geographic location alone and that future genetic analyses may help clear up if this is a geographical cline with isolation by distance.
Quynh Quach presenting her Master’s thesis work at JMIH.
Quynh Quach, a master’s student from the Revell Lab at U. Mass. Boston, presented her thesis research on “Phylogeography and Population Structure of Anolis cristatellus on the island of Vieques.” Before Quynh joined the Revell lab, former post-doc Graham Reynolds and former Losos lab undergraduate Tanner Strickland looked at the phylogeography of Anolis cristatellus across Puerto Rico and the Virgin Islands using mitochondrial DNA (in review). Tanner’s work revealed that there was a mitochondrial break on the island of Vieques, just off the coast of Puerto Rico. The mitochondrial data suggested that there were two genetically different groups of A. cristatellus, one on the East and one on the West of Vieques. The only problem was, as we know, mtDNA patterns are not always supported by nuclear whole-genome DNA patterns. In addition, Tanner’s dataset only consisted of 9 samples from Vieques.
When Quynh joined the lab, she wanted to know more about this pattern. Would this division be supported by nuclear genome analyses? Were these lineages anthropogenically introduced? If not, what was the origin of these groups – historical allopatry followed by secondary contact or isolation by distance? So she set out to answer these questions by collecting 300 tail tips from across the island of Vieques, extracting and sequencing both mtDNA and nuclear DNA.
The mtDNA variation shows a strong geographic pattern.
Quynh first constructed a mitochondrial phylogeny to verify the pattern observed by Tanner and Graham. The mtDNA analysis confirmed that there are 2 mtDNA clades on Vieques with strong geographic patterns. The island-wide pattern of mtDNA variation was not what we would expect if anthropogenic introduction were the cause since this would be unlikely to show such a clear East-West pattern with the small contact zone in the middle. So then how did this pattern arise?
Analysis with K=2 shows two clear groups associated with the East and West.
To answer that question, Quynh next looked at nuclear DNA using RADseq. She sequenced 48 individuals: 5 from Virgin Islands, 6 from Puerto Rico, and 37 from Vieques, then de novo assembled the genome and called 16,808 SNP’s. She ran STRUCTURE and DAPC analyses on this data and found that the Virgin Island samples form 1 cluster and Puerto Rico and Vieques form a second cluster with 4.1% divergence between the groups. But she wondered, what if we look at just Vieques and specify K=2? When she did this with DAPC and saw a clear geographic pattern similar to what she found with the mtDNA. Finally, she tested whether this represented isolation by distance. She found that there was significantly reduced gene flow between geographically distant individuals, supporting this hypothesis as the most likely cause of the variation.
Lastly, Quynh emphasized that it is important to consider multiple genetic markers and not just rely on mtDNA results. Had the group stopped at their original mitochondrial analysis, they would have reached a very different conclusion.
In Jonathan’s talk entitled “Known knowns and unknown unknowns: herpetological progress in fits and starts”, Jonathan started by paying homage to Ernest Williams. He managed to find slides from Ernest’s 1981 plenary address in which the perception at the time of anole biology was compared to a well-built building. All there was to know about anoles was known… or so people thought. In reality, the building looked more like this:
E.E. Williams slide on the state of anole knowledge from 1981
The metaphorical building at the time was in fact only partially built, with bits and pieces of different areas more complete than others. Jonathan’s talk focused on the fact that despite over 3 decades of progress, so much is still unknown about anoles, including basic natural history of many species. And so Jonathan shared with us a few stories highlighting some surprising anole findings and remaining unknowns, featuring the work of his students from the past 20 years:
One surprise finding over the past 30 years is that several anole species have deep mitochondrial splits. Anolis oculatus, for example, on the tiny island of Dominica has 4 distinct lineages with as great as 10% mtDNA divergence (Malhotra and Thorpe 2000)! And they aren’t the only ones. Rich Glor and Jason Kolbe really broke this story open with their analysis of several anole species showing multiple mitochondrial lineages for each (Kolbe et al. 2007). This brings into question our estimates of diversity. If every species is actually 4+ species, have we underestimated diversity?
According to Jonathan, it seems that the “dawn of anole discovery” peaked in the 1970’s – the last very distinctly different anole was discovered nearly 40 years ago. And yet just last month, Luke Mahler et al. published a record of a new species of anole discovered on the island of Hispaniola! Hispaniola has been intensely studied by anole biologists, making this all the more surprising. In honor of the naturalist that found the species in the wild, the authors named the new species Anolis landestoyi. This new species has a striking appearance, similar to a chameleon and to the Cuban “false chameleons” (Chamaeleolis clade of anoles), and brings up the question of whether there might be a seventh ecomorph.
Anolis landestoyi, photo by D. Luke Mahler
Highlighting the work of two other Losos Lab members, Alexis Harrison and Ambika Kamath, Jonathan talked about how little we know abut anole territoriality. Conventional knowledge says that males maintain polygynous territories and don’t move too far. But Ambika has shown in her dissertation work that male Anolis sagrei actually move quite a bit, and Alexis has shown that male Anolis carolinensis mate with females on opposite sides of their site, not just nearby females! In general, Jonathan commented that there is a large amount of work to be done still on social behavior in anoles.
Anolis proboscis (photo by Luke Mahler)
Jonathan talked about the Anole Annals darling, Anolis proboscis. This understudied species sports a large nasal projection of unknown purpose. This odd species was thought to be extinct for many years until it was “rediscovered” only a few years ago. While sexual selection seems like an obvious cause of this structure (the females do not possess horns), its not clear what the males use it for. The obvious hypothesis, that it is used for male-male combat, is easily refuted by video demonstrating that this structure bends easily. Moreover, it appears that they can bend the horn, as seen in this video! The mystery of this structure’s function remains unsolved.
Finally, Jonathan talked about an interesting anecdote: that Anolis agassizi from Malpelo island seems to have a strange preference for the color orange, as described by Rand et al. (1975). Jonathan described a recent test of this preference replicating the Chuckles candy experiment (the experiment has been described here on Anole Annals) and confirming that this species does, in fact, prefer the colors orange and yellow when it comes to Chuckles candy. He also showed a video of A. agassizi swooping in from afar to eat (attack?) an orange. Why are they so attracted to this color? Sounds like a project waiting to happen.
In short, Jonathan emphasized these two main points:
1. Natural history information is key; you need to know basic aspects of biology and natural history to dig into the deeper questions.
2. There are so many questions to be answered about anoles still, and room for all who want to join the party.
Shane Campbell-Staton giving his talk at Evolution 2016
We’ve heard about the effects of polar vortexes here on Anole Annals before. The infamous 2013/2014 event brought record-breaking snow and low temperatures to the Southern U.S., leaving people and animals both a little chilled. This created the perfect opportunity for Shane Campbell-Staton to investigate the effects of such extreme events on thermal tolerance of the native Carolina Anole, Anolis carolinensis. Shane also spoke about this at SICB earlier this year, and AA contributor Martha Muñoz covered the talk pretty thoroughly here on Anole Annals. Nevertheless, I’ll summarize some key points here in case you missed it.
An unlucky lizard during the polar vortex snow storms in the South.
Shane got lucky in the sense that he had measured thermal tolerance in August 2013 for populations affected by the polar vortex, 5 months before the event. Typically, the cold arctic air is tightly constrained around the North pole, but periodically the boundaries weaken and the cool air expands southward. These events are not regular, so Shane had no idea one was coming that winter or that it would extend so far south. It was serendipitous that his study populations, 3 in Texas and 1 in Oklahoma, were impacted by the extreme weather event. This species, particularly in the Southern portion of its range, is not used to low temperatures and reports came in of anoles dying off during the storm.
Air temperatures for January 5-7, 2014, compared to the 1981-2010 average. Map by NOAA Climate.gov
So Shane returned in August of 2014 and sampled again, curious as to how this cold impacted thermal tolerance. He found that tolerance to low temperatures, measured as critical thermal minimum (CTmin), was lower in some populations after the event! Even more, the difference was greatest in the Southernmost population (Brownsville, Texas). Shane returned again in the fall of 2014 to see if this effect persisted or if it was simply a plastic response to the event. He found that the populations sampled in 2014, and presumably their offspring, still had lower critical thermal minimums. This result suggests that the extreme cold weather had caused an evolutionary shift in cold tolerance via natural selection: only the animals that could tolerate the cold temperatures survived and passed on their cold-tolerance genes. Shane went on to conduct a common garden study to verify that the trait was not simply a plastic response. He found that the lower CTmin persisted in lab-reared animals: strong evidence that these shifts had a genetic basis.
Lastly, Shane looked at the functional genomics of cold tolerance. Using liver tissues to obtain transcriptomes (representing expressed genes), he found several gene modules associated with thermal tolerance including some associated with respiratory electron transport chain, lipid metabolism, carbohydrate metabolism, and angiogenesis/blood coagulation. He also found that the gene expression patterns in the Southern populations affected by the storm resembled the Northern populations that more regularly experience cool temperatures, indicating a common genetically based adaptive response across populations.
Ivan Prates presents his poster at Evolution 2016.
Here at Evolution 2016 there have been a lot of anole talks and posters. In fact, there have even been several that pretend to not actually be about anoles. Ivan Prates presented a poster which he insisted, despite multiple pictures of anoles and the use of anole DNA, was not actually about anoles… Instead, this poster was actually about the historical extent of Brazilian forest cover (or so he says).
In short, Ivan used genomic data to understand historical patterns of dispersion and distribution of South American anoles in order to infer patterns of rainforest expansion and contraction. He suspected that the geological data gave a false interpretation of rainforest patterns in Amazonia and the Atlantic Forest in Brazil, and that anoles could help tell the true story of how the forests have changed over time. By looking at species with strong genetic signals associated with forest shifts he hypothesized that true forest patterns could be elucidated based on the historical demography of these species.
Ivan and coauthors looked at three species of lizards: Anolis punctatus, Anolis ortonii, and Polychrus marmoratus. They used the next-generation sequencing technique Genome by Sequencing (GBS) to answer three main questions: (1) Did all 3 species experience range expansions simultaneously? (2) Did populations expand and contract at similar points in time? (3) How did population sizes vary over time? While all three of these questions are about anoles, don’t forget that this poster was actually about the forest.
Ivan found that the Atlantic Forest individuals composed a monophyletic group nested within the Amazonian lineage. This suggests that the anoles of the Atlantic Forest on the coast actually arose from a single colonization event from Amazonia. The land between Amazonia and the Atlantic forest is presently quite arid compared to the rainforest – more like grassland. This presumably forms a barrier to contemporary dispersal, which implies that historical dispersal must have involved greater habitat connectivity. So Ivan’s results support the hypothesis that the forests experienced a drastic historical expansion creating a contiguous habitat that enabled dispersal around 1 million years ago. Interestingly, the timing for the dispersal of all 3 species was approximately the same. A million years ago seems to have been the ideal time to move to the coast for Brazilian anoles.
Ivan and his colleagues also looked at how populations size changed over time. He found that whereas Anolis punctatus experienced a trend of population expansion, Anolis ortonii and Polychrus marmoratus experienced population contractions. It was surprising to the authors that these species did not respond the same – why did only one of the species experience population expansions? They suspected that the expansion of one species might be related to the population contractions of the others, perhaps because of competition. However, their analysis on synchrony of population trends proved otherwise. They found that although trends within species were synchronized across populations, between species the shifts in demography were asynchronous. In other words, when one species expanded or contracted in population size, the others were stable. Ivan concluded that this was support for the idea that these populations were not influencing each other and that instead there was some other factor independently controlling population size fluctuations – perhaps precipitation patterns.
In conclusion, Ivan told me a lot about the demography of anoles during the Quaternary, and a little about the forest. I look forward to hearing more about his “forest” research on these understudied mainland anoles!
Anoles, in particular Anolis carolinensis, have long been considered an ideal group for studies investigating thermal physiology, reproductive endocrinology, and even regeneration. With the recent publication of the A. carolinensis genome (see AA posts on this here and here), the possibilities for new genomic studies in this new model species have significantly increased.
Joseph Manthey and co-authors used this new resource to clarify the phylogeographic relationships of A. carolinensis. Previous research on the phylogeography of A. carolinensis using both mitochondrial DNA and nuclear DNA showed that there were 5 clades. However, the relationships between these groups differed between the two approaches. Joseph looked at the genomes of 42 individuals from 26 localities across the native range to determine the true evolutionary relationship between regional groups and to shed light on the demographic histories of the groups. Manthey sequenced 500 loci using an anchored hybrid enrichment approach.
STRUCTURE analysis showed that the clusters had little admixture
Manthey et al. found that the genomic data predicted 5 genetic groups, in agreement with both the nuclear and mitochondrial analyses previously done. Their results also indicated that the 5 genetic clusters were distinct with little admixture. However, the relationships between groups did not agree with either the mitochondrial or nuclear trees, yet all nodes had extremely high support (93-100%)
Finally, Manthey commented on the likely timing of this diversification and associated demographic trends. Their results indicate that the initial split occurred during the late Miocene or early Pliocene and that the remaining diversification occurred during the Pleistocene. They also found that the most Southern population had a significant number of fixed genes while other populations did not. This suggests that this group was likely the oldest and most stable and supports an “out of Florida” hypothesis of diversification.
Tamara Fetters, from the McGlothlin lab at Virginia Tech, reported on her ongoing work on thermal physiology in Anolis sagrei during the first poster session here at Evolution 2016 in Austin, Texas. Tamara looked at thermal tolerance and sprinting abilities at different temperatures and how that related to the latitude of the population. Specifically, she asked if lower temperatures regularly experienced by the Northern populations influence cold tolerance and performance at those temperatures. She expected that Anolis sagrei, native to Cuba and the Bahamas and introduced into the Southern U.S., would show signs of adaptation to its new, colder home in the more Northern mainland populations compared to the native range island populations in the South.
Tamara’s poster focused on two main experiments. In the first she calculated thermal tolerance to cold temperatures using a classic critical thermal minimum (CTmin) setup: with an ice bath she slowly lowered the body temperature of each animal until it was unable to right itself. This method approximates the minimum temperatures that the animals can handle in the wild. She found a clear trend showing a decrease in the minimum temperature tolerated as latitude increased. In short, Northern populations could handle the cold and Southern populations could not.
In the second experiment, Tamara acclimated the lizards to 6 temperatures ranging from 12-41 °C before running them up a track to calculate sprint speed. Tamara used an impressive 25-50 animals from each of 5 populations! She calculated sprint speed from the high-speed video she took using the program Kinovea. Tamara found that across all temperatures the most Southern population ran the slowest while the most Northern population ran the fastest, with the differences remaining fairly constant.
So what’s next for Tamara? She is planning on rearing animals in a common garden setup with some animals in hot temperatures with low variability between day and night (mimicking the native range, Southern habitats) and some animals in cool temperatures with high variability between day and night (as is experienced in the Northern habitats). She hopes that these studies will help her understand the genetic basis of this thermal tolerance and the extent of plasticity in thermal adaptation.
One last note – Tamara wanted to thank Anole Annals for helping her determine her study locations. She was able to determine which areas were likely to have Anolis sagrei and how far North they have spread because of Anole Annals posts (like this one) and comments.
We just wrapped up our Anole March Madness tournament in which we brought to you many fictional battles of mainland and island anoles. We researched each species included in the tournament and highlighted some little-known facts about the participants. We told you about dewlap colors, ecomorphs, habitat use, invasion, body patterns and colors, and much more. But finding this information for each species was more challenging than we originally expected. The state of anole knowledge is certainly imbalanced.
Looking at the number of Google Scholar citations for each species shows just how imbalanced our knowledge of different species of anoles is. Of the species we included, only three of the mainland species had more than 200 citations and none had more than 600. In contrast, of the island species, six had more than 200 citations and Anolis cristatellus had a whopping 1230 citations! Within regions there is quite an imbalance, too — check out how many more studies there are on Central American species compared to South American species (orange and red) and on Greater Antillean species compared to Lesser Antillean species (light and dark blue). This is perhaps unsurprising to many. We all know that anole research tends to be biased towards Caribbean species, but it was surprising to me how large this bias is!
This gives a sense of how much information is available for the species we highlighted in our tournament. For a few species, we were not even able to find photos (at least with appropriate usage rights) and for many the only information we could find was native range, color, and body size. For example, Anolis placidus had only five Google Scholar citations to go by, few images (other than specimens), and really no ecological information other than its ecomorph. But it must be named the “Placid Anole” for a reason, right? So we ran with that. Even with the paucity of information for some species, we were able to piece together some interesting stories highlighting some of the unique adaptations, ecology, and morphology. Here are some of my favorites with links for more information.
Anolis aquaticus and Anolis macrolepis were our two representative aquatic anoles. These species are adapted to streamside living, using the boulders as foraging grounds and for quick escape from predators–swimming, running across water, and even remaining submerged to get away from a threat! We used these behaviors in our stories–allowing both species to have sure footing in their stream side home and escape into the water when necessary.
Another unique anole we featured was Anolis onca, the only anole to have lost its toepads entirely. Anolis onca is adapted to a beachy life, making its home in sandy substrates and perching on bushes. We played this as a strength in round 1. It’s not clear what the functional reason for the loss of lamellae is–as has been suggested on Anole Annals, perhaps the sand renders lamellae or setae useless. The reasons for this morphological outlier are yet to be explored, but we figured A. onca must have an advantage in the sand over other anoles!
A crowd favorite from our tournament, but alas not the champion, was the only completely blue anole: Anolis gorgonae. This anole didn’t make it too far in our tournament because his bright blue body made him extremely visible on the forest floor. The blue may help camouflage them way up in the canopy, but it seems that down low they are visible against the green leaves from a distance. We wanted to root for him too, but how does something that visible not get eaten to extinction?
And finally, we made sure to feature a few of the anole kings: the crown giants. We know our readers here at Anole Annals love their giant anoles. These monsters of the canopy seem like they could beat out just about anything (or eat them!), and so it was in our tournament. In the end it was too tough to decide between the beloved Anolis equestris and the lesser-known giant of the mainland, Anolis frenatus. And so we enlisted the help of the mainland-island competition vs predation debate (reviewed in Losos 2009 – p.159) and had a monkey swoop in to help us decide (yes, this happens!). We wondered, could the predator-naive A. equestris establish itself in a land full of predators like the forests of South America? Despite being successful at invading Miami and some other Caribbean islands, it doesn’t seem to have established itself in South America… yet.
On behalf of all of the contributors to Anole March Madness 2016 we thank you for playing along with us. We hope to bring you another tournament next year, so let us know if you want to help make that happen!
I just got back from a trip to the Bahamas with Losos lab post-docs Anthony Geneva and Alexis Harrison, accompanied by expert lizard catchers Inbar Maayan and Sofia Prado-Irwin (Harvard graduate student). We parted ways for the first few days of the quick trip, with Anthony and Sofia headed to Bimini and Alexis, Inbar, and myself on Abaco. Read more about the Bimini trip in Sofia’s recent post.
Friends for the Environment Kenyon Center field station
On Abaco, we stayed at the brand new Friends of the Environment Kenyon Center. We were really impressed by the great accommodations of this field station. The station was sustainably built and had all the modern amenities we could wish for. The field lab was large and equipped with microscopes and plenty of counter space. We were equally impressed by the staff and their outreach efforts. The Friends for the Environment does a fantastic job providing nature education to local kids from age 3 through college! Their ambitious organization seeks to provide high-quality and low-cost facilities for visiting scientists and to provide outreach and education to the local community. We spoke with the coordinators of the organization who told us that any time researchers are looking for extra hands in the field they are happy to arrange local students to assist. We strongly encourage others traveling to Abaco to stay here!
“In the end we will conserve only what we love, we will love only what we understand, and we will understand only what we are taught.” – Baba Dioum (posted at the Friends for the Environment)
Our main goal on this trip was to capture Anolis sagrei to continue ongoing research into the amazing diversity among islands in this species. We were immediately struck by how much smaller the Anolissagrei on Abaco were compared to those on the other islands we have been to. I was also struck by how many A. sagrei used the ground. I normally study Anolis cristatellus, and although they are the same ecomorph, I rarely see A. cristatellus on the ground. I also don’t recall seeing A. sagrei frequently on the ground on Bimini or Eleuthera. So observing these lizards, particularly the females, on the ground at such a high frequency (they literally scattered as I walked!) was very surprising. Is this common on other islands with A. sagrei and I just haven’t noticed before?
As with any good field trip, we also encountered a great diversity of herps. Although the only native anole to Abaco is A. sagrei (according to Powell and Henderson 2012), we also saw plenty of Anolis distichus and a few Anolis smaragdinus. We also saw the invasive Cuban tree frog (Osteopilus septentrionalis), the native Eleutherodactylus planirostris, and plenty of curly-tails (Leiocephalus carinatus). No live snakes to report, although we did come across a couple of roadkill Cubophis.
Although we found no Sphaerodactylus, we did find plenty of non-native Hemidactylus. Interestingly, Hemidactylus is not listed in Powell and Henderson’s (2012) list of West Indian amphibians and reptiles for Abaco. Can anyone ID this species (the photos are of two individuals) and tell me if this has been reported before for Abaco? Obviously Hemidactylus are widespread in the Caribbean, but I was surprised to see it absent from the species list for many of the Bahamas islands.
If you missed the live Twitter broadcast of the final round, here it is: the conclusion of Anole March Madness 2016. In the final round, Anolis equestris represented the island anoles and Anolis frenatus represented the mainland anoles to answer the question every anole biologist ponders: are island anoles or mainland anoles superior?
Our (fictional) anole tournament is nearing its end. The two semi-final matches concluded leaving only two anoles remaining. Who will be the ultimate champion, an island anole or a mainland anole?
Here’s the recap of the Final Four:
Winner match 25 (Anolis aquaticus) versus winner match 26 (Anolis frenatus) In the rainforests of Columbia, Anolis aquaticus has ventured slightly out of his native range. Skittish from his previous streamside encounter with the giant Anolis insignis, he warily watches the canopy despite coming out on top in his last battle against Anolis limifrons. He is no stranger to Anolis frenatus, whose range extends north into Costa Rica, yet he fails to recognize the danger he is in as he climbs a tree towards a swarm of tasty insects. Out on a branch 10m up A. aquaticus gorges himself on the abundant food that tasted so much better than the streamside meals he was used to. Out of the corner of his eye, he sees the imposing form of Anolis frenatus move. More than twice his size, A. frenatus is a sight to behold. Anolis aquaticus quickly surveys his escape options. Seeing a stream below he rationalizes that he can escape if need be. He continues to gorge himself. Anolis frenatus is taken aback at the impertinence of this newcomer. He makes his way towards the branch upon which A. aquaticus is perched. Not willing to abandon his smorgasbord, A. aquaticus boldly stands his ground. He turns to face A. frenatus and begins to dewlap; perhaps this is a friendly giant that will want to avoid conflict. Anolis frenatus stops to size up this intruder and quickly determines that this tiny anole poses no threat to him. Anolis frenatus does not even bother to dewlap back. He continues on his path towards Anolis aquaticus, who stubbornly continues to dewlap and push-up in his cloud of tasty morsels. Anolis frenatus lunges at A. aquaticus, who instinctively turns and leaps without looking towards the stream. Anolis aquaticus sails through the air and lands safely in the water, or so he thinks. As he climbs onto a boulder, a fish-eating spider (Trechalea spp.) with a body size of nearly 17cm seizes the opportunity and leaps onto the unsuspecting and soggy anole. The spider makes quick work of the aquatic anole. Anolis frenatus watched from his high perch with a mouthful of delectable insects which he incidentally gobbled when he leapt at A. aquaticus with mouth agape. Anolis frenatus revels in his glory as he watches his competitor meet his end below. ***Anolis frenatus wins***
Winner match 27 (Anolis equestris) versus winner match 28 (Anolis bimaculatus) A hurricane of unprecedented proportions has just ripped through the Caribbean. The Cuban Knight Anole, Anolis equestris, and the Panther Anole, Anolis bimaculatus, both find themselves washed up on an unfamiliar low-lying island. The waves periodically break over the island, washing away the debris on the ground. Both lizards quickly find a perch and scramble to escape an incoming wave. As the reach safety atop their scrubby perches, they catchy sight of each other. Clearly this island refuge has room for only one of them. Two lizards enter, one lizard leaves on this subsiding volcanic dome. They lock eyes and begin to dewlap. Nearly evenly matched it’s not clear who will claim this island as his new home. Anolis equestris extends his dewlap first. He unleashes a flurry of push-ups and rapid flashes of his cream colored dewlap. The slightly smaller Anolis bimaculatus has no choice but to stand his ground. He strains to extend his orange-yellow dewlap as far as he can. Unfortunately, his species has a disproportionately small dewlap for their size, and this A. bimaculatus is average sized at best. Anolis equestris, completely and utterly unimpressed, leaps from bush to bush with waves breaking over the rocky ground below him as he heads towards A. bimaculatus. Anolis bimaculatus makes an offensive move and lunges at A. equestris, who has by now reached the neighboring bush. Anolis bimaculatus lands a calculated blow on the abdomen of A. equestris. Despite the searing pain in his kidney, A. equestris reaches around and snatches A. bimaculatus in his forceful jaws. In one quick motion, A. equestris flings the slightly smaller A. bimaculatus over his shoulder and off the perch. Anolis bimaculatus hits the rocky ground and begins to sprint toward the nearest bush. At this moment a large wave crashes over him and carries him off the low-lying island. Anolis bimaculatus scrambles onto a floating log, but is immediately caught in the outgoing rip and is carried far into open water within moments. Anolis equestris watches A. bimaculatus ride the waves out of his life and weathers the remainder of the storm safely on his elevated perch, alone. ***Anolis equestris wins***
Which brings us to our dramatic conclusion: Anolis frenatus, representing the mainland, versus Anolis equestris, representing the islands!
Here’s what you missed in the Elite 8 round: Anolis aquaticus proves he’s in it to win it when he battles Anolis limifrons; Anolis proboscis wonders what his proboscis is good for as he battles the giant Anolis frenatus; Anolis equestris shows Anolis porcus who the king of the jungle is; and the big-cat-lizards Anolis marmoratus (AKA Leopard Anole) and Anolis bimaculatus (AKA Panther Anole) face off. Continue reading Anole March Madness: Elite 8 reduced to Final 4!→