I am an Assistant Professor of Biology at New York University. My first love is herpetology, but my lab works on urban evolutionary ecology in diverse organisms (but primarily anoles!).
Which anole species will grace the pages of this year’s calendar?
Get ready for the Anole Annals Photo Contest: 2019 Edition.
Another year, another field season (or seasons) come and gone, and now it’s time to share the great anoles we’ve seen! As in previous years, the Anole Annals team wants to see your best anole photographs for our 2020 calendar.
Here’s how it works: anyone who wants to participate will submit their favorite photos. The editors of Anole Annals will choose a set of 30-40 finalists from that initial pool. We’ll then put those photos up for a vote on this here blog, and the 12 winning photos will be chose by readers of Anole Annals, as well as a panel of anole photography experts. The grand prize winner and runner-up will have his/her photo featured on the front cover of the 2020 Anole Annals calendar, second place winner will have his/her photo featured on the back cover, and they’ll both win a free calendar!
The Rules
Submit your photos (as many as you’d like) as email attachments to anoleannalsphotos@gmail.com. To make sure that your submissions arrive, please send an accompanying email without any attachments to confirm that we’ve received them. Photos must be at least 150 dpi and print to a size of 11 x 17 inches. If you are unsure how to resize your images, the simplest thing to do is to submit the raw image files produced by your digital camera (or if you must, a high quality scan of a printed image). If you elect to alter your own images, don’t forget that it’s always better to resize than to resample. Images with watermarks or other digital alterations that extend beyond color correction, sharpening and other basic editing will not be accepted. We are not going to deal with formal copyright law and ask only your permission to use your image for the calendar and related content on Anole Annals (more specifically, by submitting your photos, you are agreeing to allow us to use them in the calendar). We, in turn, agree that your images will never be used without attribution and that we will not profit financially from their use (the small amount of royalties we receive are used to purchase calendars for the winners). Please only submit photos you’ve taken yourself, not from other photographers–by submitting photos, you are declaring that you are the photographer and have the authority to allow the photograph to be used in the calendar if it is chosen.
Please provide a short description of the photo that includes: (1) the species name, (2) the location where the photo was taken, and (3) any other relevant information. Be sure to include your full name in your email as well. Deadline for submission is November 18, 2019.
Good luck, and we look forward to seeing your photos!
We all know that the anoles of the Caribbean partition the habitat based on structural environment and microclimate, leading to patterns of correlated morphology and habitat use within these ecomorphs. While we know a substantial amount about the morphological aspect of the ecomorph concept, many questions remain concerning the patterns of physiological trait evolution across Caribbean anoles and how this relates to habitat use and ecomorphology.
Brooke Bodensteiner, a PhD student in the Muñoz lab at Virginia Tech, is digging into this topic for her doctoral research. In her presentation at Evolution 2019, Brooke told us about two key questions she is attempting to address in her research: (1) Do ecomorphs overlap in physiological trait space or do they neatly differentiate into distinct groups as they do with morphology? and (2) Do thermal traits evolutionarily respond to the same microhabitat predictors?
Brooke measured thermal physiology of anoles in the Dominican Republic, including Anolis cybotes, shown here.
Brooke is investigating these questions in Hispaniolan anoles and has so far sampled 28 of the 41 species found in the Dominican Republic with representatives from all 6 ecomorphs! The Hispaniolan anoles are particularly good for this research topic since there are representatives of each ecomorph in very diverse habitats islandwide, providing many opportunities for physiological diversification. Building on a large dataset of morphological traits, Brooke collected thermal physiology data from all 28 of these species including critical thermal minimum and maximum and preferred temperature, to try to understand the patterns of physiological diversification and how they are correlated with morphological diversification.
Brooke’s results were fascinating, but more complex and nuanced than expected. Consequently, we will only tell you that her findings are intriguing and will give us a lot to ponder regarding patterns of correlated trait evolution and environmental factors driving physiological evolution. I look forward to seeing the finalized results published soon!
In the fall of 2017, Hurricane Maria ripped across the island of Puerto Rico leaving devastation and destruction in its wake. This caused major changes in the structural environment of forests with unknown consequences for the animals living in them. Kevin Aviles-Rodriguez, a PhD candidate at UMass Boston, wanted to know how the hurricane impacted Anolis cristatellus island wide. Specifically, Kevin was interested in knowing if lizard morphology was altered by the hurricane and how morphological changes differed in urban environments and as time passed post-hurricane.
Here on Anole Annals, we have talked a lot about hurricanes and anoles, most recently related to morphological shifts in Anolis scriptus following hurricane Irma in which Colin Donihue and colleagues observed morphological shifts in limb length and toepad size. Kevin wondered if the same shifts had occurred in A. cristatellus following hurricane Maria, but taking things one step further reasoned that since urban and forest environments differ in structural habitat, that morphological shifts following the hurricane might differ as well.
Hurricane Maria made landfall in the southeast of Puerto Rico and then traversed the island diagonally, causing widespread and lasting destruction.
Kevin resampled the same populations (which I had previously sampled in my own research) at 4 and 11 months post-hurricane. He found that immediately following the hurricane lizards in both urban and forest populations had relatively shorter forelimbs, relatively smaller toepads, and smaller body sizes compared to before the hurricane, and that this effect did not differ between urban and forest populations. These results were contrary to what Kevin expected since recent researchby Donihue et al. found that following hurricane Irma, A. scriptus had relatively longer forelimbs and larger toepads – traits that would increase gripping ability during high winds. Similar to Donihue, however, Kevin also found that the lizards had relatively shorter hindlimbs. As Donihue and colleagues elegantly demonstrated with their leaf-blower experiments, longer hindlimbs are disadvantageous during hurricanes because they increase the surface area exposed to the wind and act as sails, blowing the lizard more easily off the perch. Interestingly, within 1 year of the hurricane when Kevin again resampled these populations he found that all trait values had increased again to their pre-hurricane values in both urban and forest populations.
Kevin emphasized that the shift in trait means at each time point was small but significant. Importantly, the lack of difference between how forest and urban populations responded (both experienced decreases in mean trait values) suggests that despite structural habitat differences the hurricane imposed similar selective pressures in both habitat types. Kevin continues to dig into morphological variation of urban and forest populations post-hurricane and I look forward to seeing the published results!
Emmanuel D’Agostino presenting his undergraduate research at Evolution 2019.
Emmanuel D’Agostino, a (recently graduated) undergraduate in the Losos lab at Harvard presented his undergraduate thesis at Evolution 2019. Working with Colin Donihue, Anthony Geneva, and Jonathan Losos, Emmanuel analyzed genetics, morphology, and mating behavior of Anolis sagrei collected from across their Bahamian range. Anolis sagrei differ pretty drastically in ecomorphological and sexually selected traits on different islands throughout the Bahamas. Emmanuel wanted to find out if this differentiation created barriers to mating among divergent populations on different islands.
Emmanuel analyzed an impressive 184 videos of recently paired males and females from different islands under laboratory conditions. (Emmanuel informs me that there were actually 234 videos but many he could not score because of uncooperative lizards hiding behind the planters and out of view of the camera – who knows what they did back there!). He then quantified latency to mate to see if individuals from different islands would mate freely and if willingness to mate was related to morphological differences. He combined his video analysis with genomic and morphological data to understand how genetically and morphologically distinct populations are.
Emmanuel found that individuals from different populations mate freely, suggesting no effect of premating isolation related to morphological disparity. He also analyzed a large number of linear models to tease apart the relative contributions of genetics and morphology and found that the most important predictor of mating success was relative head size – males with smaller head sizes correlated with increased likelihood of mating success! Intriguingly, in his final analysis he found that males that mated the quickest had decreased offspring survival rates. So even though smaller-headed males may mate more readily, their offspring are less likely to survive.
It seems hard to believe almost a year has passed since the last Evolution meeting. Last year we brought you coverage of the anole talks and posters in Montpelier, France. This year, we’re coming to you live from Providence, Rhode Island from June 22nd – 25th! This year there are eight talks and eight posters scheduled *(searching the schedule for keywords “anole” and “Anolis“). There’s some pretty fascinating topics on the schedule – here’s what you have to look forward to each day:
Saturday:
Habitat use, competition, and phylogenetic history shape the evolution of claw morphology in Lesser Antillean anoles (Yuan, Jung, Wake, Wang)
The effects of volcanic activity on the phylogeographic history of the Plymouth Anole, Anolis lividus, on Montserrat (Poster board #72) (Jung, Yuan, Wang, Frederick)
Identification and assembly of an anole sex-chromosome: Rapid degeneration since autosomal fusion? (Poster board #160) (de Mello, Hime, Glor)
Effects of urbanization on toe pad shape and lamellae size in Anolis cristatellus (Poster board #174) (Howell, Hagey, Winchell)
Monday:
Using archival DNA to elucidate anole phylogeny (Mayer, Gamble)
Comparative landscape genetics and epigenetics of two trunk-ground anoles (Wang, Wogan, Yuan, Mahler)
Ancient hybridization in the adaptive radiation of Anolis lizards on Puerto Rico (Wogan, Yuan, Wang)
Urban adaptation in anole lizards of the Greater Antilles (Poster board #7) (Winchell)
Cities in the Spotlight: Does Tolerance of Artificial Light at Night Promote Urban Invasions? (Poster board #97) (Thawley, Kolbe)
Adaptive radiation in the multidimensional phenotype (Bodensteiner, Muñoz)
Patterns of morphological diversity in Draconura clade anole lizards (Huie, Prates, Bell, de Quieroz)
Did we miss any? If so, let us know in the comments so we can be sure to add it to our schedules! We will be live blogging the meeting as usual, so check back starting June 22nd to hear about the latest in anole evolutionary research. And if you are attending the meeting, consider blogging a talk or poster for us (new contributors welcome!). Just send me an email and I will fill you in on all you need to know.
Appearance: The crested anole, Anolis cristatellus, is a medium sized lizard (50-75mm SVL in adult males) with a stocky body and relatively long limbs. It is light brown in color and both males and females have varying patterns of dark brown on their backs including mottled coloration, hourglass patterns, and longitudinal stripes. As the common name implies, many individuals have a large tail crest (different from the nuchal crest that can be erected in many species), although there is substantial regional variation in this trait and many individuals have no tail fan at all. Dewlap color is typically two-toned with a yellow center and a thick orange outer edge, although some populations have a more monotone yellow-orange dewlap. Females are smaller than males (30-45mm SVL adults) and have relatively small dewlaps. Post-anal scales are not easily visible in this species, sometimes making it difficult to distinguish females from juvenile males.
Within the native range, this species may be confused with Anolis gundlachi and Anolis cooki. Anolis gundlachi can be distinguished from A. cristatellus by the yellow-tipped chin, blue eye, and solid yellow dewlap, but is otherwise similar in size and appearance. Anolis cooki is more difficult to distinguish from A. cristatellus, but the two only co-occur in the dry forests of southern Puerto Rico. In their non-native range in Florida, this species may be confused with Anolis sagrei, which is slightly smaller in size and has a dewlap that is red-orange in the center with a thin band of yellow on the edge.
A. cristatellus male with large tail crest (left) and without (right). Both are in head-down foraging position.
Ecology and Habitat: The crested anole is a trunk-ground ecomorph. It typically perches relatively low to the ground (around 2m high or lower) on broad diameter trees. It is often observed in foraging position on tree trunks with head downward as it sits and waits for insect prey to pass by on the ground. It typically eats insects and spiders, but is also known to consume fruits and to prey on small vertebrates, including anoles of their own and other species. This species is rarely seen on the ground except for when moving between perches or catching prey. Like other trunk-ground ecomorphs, A. cristatellus, has relatively long limbs and a stocky build ideal for quickly navigating both arboreal and ground habitat. Anolis cristatellus is commonly found at lower elevations in warm forest habitats and is often restricted to edge or open, disturbed forest habitat at cooler, high elevations. This species is the most common and abundant anole in urban areas in Puerto Rico.
Body size differences are the easiest way to differentiate adult female (left) and male (right) A. cristatellus. (Photo by Kristin Winchell)
Geographic Range and Biogeography: Anolis cristatellus is endemic to the Puerto Rican bank (Puerto Rico and the Virgin Islands). Its closest relative is A. desechensis, which is found only on the island of Desecheo off the west coast of Puerto Rico. It is also closely related to A. scriptus (found in the Turks and Caicos), A. cooki (found in dry forests in the southwest of Puerto Rico), and A. monensis (found on the island of Mona off the coast of Puerto Rico). Genetic analyses indicate that the ancestor to A. cristatellus (and 12 other Puerto Rican species, which make up the “cristatellus” group) likely colonized Puerto Rico from Hispaniola at least 40 MYA. More recently, A. cristatellus has established in several places outside of its native range, facilitated largely by sale of tropical plants. In particular, it is established in Miami (Florida), Dominica, Costa Rica, Mexico (Yucatan), Trinidad, Saint Martin, and the Dominican Republic.
Research Highlights:
Anolis cristatellus is a great study species for answering so many different questions! As the most wide-ranging Puerto Rican species, it is perfect for comparative studies. Researchers have found no end to the questions they can answer by examining variation within A. cristatellus in different environments and between A. cristatellus and other Puerto Rican species.
An urban A. cristatellus male perched on a metal fence in Puerto Rico. (Photo by Kristin Winchell)
Satellite imagery of when the lights went out in the brightest region of the Caribbean.
You have probably heard about the hurricane’s effect on humans: months of ensuing darkness, destroyed roads, houses leveled and roofs torn clean off, no fresh water, and significantly crippled infrastructure and public services leading to over 1,000 lives lost when it all was over.
I’ve been back to the island now twice since the hurricane, once in January of 2018 and once last week (November 2018).
Four months post-hurricane
The destruction to both urban and forest areas was jaw-dropping when I visited in January to help Kevin Aviles-Rodriguez (UMass Boston) launch a project on urban lizard recovery and natural selection following hurricanes. (Side note – this research has yielded some really intriguing results so far and I look forward to Kevin sharing those with us here at Anole Annals in the future!) On that trip, four months after the hurricane, I found the island in disrepair. Many people still had no power or clean water, stoplights and electrical lines dangled from their snapped poles island-wide, roofs were covered in blue tarps, and driving involved dodging car-eating potholes, downed power lines, and debris. Most stores and restaurants were closed and many roads were impassable.
A stand of trees on the west coast four months post-hurricane (near Rincón).
The trees left standing in urban areas were bare toothpicks. I’m told that immediately following the hurricane, the leaves looked like green snow coating the ground several inches thick. Most of the trees that survived were the large and common urban species: mango, flamboyán, ceiba–leafless but still rooted. When we visited the forests I was equally shocked by the destruction: trees looked as if someone clipped them all off clean around 15 feet up, the canopy was gone and all of the large trees like Cecropia and Cocoloba were downed. Lianas had taken over giving the forests a bushy, surreal appearance. I left the island that January wondering how long it would take to recover; the human side and nature side alike had a long road ahead of them.
What was once closed-canopy secondary forest on the north coast (near Arecibo).
Fourteen months post-hurricane
When I returned last week, now 14 months post-hurricane, I was pleasantly surprised to see the island was recovering. Roads had been repaired, power had been restored, stoplights were working, debris had been cleared, restaurants and stores were open, and houses rebuilt. From the human side of things, the island seemed to be recovering. On the west side of the island, the leaves of the large trees had returned. Forested areas had more dense understory than typical and the canopy was still fairly open, but overall it seemed like the forests and urban areas were both returning to normalcy. I found many urban lizards without a problem, including Anolis cristatellus, A. pulchellus, A. stratulus, Ameiva exsul and the non-native green iguana. I was surprised however, that the nights were eerily quiet. The familiar ear piercing chorus of coqui was reduced to intermittent calls of only a few individuals. The coqui don’t seem to have recovered quite as well as the anoles.
No trees? This urban A. cristatellus seems okay with that.
Anolis cristatellus
Anolis pulchellus
Many challenges certainly still face the residents of the island, but it was starting to look more like the Puerto Rico I knew. So it was quite a shock when I visited the newly re-opened El Yunque National Park. El Yunque was hit particularly hard by the hurricane as the first landfall was just south of the forest near Yabucoa. Strong bands of wind pummeled the area, leading to massive landslides that closed the rainforest for months. The national park website said that only La Coca falls and Yokahu Tower were open to visitors, but I found a park ranger who informed me that the Mt. Britton trail was open (and the road to the peak of El Yunque had been cleared as well, though not the cloud forest trail).
As I drove up the mountainside to the Mt. Britton trailhead I was shocked at how open the forest was. When we arrived at the trailhead, my jaw dropped. The canopy had not recovered at all. The palms seemed to be the only trees that survived. I’ve hiked this trail many times, but this was the first time I did not wear a long-sleeve shirt – it was hot and dry. Perhaps the lack of animals shouldn’t have come as a surprise then. I didn’t hear a single coqui call while hiking the trail, where in the past we would hear many different species along the route. I also did not see a single Anolis gundlachi, where before my favorite trick was to tell someone that I could make lizards appear on demand then reach out and snatch one off a tree – they were that common! I did see a handful of Anolis evermanni, but only a few. Below are a couple of before and after photos of the same portions of the trail.
Mt. Britton trail in January 2017
Mt. Britton trail now, 14 months post hurricane
The entrance to the Mt. Britton trail before the hurricane…
and the same location 14 months after the hurricane
The impacts of hurricanes on wildlife
Recent research has shown that the insect populations of El Yunque have been declining for years, and certainly hurricane Maria did not help this situation. Perhaps the anole and coqui populations have suffered because of a collapse of food resources? Or perhaps the microclimatic shifts were too much for the lizards to handle? Anolis gundlachi does have a strong affinity for cool and moist habitats and it seems quite likely that with the current state of El Yunque, very little suitable climatic habitat exists for this species. Or perhaps the hurricane itself reduced the anole populations. Recent research on Anolis scriptus found that hurricanes can pose strong selective pressures leading to phenotypic change. Whatever the reason for the apparent decline, I am eager to check back in with the lizards in a few months when I visit again and even more eager to hear about the research of those studying herpetofaunal hurricane recovery.
No A. gundlachi to be found at El Yunque 14 months after the hurricane, but quite a few A. evermanni like the one seen here.
Are you studying the effects of hurricanes on lizards? Are you studying the recovery of Puerto Rican herpetofauna after Maria? We would love to hear more about it! Let us know in the comments, or consider contributing a blog post to Anole Annals.
“Squamates Playing Poker” – a clever depiction of sex chromosome evolution (image by Anna Minkina shared with permission from Tony Gamble; read more about the image on the Gamble lab website)
Anole Annals contributor Yann Bourgeois reports on the talk by Tony Gamble on sex chromosome evolution. While this talk wasn’t specifically about anoles, our favorite lizards are no stranger to this topic, as discussed previously here on Anole Annals. Gamble builds on his previous work in an impressive analysis of sex chromosome evolution across squamates and snakes. We can look past the anoles taking the back-seat on this one because the talk was fascinating and sure to be of interest to readers here. Yann Bourgeois reports:
How sex chromosomes originate is one of the most intriguing questions of evolutionary biology. It is also a complex one, as the mechanisms that lead to their formation are not clearly understood and our knowledge is mostly based on model species that are not necessarily representative (most of them have strongly heteromorphic sex chromosomes). It is generally thought that sex chromosomes emerge as new alleles at a sex-determining gene stop recombining with each other. Since sex-ratio has to reach an equilibrium, balancing selection maintains the two alleles at high frequencies, and strong linkage locks together loci involved in reproductive isolation and mating. As the two non-recombining blocks diverge they accumulate mutations that can be used to discriminate them using molecular tools. In the most extreme case, one of the two chromosomes degenerates, such as the Y chromosome in humans.
Most sex-determining systems fall into two categories: ZW systems where the male is homozygous ZZ and females are heterozygous, and the classical XY system with XY males and XX females. We know from previous research that anoles fall into the XX/XY category (although some species are XXXX/XXY). However, in general in squamates and snakes in particular, the evolution of sex-chromosomes is poorly known. Early studies mostly focused on heteromorphic chromosomes, which are so divergent that they can easily be identified through cytogenetics. But heteromorphic sex chromosomes like those in anoles and other squamates are not necessarily visible, and other tools are needed to identify which system occurs in a given species.
In his talk, Gamble showed how to use RAD-seq or RNA-seq to identify loci associated with sex, and to discriminate between XY and ZW systems (for more information on this approach, check out his 2015 paper in Molecular Biology and Evolution). For example, in an XX system, all males will be heterozygous at sex-linked loci while all females will be homozygous at the same sites. Depth of coverage will also be twice as low at X-linked loci for males than for females as they harbor a single X chromosome. Using this set of molecular methods, Tony demonstrates that there is a high turn-over of sex-determining systems in squamates and snakes, with more than 40 transitions between ZW and XY, half of those transitions being found in geckos.
It is also possible to map those sex-associated loci to reference genomes to identify syntenic blocks that may be repeatedly recruited during sex-chromosome evolution. For example, in the crested gecko (Correlophus ciliatus), most sex-associated loci map on chicken’s chromosome 10. Some genes may have a higher likelihood to be recruited when a new sex chromosome appears, but whether this can be extended to specific syntenic blocks remains an open question. This is made even more difficult by the fact that sex-determining genes in squamates are not yet known with certainty. This ongoing work on macro-evolutionary dynamics of sex chromosomes will provide interesting findings that may be linked to the evolution of mating strategies and speciation in anoles.
Whole genome sequencing approaches are rapidly becoming more accessible and gaining popularity. The development of powerful analytical tools for these data has enabled novel approaches to answering outstanding evolutionary questions. Yann Bourgeois, a post-doc at NYU- Abu Dhabi, is the first to take a whole genome approach to understand the population genomics of Anolis carolinensis in the southeastern United States. Yann presented his work in a poster at Evolution 2018 in Montpellier.
Yann sequenced 27 individuals from across the native range representing the five unique genetic clusters (Gulf Atlantic, Carolinas, North Eastern Florida, North Western Florida, South Florida). He found that the Gulf Atlantic and Carolina populations were nested within the Florida populations, supporting the hypothesis of a northward expansion from southern Florida. He was able to estimate that this colonization of regions north of Florida likely occurred in the past 100,000 years. Interestingly, he also found that this dispersal event was associated with a reduction in X chromosome diversity, suggesting that dispersal was either male biased or that there has been positive selection on the X chromosome.
Whole genome sequencing of 27 individuals from across the native range reveals population genetic structure
Taking this one step further, Yann then investigated patterns of recombination via secondary contact among the genetic clusters. Yann and his colleagues found that there has been gene flow between clusters over periods of secondary contact with interspersed periods of isolation. Limited introgression between Florida and the northern populations suggests local adaptation in the northern populations.
Yann and his colleagues have provided an interesting first look at the evolutionary history of Anolis carolinensis from a genomic perspective. The revealed patterns of expansion, reduced diversity, isolation, and secondary contact raise interesting questions about the origin of new genetic clusters (and perhaps species) and their maintenance with ongoing or periodic gene flow.
Evolution 2018 may have been a week and a half ago, but the fun doesn’t have to stop just yet. Shane Campbell-Staton reports on the talk by Guin Wogan:
As we all know by now, contemporary climate change is expected to cause problems for species across the globe. Understanding the mechanisms that will allow species to cope with these changes, through acclimation and/or adaptation, is one of the most pressing issues of contemporary biology. Reptiles, and lizards in particular, have been a model for studying the effects of climate on extinction, gene flow, performance, and adaptation. Yet, only recently have we really begun to understand the genetic mechanisms associated with survival and persistence in the face of changing environments. In this year’s Epigenetics and Adaptation session of the Evolution Meeting, Guinevere Wogan – a postdoctoral researcher in Ian Wang’s Lab at UC Berkeley – presented a first look at how variation in the epigenome correlates with climate variation with and between anole species.
Wogan et al. used reduced representation bisulphite sequencing to search for epigenomic associations with environment in two wide ranging species – Anolis cristatellus on Puerto Rico and Anolis cybotes on Hispaniola – both species that occur in a wide variety of habitats from cool, wet forests to dry, arid scrubland. They found some indication of convergent methylation profiles under similar climates within species, suggesting epigenetic signals may be important for acclimation and/or adaptation to local climate. However, this association was not perfect potentially due to habitat use differences between populations. Additionally, they found that variation in climate between populations explains a large degree of variation in methylation profiles between popualtions within each species (75.6% in A. cristatellus and 39.1% in A. cybotes), again suggesting an important role of epigenetic modification in contributing to survival in local environments. However, local climate isn’t the only factor effecting variation in epigenetic modification; they also found strong species level differences in methylation, even when populations occurred in similar environments.
As they continue to work on this study, it will be very exciting to see what further patterns emerge. As we collectively seek to better understand the mechanisms involved in environmental adaptation and acclimation, Wogan et al. are exploring an extremely understudied aspect of Anolis biology that is bound to shed valuable light on the subject. I’ll certainly be on the lookout for this manuscript in the near future.
