Anole Annals

Photo credit: Rayna Bell

We all know the story of the anole ecomorphs of the Greater Antilles, but to what extent does this pattern extend to the mainland? Does the mainland perhaps harbor unrecognized ecomorphs not found in the Greater Antilles? The Draconura clade on the mainland is most likely descended from a West Indian ancestor after all. Unfortunately, we currently have a much shallower understanding of the ecology of mainland anoles. Jonathan Huie, an undergraduate student at the University of Washington and former REU student with Dr. Kevin de Queiroz at the Smithsonian’s National Museum of Natural History, presented on his efforts to tackle these questions. Despite some unforeseen technical difficulties, Huie persevered and delivered an excellent talk!

Huie and colleagues utilized the concepts of convergent morphology as a first step to examine this question in the Draconura clade of mainland anoles. They compared various levels of stringency in classification algorithms to examine if mainland Draconura species could be assigned to Greater Antillean ecomorphs or potentially undescribed new ecomorphs. They found that Draconura anoles showed extensive morphological variation, although no species clustered with the more highly derived Greater Antillean ecomorphs such as the twig anoles. Several mainland species could be assigned to existing ecomorphs. However, many species remained unclassified using all classification methods.

Next, Huie discussed evidence for potential unrecognized ecomorphs among unclassified species. Specifically, he proposes a potential “ground” (or “leaf-litter”) associated ecomorph among Draconura anoles which was characterized by relatively longer hindlimbs and narrower toepads. This potential new ecomorph is likely even present in the Greater Antilles. Hispaniola’s own leaf-litter specialist, Anolis barbouri, clusters morphologically with mainland leaf-litter specialists. Huie et al.’s work demonstrates the potentially underappreciated applicability of the ecomorph concept to the diversity of mainland anoles and may have even uncovered a new ecomorph!

Anolis planiceps, a member of the new proposed “ground” ecomorph. Photo credit: Ivan Prates

Evolution 2019: Urban Lizard Morphology Shifted Post-Hurricane Maria

By kmwinchell

On June 26, 2019

In New Research

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 research by 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!

Evolution 2019: What Shapes the Shape of Lesser Antillean Anole Claws?

By Brooke Bodensteiner

On June 25, 2019

In New Research

Organismal performance frequently depends on multiple phenotypic traits in the context of the environments these organisms inhabit. Earlier this year, we saw the study by Yuan and colleagues examining the integration of claw and toe pad morphological evolution related to structural habitat partitioning of the Greater Antillean anoles. At Evolution 2019, Michael Yuan, a PhD student in Dr. Marvalee Wake’s Lab at U.C. Berkeley, presented work delving into the next steps of this line of questioning investigating the morphological evolution of claw and toe pad morphological evolution in Lesser Antillean anoles.

Do the patterns of claw and toepad evolution found on the Greater Antilles hold for the divergent lineages found in the Lesser Antilles?

Yuan collected data characterizing toe pad width; lamella number; claw height, length and width and claw geometric morphometric data on species found in the Lesser Antilles. He found that the total variation in claw and toe pad morphology was similar between the Lesser Antillean and Greater Antillean anoles. To potentially explain this variation, he explored environmental variables, seeking to explain if macrohabitat is associated with claw and toe pad morphology. He found that on single species islands, there was a strong relationship between habitat and toe curvature, leading to a pattern between macrohabitat and claw shape that is disrupted by competitive interactions on the two-species islands. To investigate microhabitat as a potential predictor of this variation, he asked if claw and toe pad traits are correlated with perch height. Unlike his study in the GA anoles, he found no relationship between claw and toe morphology and perch height, unless it was broken down by series. Functional traits are predictably correlated with vertical habitat in the bimaculatus series (anoles that colonized the Lesser Antilles from the Greater Antilles), but not in the roquet series (anoles that colonized the lesser Antilles from mainland South America).

Evolution 2019: On the Origin of Anolis Sex Chromosomes

By Pavitra Muralidhar

On June 25, 2019

In All Posts, New Research

The origin and maintenance of reproductive isolation between species is a central question to evolutionary biologists. Divergent sex chromosomes can play an important role in this process, and are generally assumed to have outsized importance in the establishment of reproductive barriers. Studying the origin and evolution of sex chromosomes – and their respective fusions and fissions – may therefore provide key insights into their role in these processes.

Anole are known to vary in sex chromosome size and content, although all anoles are male heterogametic. In a poster at Evolution, de Mello et al. investigate the neo-sex chromosomes of Anolis distichus, one of the “model anoles” of speciation research. Starting from a newly assembled genome, these researchers used differences in coverage, k-mer comparisons, and synteny mapping to the Anolis carolinensis genome, to identify the sex-linked genomic regions of A. distichus.

From these results, de Mello et al. were able to identify deep conservation of the X chromosome between A. distichus and A. carolinensis – implying an ancient origin of a shared anole X chromosome. They also identified explicitly Y-linked scaffolds for the first time in any Anolis species, which will prove useful for future work on the evolution of these sex chromosomes. However, perhaps most excitingly, de Mello et al. identified a chromosome fusion of the Anolis carolinensis microchromosomes 11 and 12 to the A. distichus X chromosome. In other words, the A. distichus X chromosome has expanded through the fusion of these two microchromosomes.

de Mello et al.’s result that the A. distichus sex chromosomes are simultaneously ancient and newly expanding provides a fascinating look at the dynamic lives of these sex chromosomes. Future investigations into the evolution of Anolis sex chromosomes will surely prove fruitful to understanding their role in the diversification of the Anolis lineages.

Evolution 2019: How Do Anoles Handle Artificial Light at Night?

By edagostino

On June 25, 2019

In New Research

At the 2019 Evolution Meetings thus far, we’ve seen some excellent work on anoles’ interaction with, and adaptation to, our changing world. Vincent Farrallo gave a talk on modeling the (surprising) effects on climate change on anole species, and Bailey Howell presented a poster on how Anolis cristatellus‘ toepads differ in shape and size between urban and non-urban environments.

In Monday’s poster session, Chris Thawley, a postdoctoral fellow in Jason Kolbe’s lab at the University of Rhode Island who will be teaching at Davidson College in the fall, gave a great contribution to this body of presentations at the meeting. His poster, “Cities in the spotlight: Does tolerance of artificial light at night promote urban invasions?”, showed his detailed work on this “evolutionarily novel condition.” He predicted artificial light at night, or ALAN, would be a double-edged sword for anoles. On the one hand, it perturbs sleep and endocrine cycles, makes it easier to for predators to find an anole late-night snack, and may negatively impact reproduction. It might not necessarily be all negative, however, as it could make it easier for anoles to find food and mates and protect territories.

Chris found significant effects of ALAN on reproductive habits: anoles exposed to ALAN start to lay eggs earlier and lay more eggs than anoles facing natural lighting conditions. Further, ALAN increases anole growth! Interestingly enough, however, Chris found that anoles have no real preference between ALAN and natural lighting conditions, and don’t appear to be more or less stressed under ALAN. In addition to this work with live anoles, Chris searched the literature to see if there’s an overlap between anole species that are invasive and those that have been reported to take advantage of ALAN. There is indeed such an overlap — 7 species are invasive but aren’t known to use ALAN and 8 non-invasive species use ALAN, but there are 15 invasive ALAN-using anole species!

Chris’s next questions involve the effect of ALAN on other taxa, as well as whether urbanizing anole species have adaptations that make them predisposed to take advantage of ALAN and what the effects of plasticity are in doing so. Given the prevalence of artificial light at night, and our love of Anolis, it should prove really exciting to learn more about the interaction between the two!

Evolution 2019: Can Archival DNA Illuminate A. roosevelti’s Evolutionary History?

By Chris Thawley

On June 24, 2019

In New Research

Resolving how extinct species are related to extant ones is often a challenge, as we may not possess the right information, especially genetic data, needed to understand how these species evolved from others. Recently, scientists have increasingly employed archival DNA, or DNA taken from preserved specimens such as those in natural history collections, to understand the evolution of extinct species, including the quagga and thylacine among others.

Thylacines (Thylacinus cynocephalus) in the National Zoo, Washington D.C. (Smithsonian Institute).

Fortunately, to our best knowledge, only one species of anole is suspected to have become extinct in historical times, Anolis roosevelti, the presumed crown giant anole of the eastern Puerto Rico Bank, where it was found on Vieques, Culebra, St. John, and Tortola. Something of a holy grail for anolologists, many researchers have done their best Indiana Jones and taken a crack at finding living A. roosevelti, including some truly heroic fieldwork.

Puerto Rico and the Virgin Islands, with the known distribution of Anolis
roosevelti (stars). From west to east: Vieques, Culebra, St. John, and Tortola. From Mayer and Gamble 2019.

Despite these efforts, no live individuals have been found. Only six specimens of A. roosevelti are known to exist and thus are precious records of this presumably lost species. Previous work has used quantitative characters to attempt to resolve the placement of A. roosevelti in the anole phylogeny, but genetic data is the gold standard for describing evolutionary relationships. Could archival DNA from these specimens, preserved at museums across the world, resolve how A. roosevelti is related to extant species?

MCZ 36138, the holotype of Anolis roosevelti. Laszlo Meszoly, del. From Mayer and Gamble 2019.

Greg Mayer at University of Wisconsin-Parkside and Tony Gamble at Marquette University have embarked on their own quest to answer this question. First, Greg tracked down all six known specimens of A. roosevelti. He determined that they have all been preserved in ethanol, rather than formalin, indicating a reasonable chance of obtaining DNA from these individuals. Because the roosevelti specimens are so precious, Greg and Tony worked to generate a proof of concept for the use of archival DNA sequencing on them. They extracted DNA from specimens of the common crested anole (Anolis cristatellus) preserved using the same methods by the same collectors and at the same times and general locations.

One of the six extant specimens of A. roosevelti (ZMUK 37642, Vieques, A.H. Riise; photo by Mogens Andersen).

They were able to successfully extract and sequence at least partial mitogenomes from 5 of 8 historical samples, including some preserved as far back as 1861! The sequences from these archival specimens clustered with those collected contemporaneously from similar localities. These results indicate that the sequencing of archival DNA provides quality data and that similar procedures are likely to be effective in A. roosevelti specimens.

Greg and Tony’s next step is to obtain tissue from these important specimens, sequence their mitogenomes, and add to our knowledge of this presumably extinct species. Stay tuned for their findings!

For more info, check out the article in Anolis Newsletter VII:

Mayer, G. C. and T. Gamble. 2019. Using archival DNA to elucidate anole phylogeny. Anolis Newsletter VII, p. 158-168. Eds. Stroud, J.T., Geneva, A.J., Losos, J.B. Washington University, St. Louis MO.

Evolution 2019: How Does Urbanization Affect Toepad Shape and Size in Anolis cristatellus?

By edagostino

On June 24, 2019

In New Research

Bailey Howell, a rising senior in Travis Hagey‘s lab at Mississippi University for Women, presented a poster at Evolution on differences in toepad morphology between urban and non-urban populations of Anolis cristatellus. The two of them coauthored the work with Kristin Winchell, who has been investigating morphological effects of urbanization in that species, and who captured A. cristatellus for the study. Bailey mapped their toepad landmarks and quantified a suite of toepad traits, including length and width, in a whopping 160 of them! She did this to investigate differences between individuals from urban and non-urban sites, with the goal of contributing to our understanding of the species’ adaptation to cities.

She ran some neat statistics for the project: first, a principal component analysis of all toepads scanned, which found differences in the degree to which urban and non-urban toepads are bent. She went one step further by running a canonical variate analysis to find which factors are maximally different between the urban and non-urban lizards. A scaled (pun unintended) figure from her poster of the theoretical most-urban and most-non-urban toepads is below (urban is in gray, non-urban is in green).

This CVA explained significant variation between the two populations, and accounted for 14.5% of the difference! Taking things a step further, Bailey analyzed size as well as shape from the traits she measured, and saw that urban toepads were wider, and, in particular, longer, than non-urban ones. Next steps for the project include adding more toepads to the dataset, analyzing the data in light of more (toepad and non-toepad) traits in these individuals, and looking for an effect on performance. It seems like they’re well on their way to understanding this important effect of urbanization in this species!

Evolution 2019: Morphologically Distinct Populations of Anolis sagrei Have No Issues Interbreeding

By kmwinchell

On June 23, 2019

In New Research

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.

Evolution 2019: How Many Species of Anolis distichus?

By Travis Hagey

On June 23, 2019

In All Posts

Anolis distichus is a highly variable species from Hispaniola. It’s especially variable in its dewlap color, ranging from white, to orange, to red. In the past, A. distichus has been broken up into 16 subspecies based on its dewlap variation! Previous work by Rich Glor and his students used genetic data to identify six candidate species, although these six candidate species didn’t correspond well with the 16 dewlap-based subspecies. In order to get a better handle on how justified these candidate species are, undergraduate Tanner Myers, working with Pietro Longo Hollanda de Mello and Rich Glor, from the University of Kansas, presented a poster titled Identifying species when boundaries are blurred.

Myers collected morphological data from populations of A. distichus from across Hispaniola. The authors expected their morphological data to also partition along with the previously identified genetic candidate species. They found this to not be the case! When the authors looked at their morphological data (linear body, limb, and head measurements), to see if these 6 candidate species had any morphological divergence, they found no strong pattern. All of the candidate species clustered together to support one morphological group. In the end, the authors suggest that Anolis distichus may represent a highly variable group in in the early stages of speciation, but at this point, they do not support any taxonomic revisions of the species.

Tanner Myers will be starting graduate school with Jamie Oaks at Auburn University in the fall.

Evolution 2019: How Should We Predict the Impacts of Climate Change on Anoles?

By Chris Thawley

On June 23, 2019

In New Research

Climate change on earth is accelerating. These changes will have important impacts on all species, but some types of organisms are predicted to be affected more strongly than others. One such group is ectotherms which use the temperatures available in surrounding habitats to regulate their body temperatures. Another such group is mountaintop endemics. These species are restricted to one or several mountain peaks by climate and/or competition with other organisms. As such, they cannot easily disperse to other areas if climate makes their current habitat unsuitable!

Mountaintop endemic species may be particularly vulnerable to climate change (Chand Alli, CC BY SA).

Predicting how climate change will impact ectotherms and montane endemics has become a proverbial “hot topic” in recent ecological work, with studies focusing on lizards, salamanders, plants, and insects among other taxa.

Hispaniola contains several high elevation areas home to mountaintop endemic species, including anoles (NASA).

Many studies use correlative modeling approaches (often termed ecological niche models [ENMs] or species distribution models [SDMs]) to assess a species’ current distribution and predict its future distribution by projecting it into simulated future climate scenarios. This approach has some advantages including ease of implementation across many species. However, it has at least two potential drawbacks: the environmental data used in building such models are often measured at a fairly coarse scale that does not represent how many organisms use their environments, and the models do not explicitly include biological processes such as physiology and behavior.

Anolis armouri in a montane rock meadow (Reptile Database).

Vincent Farallo, a post doc at Virginia Tech, and his advisor, Martha Muñoz (both moving to Yale in a few weeks!), investigated whether incorporating physiology and behavior into modelling might affect predictions of climate change impacts on two mountaintop endemic anoles of Hispaniola, Anolis armouri and Anolis shrevei. Correlative SDMs (via BioMod2) predicted both species would lose much or all of their suitable habitat under climate change, perhaps leading to extinction. However, when Vincent constructed mechanistic niche models (via NicheMapR) that included knowledge about the thermal physiology and habitat use behavior of these species to predict activity time, they showed that habitat would increase in suitability under climate change, the opposite result! Interestingly, these models also predicted increased suitability for a widespread anole, A. cybotes. This result suggests that while climatic changes may not be a direct threat to these mountaintop anoles, increased competition with another anole, an indirect impact of climate change, may be.

Activity time of Anolis shrevei is predicted to increase across its range in Hispaniola with climate change (Farallo and Munoz).

As a whole, Vincent and Martha’s work shows that incorporating more mechanistic knowledge into models, including physiology and behavior, may be critical to predicting the impacts of climate change on organisms and making sound conservation decisions.