There have been lots of posts on the many great anole papers and posters at Evolution 2019, but here are a few of the non-scientific anole-related items from the meetings. First, a group of anolologists gathered at Trattoria Zooma on Federal Hill for lunch, where we feasted on Neapolitan specialties. Thanks to Nick Herrmann for picking the restaurant!
Anolologists gathered at Trattoria Zooma on Federal Hill, Providence, RI, for lunch on 24 June 2019.
And, a closer look at Kristin Winchell’s absolutely fabulous Anolis lineatopus dress, which has already been noted.
Kristin also produced a set of attractive anole (pus one boa) stickers, which she was handing out during her poster session.
And finally, huge props to Jonathan Huie. He gave a nice talk on the ecomorphology of mainland anoles, but what I want to highlight here is that he did so under the most dire circumstances: not just afternoon of the last day, but his slides wouldn’t project! The modern equivalent of the old overturned slide carousel, Jonathan handled the absence of his visuals with aplomb, calmly opening his talk and introducing his topic before an empty screen, as technicians scurried to resuscitate the projection system.
When it seemed that the technicians would fail, I decided to document Jonathan’s admirable handling of the situation, but as I brought out and readied my camera, the slides finally appeared, so the photo below shows Jonathan with one of his slides. (Note the technician still at the podium, and that’s Ivan Prates and Kevin de Queiroz in the slide with Jonathan.) It was 5 minutes into his talk before the slides worked– an eternity for a 12 minute talk with 2 minutes for questions. Jonathan’s an undergraduate, but dealt with adversity like a pro!
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!
Dewlap variation in A. fuscoauratus. Photos by Ivan Prates.
One of the most well-known and “classic” anole traits is the dewlap, the (usually) colorful flap of skin under the chin that anoles use to display to one another. The dewlap plays a role in numerous anole interactions, including male-male and male-female displays of aggression or courtship. Throughout the Anolis genus, dewlap color and pattern are both quite variable. Dewlap color is thought to be a sign of reproductive isolation, and has been used by researchers to define and recognize species boundaries, although lots of variation within-species exists as well.
Ivan Prates, a postdoctoral fellow at the Smithsonian National Museum of Natural History, has been exploring this variation with the curious case of the Amazonian slender anole, A. fuscoauratus. The species is distributed throughout much of the Amazon, and different populations vary in dewlap color – some are white, some are yellow, and some are pink! Within each population, the dewlaps don’t appear to vary, but different populations have different dewlap colors, seemingly unpredictably. For example, two study populations that are separated by just 60km show different dewlap morphs, with one population having all yellow dewlaps, and the other having all pink. (Note: only males have dewlaps in this species).
This observation led Prates to two questions: first, does the phenotypic variation represent distinct evolutionary lineages? That is to say, are populations with the same colored dewlap more closely related to one another than to populations with different colored dewlaps? And second, what is driving the diversity in dewlap color?
To answer the first question, Prates performed RAD sequencing on a large number of populations throughout the range of A. fuscoauratus. Prates found a fair amount of genetics structure within the species, and identified areas that have experienced high levels of admixture as well. For example, the Atlantic Forest population and northern South American were genetically distinct, but populations within central Amazonia tend to be relatively admixed with one another. Interestingly, he found that this genetic structure of populations was not related to dewlap color at all. Populations with different dewlap colors were present within each of the distinct genetic clades. So each of the dewlap colors did not come from a single source population, and have instead diverged from one another seemingly at random.
So if the genetic structure does not predict the dewlap color phenotype, what does? Previous work on Greater Antillean anoles has shown that dewlap color and pattern vary across habitat types due to differences in light environment and visibility. Denser habitats are thought to lead to more reflective colors and patterns, while more open habitats lead to less reflective dewlaps. Prates therefore used climate data to assess whether environmental variables were correlated with dewlap color. Similar to the genetic results, Prates found no association between climate variables and dewlap color.
What about species interactions? Previous work has also shown that dewlaps can function as inter-species recognition signals. It is expected that anole species that overlap with one another should have distinct dewlaps, in order to efficiently recognize conspecifics in multi-species communities. Prates addressed this hypothesis by examining the dewlaps of other species of anoles that are sympatric with A. fuscoauratus, and assessing whether dewlap variation might correlate with Anolis community composition. Prates found limited evidence for this hypothesis – for example, in areas where it co-occurs with A. tandai, a blue-dewlapped anole, A. fuscoauratus has a fewer gray-dewlapped populations, which are more similar to blue than the yellow or pink morphs. However, Prates also found that even in sympatry with other yellow-dewlapped species, A. fuscoauratus does not have a reduction in yellow- or white-dewlapped populations.
So what is driving this dewlap diversity? So far, there’s no smoking gun, but a few suggestions come from the data. Prates plans to continue working on this question by digging deeper on both genetic and environmental scales. Stay tuned!
The field of landscape genetics seeks to understand how patterns of genetic diversity vary across a landscape. But an organism’s traits are not just determined by their genome – they are also impacted by processes that affect the way the genome is expressed. The study of such mechanisms (i.e. heritable non-genetically based gene expression) is known as epigenetics, and has become a topic of great interested to evolutionary biologists who aim to understand the processes by which phenotypes change over time and space. Non-genetically based phenotypes can be the targets of selection, can impact the plasticity of traits in different environments, and more.
Understanding the impact of epigenetics on evolutionary processes is difficult, because it is hard to disentangle the genetic and epigenetic effects on phenotypes. Of course, epigenetics are not independent from the underlying genetic code – the genes that are expressed are a part of the genome after all. Thus because populations differ in genetic structure, it is difficult to determine whether differences in phenotypes across populations are driven by genetic changes, or epigenetic changes. To understand the influence of epigenetic changes on phenotypes, it is necessary to “subtract” the effects of the underlying genetic variation.
Ian Wang decided to tackle this problem using a well-studied Anolis species, A. cristatellus. Wang is interested in understanding what factors drive epigenetic patterns; but before understanding the factors involved, it is first necessary to describe the patterns. Wang chose to focus on A. cristatellus because it is distributed widely and throughout various environments on the island of Puerto Rico, and is therefore a good candidate for understanding how populations diverge across geographic regions (i.e. isolation by distance) and in different habitats (i.e. isolation by environment).
Wang and colleagues collected tissues from 8 localities, some of which were located in the xeric southwest, and some of which were located in the mesic interior. He performed RRBS sequencing, which captures information about methylated regions of DNA, and therefore provides information on variation in gene expression across populations (i.e. epigenetic variation). He also performed ddRAD sequencing, which captures information about genetic differences across populations (i.e. genetic variation).
In analyzing these two complementary datasets, Wang found that epigenetic and genetic distances were correlated between populations – that is to say, populations with high genetic divergence also had high epigenetic divergence. Recall that epigenetics are to not wholly independent from genetics, so this result is expected. However, each of these two types of variation – genetic and epigenetic – were also influenced by other factors.
In terms of genetic divergence, geographic distance was the strongest correlate – populations that were close to one another were more similar than populations that were further away. Interestingly, temperature and vegetation also appeared to play a role as well. In terms of epigenetic divergence, genetic distance (as represented by Fst) was the strongest predictor. Interestingly, however, vegetation was also a strong predictor as well. This suggests that on top of the genetic changes that accumulate when populations diverge, additional epigenetic shifts have also occurred, and are likely impacting the populations’ fitness in their respective environments.
These results highlight the importance of considering both genetic and epigenetic changes in studies of adaptive variation. Genomes alone may not explain the whole story! Wang is continuing this research in multiple avenues, including comparing results across species (e.g. comparing results from A. cristatellus to another trunk ground anole, A. cybotes on Hispaniola), and digging deeper into the functions of individual outlier loci from the RRBS sequencing. Looking forward to hearing more about this emerging perspective on adaptation in anoles!
Aging theory predicts that organisms will age faster when the probability of survival to old age is low. As a result, males and females of a species may age at distinct rates if they experience different rates of mortality due to environmental factors. Postdoctoral researcher Dr. Aaron Reedy (Auburn University) and colleagues tested this idea by performing a mark-recapture study of introduced Anolis sagrei in the small Island H in Florida, an island that is approximately the size of a baseball field.
Location of island H in Florida.
The team tracked 6,591 individuals of A. sagrei from hatchling to death through a near-complete sampling of the population four times a year between 2015 and 2019 (!!). The research group measured the body condition of individuals based on the residuals of mass on body length and estimated the rate of aging based on chromosomal telomere length from real-time qPCR.
The results suggest that males have higher mortality and shorter lifespans than females; most males die within two years, while females can live up to three and even four years. The study also found that males suffer a decline in body condition with age that females don’t seem to – Aaron even mentioned that he is often capable of predicting how old a male individual is based on how haggard it looks! Preliminary data suggests no statistical differences in telomere length between males and females, although there seems to be a trend of decreasing telomere length with age in males only.
Male brown anole.
In conclusion, Dr. Reedy and colleagues found that males have increased mortality and shorter lifespans than females, but it is unclear whether males senesce more rapidly. The next steps of this investigation will include longitudinal studies in both the field and lab to follow how fast single individuals age over their lifetimes.
Anoles throughout the Caribbean are found in urban environments and differ in the extent to which they utilize anthropogenic habitats. There is strong phylogenetic signal in urban tolerance but is not correlated with ecomorphology of anole species. Previous work by Dr. Kristin Winchell (currently a postdoctoral researcher at Washington University in St. Louis with Dr. Jonathan Losos) and collaborators showed that Anolis cristatellus commonly uses anthropogenic perches (e.g.- buildings and fences) in urban habitats, and that A. cristatellus has repeatedly adapted to urban environments. Urban A. cristatellus have longer limbs and greater numbers of lamellae when compared to their more rural counterparts, a pattern that is repeated island-wide.
With the prediction that species within the same ecomorph class would adapt to urban environments similarly, sampling has begun with four species from the Greater Antilles. Three species belong to the trunk-ground ecomorph (Anolis cybotes, Anolis lineatopus, and Anolis sagrei) and one trunk-crown species (Anolis grahami). In the Bahamas, examining Anolis sagrei she found significant shifts in relative limb length but in the opposite direction as seen in A. cristatellus. Meaning that urban A. sagrei have relatively shorter limbs, but it is worth noting that they have longer absolute limb length along with larger body sizes. Preliminary analyses of Anolis cybotes (Dominican Republic) and Anolisgrahami (Jamaica), suggest shifts in relative and absolute limb lengths consistent with the morphological differences found in urban A. cristatellus. In Anolis lineatopus, the suggested shifts in relative and absolute limb length are consistent with those shifts seen in A. sagrei.
Additionally, Kristin had all of us at the conference beat when it came to attire. Her Anolis lineatopus dress that she designed the art work for was spectacular. If you are interested in her Anolis and urban stickers and art– check out her work on RedBubble— all proceeds from her art goes to printing more stickers for outreach purposes in the communities she does her field research in.
Excellent job Kristin and we are all looking forward to learning more about this work!
In the 1990s, volcanic eruptions occurred on the island of Montserrat, which of course led to a reduction in the resident population of the plymouth anole, Anolis lividus, in the area of the island affected by the blast. However, populations appear to have recovered. But how? Were there a limited number of individuals that survived the volcano, and have now succesfully repopulated? Or did individuals from the northern region of the island colonize the southern region after the eruption? In addition, different populations throughout the region exhibit different body coloration, ranging from dark green to light brown. Does this morphological diversity represent underlying genetic divergence?
Catherine Jung is addressing these questions using genetic data from historical (1991-1992) and current (2018) samples. She has sequenced one nuclear and two mitochondrial genes to determine the relatedness among current populations across the island. Interestingly, she’s found no signatures of genetic structure across the island so far. She plans to continue this work by incorporating the genetic data from the historical specimens and performing more formalized demographic models to determine whether current southern populations (which were re-populated after the volcano) are more related to current northern populations (unaffected by the volcano), or historic southern populations (pre-volcano). As of right now, the question remains open, but stay tuned for more data! Answering these types of questions about the dynamics of population recovery is an important part of conservation research and application, and Jung’s work will contribute to our understanding of these processes in anoles.
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
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!
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).
