Author: Kristin Winchell Page 1 of 8

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!).

Puerto Rico Herpetology Symposium

The 7th annual Puerto Rico Herpetology Symposium will be held in just 3 weeks at the Universidad de Puerto Rico in Arecibo. Although we considered combining our anole meeting with this amazing event, we decided to keep the events separate for logistical reasons (thank you to everyone who so enthusiastically responded!). But that doesn’t mean you can’t still attend the upcoming one-day symposium on the beautiful island of Puerto Rico. This is a fantastic event that features academic and applied herpetological research from across the island. If you conduct your research in Puerto Rico (or would like to) this is a must-not-miss event. There are certain to be many talks and posters on anoles!

Tomorrow is your last chance to sign up for the meeting, which you can do at the following link: https://docs.google.com/forms/d/e/1FAIpQLScOC3PCCN5XjSnWwrptC2bCx7SCjKriQ0MnHG6x29qqtDA7iw/viewform

Hope to see you there!

Anole Symposium This Fall?

Calling all anole researchers and enthusiasts! We have a unique opportunity this fall that I would like to suggest we capitalize on. The Caribbean PARC (Partners in Amphibian and Reptile Conservation) meeting and the Puerto Rican Herpetology Symposium are currently being planned, tentatively for October 14-15 in Arecibo, Puerto Rico. I recently discussed with one of the organizers, Alberto Puente, the possibility of combining these two meetings with an Anole meeting. After all, it’s been 5 years since our 2018 meeting in Miami, so we are due for another meetup!

We had a great group of 68 attendees at the last Anolis symposium, held in Miami, Florida in 2018.

I’m here to gauge your interest, but first, let me sell you on the merits. I know October is only a few short months away, but combining forces with these other two groups in beautiful, anole-laden Puerto Rico has its benefits:

  • Researchers from all over the Caribbean will be in attendance, with a strong effort by the organizers to bring in herpetologists from Cuba and Dominican Republic.
  • There is tons of anole research in Puerto Rico by local researchers and tons of great herpetology as well! It will be a great opportunity to learn about local research and conservation efforts and build connections with students and professors at the extensive UPR system.
  • By combining forces we can have a much bigger and diverse meeting!
  • Puerto Rico has anoles! and bat hunting boas! and dwarf geckos! So many amazing herps! There will be herp outings!
  • We are working on arranging transportation and affordable options for housing.

Convinced? Fill out this poll and if there is support for this plan then I will take on organizing it (of course, anyone who wants to help out, let me know!). The format of such a meeting is still up in the air – integrate fully? have one day per group? parallel sessions? … So leave your feedback, advice, suggestions, warnings about how much work this will be, enthusiasm for the idea, offers to help, etc. in the comments below!

Parallel Urban Adaptation from Phenotype to Genotype in Anolis Lizards

Anoles are models for studying evolution in the wild. Not only do anoles have a history of repeatedly diversifying to specialize in the same types of microhabitats in the same ways across the Greater Antilles, these lizards also have a tendency to adapt on rapid timescales to environmental change — be it the addition or subtraction of a predator or competitor, a polar vortex, a change to the structural environment, or a hurricane.

Anoles are also models for urban evolution. Why? Anoles are found abundantly across the Caribbean in urban and forest environments where they specialize in divergent microenvironments characterized by shifts in climate and physical structure. Urban habitats tend to be warmer, drier, more open, and dominated by buildings and impervious surfaces instead of vegetation — providing the perfect opportunity for repeated adaptation to a novel combination of environmental conditions. In other words, Caribbean cities provide a replicated natural laboratory to study adaptation as it happens when these lizards colonize and thrive in urbanizing areas. And there is no shortage of urban-tolerant and urbanophilic anole species to choose from!

Species of Anolis lizards are found in urban environments across the Caribbean (photos CC-BY K. Winchell; Earth at night by NASA).

Congrats to the Newest Anole PhD: Dr. Avilés-Rodríguez!

A PhD that started with a hurricane and ended with a pandemic couldn’t slow down Kevin Avilés-Rodríguez — this past Friday Kevin became the newest anole doctorate when he defended his dissertation over Zoom on the interacting effects of urbanization and hurricane Maria on Anolis cristatellus.

Congratulations to Dr. Avilés-Rodríguez! And check out his amazing celebratory cake!

Urban Lizards Like It Hot (and Their Genes May Tell Us Why)

Anolis allisoni, Photo by breslauer iNaturalist

Cities are hot. Because of the urban heat island effect, urban environments tend to be significantly warmer than nearby non-urban environments. For ectothermic organisms, like lizards and insects, elevated urban temperatures create thermally stressful conditions. It might be unsurprising then that researchers have documented an increase in thermal tolerance in urban animals (e.g., City Ants Adapt to Hotter Environment). These studies point to the ability to cope with elevated urban temperatures as a critical aspect of persisting in urban environments.

Although there is evidence that the urban environment shapes adaptive thermal tolerance in Anolis lizards at the genomic level, it is also possible that anole species that thrive in hot urban environments have an innate ability to do so due to local adaptation in their ancestral habitat (i.e., forests). In fact, an analysis of patterns of urban tolerance across Caribbean anoles found that species that experience hotter and drier temperatures in their native ranges and those that maintain higher field body temperatures tended to be the ones that do well in urban environments (Winchell et al. 2020). And when researchers looked at genomic variation in Cuban species not found in urban areas, they identified genes associated with thermal sensitivity (Akashi et al. 2016), suggesting tolerance of different thermal environments may be encoded at the genomic level. But does this mean that some anoles are predisposed to tolerate hot urban temperatures based on the climate of their ancestral forest homes?

Kanamori et al. (2021) — “Detection of genes positively selected in Cuban Anolis lizards that naturally inhabit hot and open areas and currently thrive in urban areas” — set out to answer this question by examining the transcriptome of nine species of Cuban anoles that occupy different thermal microhabitats. Cuba is home to the largest number of anole species, with species diversifying to occupy distinct thermal and structural microhabitats. In their study, the researchers attempted to identify genomic signatures of selection in non-urban populations of species that thrive in urban environments in order to understand if there was something unique about the genetic background related to thermal tolerance in these species that enables urban colonization.

Of the nine species Kanamori and colleagues studied, three are found in naturally hot and open environments: A. allisoni, A. porcatusand A. sagrei, representing two different branches of the Cuban anole radiation. These three species (and several of their close relatives) also thrive in urban environments both in Cuba (e.g., Havana) and in their non-native range (e.g., Miami, Florida).

Five other species are found in cool and deeply shaded forests: A. alutaceusA. isolepisA. garridoiA. allogus, and A. mestrei. The last species, A. homolechis, is common in the shaded areas of forest margins.

Kanamori and colleagues examined a total of 5,962 genes and found genomic signatures of selection in 21 genes in the two main branches of species that contain urbanophilic species (A. porcatus  A. allisoni, and A. sagrei), but did not identify selection in the same genes across the two lineages. In other words, these closely related species have found unique genomic pathways to deal with the hot and dry forest environments in which they thrive. This finding suggests that the predisposition to tolerate hot urban environments is determined by different genes in different anole species, and raises the possibility that further local adaptation to urban thermal environments may also be lineage specific.

When the researchers looked at the functional associations of the genes under selection in each species, they found that they were related to stress responses, epidermal tolerance to desiccation, and cardiac function. All three of these biological functions are implicated in maintaining appropriate acclimation responses to thermal stress in anoles. These findings implicate ancestral selection on stress responses, perhaps in response to thermal or ultraviolet radiation, as potential factors influencing tolerance of anoles in urban environments. Further exploring the importance of these functions will shed light on their role in the initial tolerance of urban environments upon urban colonization and adaptive modification as urban lineages persist.


Read the full paper here: 

Kanamori, S., Cádiz, A., Díaz, L.M., Ishii, Y., Nakayama, T. and Kawata, M., 2021. Detection of genes positively selected in Cuban Anolis lizards that naturally inhabit hot and open areas and currently thrive in urban areas. Ecology and Evolution, 11(4), pp.1719-1728.

This post was cross-posted on the blog “Life in the City” — check it out if you want to learn more about urban evolution!

Tolerance to Urbanization is Widespread in Anoles

From Winchell et al. (2020): Anoles throughout the Caribbean differ in their tolerance to urbanization. Red colors = urban tolerant, blue colors = intermediate tolerance, green colors = urban intolerant.

Seven years ago I asked for the help of Anole Annals readers as I started to think about how different species of anoles throughout the Caribbean tolerate urbanization. This question, it turned out, was a lot more complex than I had originally anticipated! The idea was simple, find out which species are in urban areas and to what extent they use urban habitat elements, then determine if there is an evolutionary signal in urban tolerance and what traits are correlated with urban tolerance. Many hours of troubleshooting and brainstorming with my coauthors Klaus Schliep, Luke Mahler, and Liam Revell (and years later) and this study is finally out in the journal Evolution: Phylogenetic signal and evolutionary correlates of urban tolerance in a widespread neotropical lizard clade.

Anolis lineatopus, one of many urban tolerant anoles (photo K. Winchell)

Inventorying urban species

To figure out which anole species are tolerant of urbanization, my initial plan was to survey researchers and the literature to score each of the 100+ Caribbean species based on their presence in different types of urban habitats and their habitat use. Although I got a lot of great feedback from this original survey, it left a lot of gaps in the dataset. I needed to find a more objective way to assess urban tolerance.

With the help of Klaus Schliep and Luke Mahler, we decided to examine location records in museum collections (via GBIF) to determine which species had been observed (collected) in urban environments. Because we suspected museum records might be biased towards non-urban habitats, we also examined location records from the citizen science database iNaturalist, which we suspected might be biased in the opposite direction (i.e., people photograph things where they live). For each record, we looked at satellite imagery and scored the observation as urban or non-urban, then tallied the total number of observations and the total number of urban observations per species.

Even with these two data sources, we noticed gaps in our data for some species. So we included a third source, Henderson & Powell’s (2009) book on the Natural History of West Indian Amphibians and Reptiles. This fantastic reference (highly recommended!) gives detailed natural history information and summarizes key features of every anole (and other Caribbean herps) in the Caribbean. Of course, this is more subjective than the location-based data, so Luke and I came up with a scoring system that assigned a set number of urban tolerant or avoid “points” based on key descriptors. For example, if a species was described as being common around houses and often observed on buildings, it would get points for being tolerant of urbanization. In contrast, a species described as having a restricted range and intolerance of anthropogenic disturbance, it would get points for being intolerant.

Analyzing urban tolerance in a phylogenetic framework

We combined these disparate data sources into a logistic model with parameters we set based on the number of urban observations we would need to be certain of urban tolerance and how many total observations we would need to be certain of our species assessment. This resulted in a probability of being an urban avoider or urban tolerant for each species, which we used as our prior probabilities for these states in our phylogenetic model. We then reconstructed ancestral states and missing tip states for urban tolerance in 131 species of Caribbean anoles.

Of course, we don’t mean to say that we attempted to reconstruct the evolution of urban habitat use — anoles are far older than urbanization! Instead, we wanted to understand the evolution of the behavioral, physiological, ecological, and morphological traits traits that influence whether a species will exploit or avoid urban habitat when it arises. The threshold model is well-suited for this type of complex trait. The threshold model assumes that a discrete trait is determined by a combination of continuously valued characteristics. These characteristics may be measurable, unmeasurable, or even unknown. As a taxon accumulates specific trait changes, the species is pushed incrementally closer and closer to the discrete state change (in this case urban tolerance), and the more recently this discrete character state has flipped, the more likely a reversal to the previous state could occur. From this model we can extract a single continuously valued trait, the liability, that underlies the complex trait of urban tolerance.

Urban tolerance in Caribbean anoles, from Winchell et al. (2020).

Traits of urban species

So what did we find? To start, urban tolerance appears to be widespread in Caribbean anoles and has a strong phylogenetic signal. Because of that, we suggest that our approach may be used to predict urban tolerance of species that either have yet to encounter urbanization or for which we are lacking information. This application could be particularly useful for determining which species are likely to be intolerant of urbanization and thus should be prioritized in conservation efforts. At the other end of the urban tolerance scale, we caution that our approach should not be used to predict species that are robust to anthropogenic habitat loss, but rather that it might be useful to identify species that are promising for future urban ecology and evolution studies.

Finally, we used the liability score for each species to try to get a better understanding of what those traits underlying urban tolerance are exactly. Using PGLS we looked for correlations between the liability and a suite of ecological and phenotypic traits. We found that species that are more tolerant of urbanization had higher field body temperatures, fewer ventral scales, more rear lamellae, shorter hindlimbs, and experience warmer and drier climates within their native range. These traits may be key “pre-adaptations” enabling species to colonize urban habitats as they arise and to take advantage of anthropogenic niche space (i.e., on and around buildings). For example, urban habitats tend to be hotter and drier than nearby forest sites, so it makes sense that species with larger ventral scales, higher field body temperatures, and which experience hotter and drier temperatures in their non-urban range would be predisposed to tolerate urban habitats. Similarly, lamellae are important for clinging to smooth surfaces, which may be particularly beneficial in urban habitats dominated by smooth anthropogenic surfaces.

Lastly, we found, somewhat to our surprise, that no one ecomorph seems to be best suited for urban environments. Based on our experience, we had thought that trunk-ground anoles would be more likely to tolerate urbanization, but it turns out that there are a lot of trunk-ground anoles that are intolerant of urbanization and a lot of species from other ecomorphs that are tolerant (think A. equestris or A. distichus)!

The Highest Kingdom of Anolis: Thermal Biology of the Andean lizard Anolis heterodermus Over an Elevational Gradient in the Eastern Cordillera of Colombia

New literature alert!

In Journal of Thermal Biology
Méndez-Galeano, Paternina-Cruz, and Calderón-Espinosa

Abstract

Vertebrate ectotherms may deal with changes of environmental temperatures by behavioral and/or physiological mechanisms. Reptiles inhabiting tropical highlands face extreme fluctuating daily temperatures, and extreme values and intervals of fluctuations vary with altitude. Anolis heterodermus occurs between 1800 m to 3750 m elevation in the tropical Andes, and is the Anolis species found at the highest altitude known. We evaluated which strategies populations from elevations of 2200 m, 2650 m and 3400 m use to cope with environmental temperatures. We measured body, preferred, critical maximum and minimum temperatures, and sprint speed at different body temperatures of individuals, as well as operative temperatures. Anolis heterodermus exhibits behavioral adjustments in response to changes in environmental temperatures across altitudes. Likewise, physiological traits exhibit intrapopulation variations, but they are similar among populations, tended to the “static” side of the evolution of thermal traits spectrum. The thermoregulatory behavioral strategy in this species is extremely plastic, and lizards adjust even to fluctuating environmental conditions from day to day. Unlike other Anolis species, at low thermal quality of the habitat, lizards are thermoconformers, particularly at the highest altitudes, where cloudy days can intensify this strategy even more. Our study reveals that the pattern of strategies for dealing with thermal ambient variations and their relation to extinction risks in the tropics that are caused by global warming is perhaps more complex for lizards than previously thought.

 

Méndez-Galeano, M. A., Paternina-Cruz, R. F., & Calderón-Espinosa, M. L. (2020). The highest kingdom of Anolis: Thermal biology of the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) over an elevational gradient in the Eastern Cordillera of Colombia. Journal of Thermal Biology, 89, 102498.

Anole Annals Has a New Look!

You spoke, we listened. We’ve been working hard behind the scenes to renovate Anole Annals. Yesterday we unveiled a new look, but not just that — comments are working again!

Please bear with us over the next few days as we work out the minor issues with this transition. And if you have any ideas of ways to improve the site, let us know by email or comment below, or better yet, consider joining our board of editors to get in on the behind the scenes action!

Hurricane Effects on Neotropical Lizards Span Geographic and Phylogenetic Scales

New literature alert!

In PNAS
DonihueKowaleski, Losos, Algar, Baeckens, Buchkowski, Fabre, Frank, GenevaReynolds, Stroud, Velasco, Kolbe, Mahler, and Herrel

Abstract

Extreme climate events such as droughts, cold snaps, and hurricanes can be powerful agents of natural selection, producing acute selective pressures very different from the everyday pressures acting on organisms. However, it remains unknown whether these infrequent but severe disruptions are quickly erased by quotidian selective forces, or whether they have the potential to durably shape biodiversity patterns across regions and clades. Here, we show that hurricanes have enduring evolutionary impacts on the morphology of anoles, a diverse Neotropical lizard clade. We first demonstrate a transgenerational effect of extreme selection on toepad area for two populations struck by hurricanes in 2017. Given this short-term effect of hurricanes, we then asked whether populations and species that more frequently experienced hurricanes have larger toepads. Using 70 y of historical hurricane data, we demonstrate that, indeed, toepad area positively correlates with hurricane activity for both 12 island populations of Anolis sagreiand 188 Anolis species throughout the Neotropics. Extreme climate events are intensifying due to climate change and may represent overlooked drivers of biogeographic and large-scale biodiversity patterns.

 

Does Breeding Season Variation Affect Evolution of a Sexual Signaling Trait in a Tropical Lizard Clade?

New literature alert!

In Ecology and Evolution
Gray, Barley, Hillis, Pavón‐Vázquez, Poe, White

Abstract

Sexually selected traits can be expected to increase in importance when the period of sexual behavior is constrained, such as in seasonally restricted breeders. Anolis lizard male dewlaps are classic examples of multifaceted signaling traits, with demonstrated intraspecific reproductive function reflected in courtship behavior. Fitch and Hillis found a correlation between dewlap size and seasonality in mainland Anolis using traditional statistical methods and suggested that seasonally restricted breeding seasons enhanced the differentiation of this signaling trait. Here, we present two tests of the Fitch–Hillis Hypothesis using new phylogenetic and morphological data sets for 44 species of Mexican Anolis. A significant relationship between dewlap size and seasonality is evident in phylogenetically uncorrected analyses but erodes once phylogeny is accounted for. This loss of strong statistical support for a relationship between a key aspect of dewlap morphology and seasonality also occurs within a species complex (A. sericeus group) that inhabits seasonal and aseasonal environments. Our results fail to support seasonality as a strong driver of evolution of Anolis dewlap size. We discuss the implications of our results and the difficulty of disentangling the strength of single mechanisms on trait evolution when multiple selection pressures are likely at play.

 

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