Tag: urbanization Page 1 of 2

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)!

Parallel Selection on Thermal Physiology Facilitates Repeated Adaptation of City Lizards to Urban Heat Islands

New literature alert!

In Nature Ecology and Evolution
Campbell-Staton, Winchell, Rochette, Fredette, Maayan, Schweizer, and Catchen

Abstract

Only recently have we begun to understand the ecological and evolutionary effects of urbanization on species, with studies revealing drastic impacts on community composition, gene flow, behaviour, morphology and physiology. However, our understanding of how adaptive evolution allows species to persist, and even thrive, in urban landscapes is still nascent. Here, we examine phenotypic, genomic and regulatory impacts of urbanization on a widespread lizard, the Puerto Rican crested anole (Anolis cristatellus). We find that urban lizards endure higher environmental temperatures and display greater heat tolerance than their forest counterparts. A single non-synonymous polymorphism within a protein synthesis gene (RARS) is associated with heat tolerance plasticity within urban heat islands and displays parallel signatures of selection in cities. Additionally, we identify groups of differentially expressed genes between habitats showing elevated genetic divergence in multiple urban–forest comparisons. These genes display evidence of adaptive regulatory evolution within cities and disproportionately cluster within regulatory modules associated with heat tolerance. This study provides evidence of temperature-mediated selection in urban heat islands with repeatable impacts on physiological evolution at multiple levels of biological hierarchy.

 

Campbell-Staton, S. C., Winchell, K. M., Rochette, N. C., Fredette, J., Maayan, I., Schweizer, R. M., & Catchen, J. (2020). Parallel selection on thermal physiology facilitates repeated adaptation of city lizards to urban heat islands. Nature Ecology & Evolution, 4(4), 652-658.

Phylogenetic Signal and Evolutionary Correlates of Urban Tolerance in a Widespread Neotropical Lizard Clade

New literature alert!

In Evolution
Winchell, Schliep, Mahler, Revell

Abstract

Urbanization is intensifying worldwide, and while some species tolerate and even exploit urban environments, many others are excluded entirely from this new habitat. Understanding the factors that underlie tolerance of urbanization is thus of rapidly growing importance. Here, we examine urban tolerance across a diverse group of lizards: Caribbean members of the neotropical genus Anolis. Our analyses reveal that urban tolerance has strong phylogenetic signal, suggesting that closely related species tend to respond similarly to urban environments. We propose that this characteristic of urban tolerance in anoles may be used to forecast the possible responses of species to increasing urbanization. In addition, we identified several key ecological and morphological traits that tend to be associated with tolerance in Anolis. Specifically, species experiencing hot and dry conditions in their natural environment and those that maintain higher body temperatures tend to have greater tolerance of urban habitats. We also found that tolerance of urbanization is positively associated with toepad lamella number and negatively associated with ventral scale density and relative hindlimb length. The identification of factors that predispose a species to be more or less urban tolerant can provide a starting point for conservation and sustainable development in our increasingly urbanized world.

 

Winchell, K. M., Schliep, K. P., Mahler, D. L., & Revell, L. J. (2020). Phylogenetic signal and evolutionary correlates of urban tolerance in a widespread neotropical lizard clade. Evolution.

SICB 2020: Artificial Light at Night Suppresses CORT Rhythmicity

Margaret McGrath at SICB 2020

If you look at a map of the United States at night, the urban areas are aglow with light pollution. Urban light pollution disrupts biological processes from gene expression to ecosystem composition across multiple taxa, including birds, insects, mammals, and fishes. With ever-increasing urbanization, understanding the effects of artificial light at night (ALAN) on organisms is crucial to future conservation efforts.

Margaret McGrath, an undergraduate in Dr. Christopher Howey’s lab at the University of Scranton, is examining the impact of ALAN on glucocorticoids in green anoles (Anoles carolinensis), which are commonly found in urban environments. Margaret specifically examined the impact of ALAN on the daily rhythmicity of corticosterone (CORT) and CORT responsiveness to an environmental stressor. She exposed green anoles to either a natural light-day cycle of 12 hours of light and 12 hours of dark or 24 hours of light. After six weeks of exposure, Margaret performed competitive immunoassays to measure baseline CORT levels at midnight and noon. Additionally, she measured CORT responsiveness after placing the green anoles in a bag for 30 minutes to simulate an environmental stressor.

Anoles not exposed to ALAN displayed an expected CORT daily rhythmicity with higher levels of CORT during the day than at night. Anoles exposed to ALAN lost this CORT rhythmicity and maintained CORT at a level intermediate to the other group. In contrast, ALAN does not appear to impact the anoles’ CORT responsiveness to environmental stressors. Her results suggest that green anoles exposed to ALAN are still able to respond to environmental stressors. However, there could be downstream effects from the loss of CORT rhythmicity because it has been linked to arrhythmic activity in mammalian studies.

In the future, Margaret plans to investigate if the natural CORT rhythmicity can be regained by anoles exposed to ALAN when placed back into a natural light-dark cycle. This future research can aid in determining the longevity of ALAN’s impacts on organisms. You can reach Margaret at margaret.mcgrath@scranton.edu and find more about her research on chowey.net, Dr. Howey’s website.

SICB 2020: Artificial Light Doesn’t Influence Immune Responses in Green Anoles

The Howey lab showed up to work at SICB 2020! In keeping with the theme of how urbanization and artificial light at night (ALAN) impacts wildlife populations, Elizabeth Kenny, an undergraduate researcher at the University of Scranton performed a study to describe the influence of artificial light on the immune response in green anoles (Anolis carolinensis).

The researchers used a test for immune response called a phytohemagglutinin test (PHA-L), where they injected the hindlimbs of green anoles with PHA-L and measured how much the foot swelled after both a 24 and a 48h hour period. But rest assured! PHA-L tests are temporary, only induce localized swelling, and have no larger impacts on the health of the organism; it’s sort of like if you’ve ever had a tuberculosis test done at your local physician. Interestingly, Elizabeth found no difference in swelling between green anoles exposed to ALAN and to green anoles that had not been exposed to ALAN. However, Elizabeth suggested that green anoles could respond sufficiently to ALAN by changing how they use the energy within their bodies and where they allocated those limited energetic stores, which provides a lot of support for the work of Michelle D’Allesandro and Meg McGrath. Altogether, the three undergraduate researchers of the Howey lab created a convincing and interesting story about how urban environments influence the energetics and physiology of city-dwelling lizards. Great stuff!

SICB 2020: City Anoles Have Bigger Toes!

Urbanization was a big theme at SICB 2020 this year, and studies of how city life influences wildlife populations are really important to help us understand the effects of human activity on natural environments and animals. One of the most rapid ways in that city-dwelling animals can adapt to these new environments is by changing the shape and size of various morphological traits.

Anoles in their natural habitat do tend to be tree-dwelling, or arboreal lizards, and they spend a lot of time climbing to find food resources, regulate their body temperature, and do other ecological activities. A lizard that relies so much on climbing performance frequently uses its claws and toe pads in its climbing ventures, so one of the first changes that city anoles might exhibit is changes in toe pad or claw shape to better climb on slick city surfaces (say that 3 times fast!). To get at this question, Bailey Howell from the Mississippi University for Women, along with her co-authors Travis Hagey and Kristin Winchell, compared urban crested anoles (Anolis cristatellus) to forested crested anoles and found that toe pads in urban anoles are longer and wider than toe pads from lizards in natural environments.

Bailey goes on to discuss that these toe pads that have an increased area might be better for urban anoles to climb on slicker and smoother substrates found in city environments. Bailey is going to continue adding to her dataset by incorporating more anoles and testing additional hypotheses such as measuring performance differences between urban and forested anoles. Stay tuned for more urban anole work!

Evolution 2019: Urbanization Across the Radiation

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 Anolis grahami (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!

JMIH 2018: How Does Artificial Light at Night Affect Anoles?

Crested Anole (Anolis cristatellus) under a leaf. Photo by Chris Thawley.

Conservation biologists have long been concerned about the effects of human development on species and environments. Urban habitats can significantly change lighting patterns for animals by increasing nocturnal ambient illumination. Artificial light at night (ALAN) has the potential to disrupt an organism’s physiology, behavior, and ecology. However, light pollution remains poorly studied and is a concern for urban herpetofauna.

Anolis lizards in Miami, Florida are a great system to study the effects of ALAN on behavior, health, reproduction, and survival. Anoles are diurnal and are adapted to a distinct photic habitat appropriate to their sun/shade preferences. However, many anole species have been observed active at night where artificial lights are prevalent. So, what are the effects of ALAN on anole fitness?

Chris Thawley, a postdoctoral researcher in the Kolbe Lab at the University of Rhode Island, is interested in whether ALAN  imposes selection on anoles and how they might adapt to these pressures. Chris conducted a field experiment introducing landscape lightning into a previously unlighted habitat within an urban matrix. For over two months, he assessed whether Brown Anoles (Anolis sagrei) and Crested Anoles (A. cristatellus) experienced higher levels of ALAN at their sleeping perches and if these lizards behaviorally avoided exposure to artificial light. Also, lizards were marked and followed to determine if light exposure impacted survival, growth, body condition, and physiology.

Chris found that A. sagrei and A. cristatellus lizards are not behaviorally avoiding ALAN at night. Anoles that were more exposed to artificial light had lower glucose levels compared to those that were less exposed. Also, there were no dramatic changes in reproduction, but ALAN reduced follicle size. Egg mass showed a positive relationship with snout-vent length (SVL) in lizards exposed to ALAN, which suggests that ALAN increases egg mass in larger lizards. Chris continues analyzing growth and survival data and aims to explore if there is a correlation between levels of corticosterone (CORT), melatonin, and glucose.

SICB 2017: Impacts of Urbanization on Morphology, Thermal Preference, and Parasitism

Chris Thawley at a crossroads.

Chris Thawley at a crossroads.

Urban environments are widespread and expanding across much of the earth, and this urbanization likely affects the flora and fauna in its path. Anoles are no exception and are frequently observed perching on anthropogenic structures. Thus, Chris Thawley, a post-doc in Jason Kolbe’s lab at the University of Rhode Island, and colleagues wondered how the abiotic and biotic changes in urban areas influence anole traits.

Thawley compared populations in urban and natural habitats of two species that we’re quite familiar with on Anole Annals – the Brown Anole (Anolis sagrei) and the Puerto Rican Crested Anole (Anolis cristatellus). Thawley found that A. sagrei prefers warmer temperatures than A. cristatellus, but that urban anoles do not differ in thermal preference than natural anoles for either species. Alternatively, urban male A. cristatellus and both sexes of urban A. sagrei were larger than their natural counterparts. As for parasites, A. sagrei had a higher parasite prevalence than A. cristatellus, but urban anoles did not differ from natural anoles in either species in parasite prevalence. However, for the A. sagrei that were parasitized, urban A. sagrei had higher parasite loads than natural A. sagrei.

These findings show that urbanization can influence anole morphology and parasite ecology. Thawley has just begun this work, and I look forward to seeing his future research on anole adaptation to urban environments!

Page 1 of 2

Powered by WordPress & Theme by Anders Norén