Tag: phylogenetics

Tolerance to Urbanization is Widespread in Anoles

On May 5, 2020

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)!

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

By Kristin Winchell

On March 5, 2020

In New Lit Abstracts

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.

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.

JMIH 2018: Does the Bluefields Anole (A. opalinus) Contain a Cryptic Species?

By Chris Thawley

On July 14, 2018

In New Research

Kiyomi Johnson (L) and Marina Carbi (R) presenting their poster, “Speciation and Phylogeography of Anolis opalinus on Jamaica,” at JMIH 2018.

Caribbean anoles have been studied extensively, with researchers examining their evolution, ecology, physiology, morphology, and behavior in many different contexts. In some respects, they are one of the best known groups of organisms in the world. But are there still unique species “hidden” within the diversity of anoles we already know? Some papers suggest just that. In 2002, Jackman et al. examined the mitochondrial DNA of Jamaican anoles and found evidence that several species contained deeply diverged clades, indicating the potential presence of cryptic species.

Enter Marina Carbi and Kiyomi Johnson, two public high school students with a drive to dig into the biological sciences and a budding curiosity about all things Anolis. Ms. Carbi, a recent high school graduate, and Ms. Johnson, a rising senior at Fiorello H. LaGuardia public high school, began an internship specifically for high school students at the American Museum of Natural History. Working with Dr. Ed Myers, they set out to investigate the phylogenetic diversity in A. opalinus, the Bluefields anole, by sequencing a combination of mitochondrial and nuclear DNA from a series of 22 specimens of Jamaican anoles.

Mss. Carbi and Johnson found that both the mitochondrial data and combined species tree support the existence of a cryptic species within what is currently considered A. opalinus. Populations of the Bluefields anole found in the Blue Mountains area are monophyletic and sister to A. valencienni, indicating a potentially deep divergence from A. opalinus. Todd Jackman, whose initial work inspired this research, dropped by to check out Kiyomi and Marina’s follow up to his paper and was impressed. “Hopefully, they can go to Jamaica themselves,” Todd remarked, before adding as an aside, “I’m glad that their results match ours.”

The authors presented strong evidence that A. opalinus contains a cryptic species. Pic via Twitter.

Looking forward, Ms. Carbi has plans to attend Cornell University in the future, while Ms. Johnson is completing her high school degree. Both expressed interest in continuing to work in biology, with Ms. Carbi noting that she was excited to have had the opportunity to interact with researchers from Cornell at JMIH. The Society for the Study of Amphibians and Reptiles provided support for Mss. Johnson and Carbi to attend the meeting. More extensive sequencing is ongoing in order to further elucidate the phylogeography of what is currently known as Anolis opalinus. Stay tuned!

Resolving Phylogenetic Uncertainty in Anoles Using Treescape

By Michelle Kendall

On July 5, 2016

In All Posts, Lizards in an Evolutionary Tree

It’s an all-too-common situation: you would like to infer a phylogeny for a set of organisms, you try a few different methods and you end up with many different trees. Even with the most careful choice of software, settings, tree priors, and the most beautifully converged Bayesian posterior likelihood, you may find that the maximum clade credibility (MCC) tree has low posterior support for certain deep clades.

Anole MCC tree with posterior supports, from Geneva et al. [1]

Tree inference is very complicated, particularly for species trees, and is hampered by factors which include the vast size of tree space, conflicting signals from different genetic loci, confusing signals from convergent evolution, and non-tree-like evolution (recombination, hybridisation, etc.). Geneva et al. experienced just this sort of difficulty when they performed a comprehensive Bayesian phylogenetic analysis of the distichus group of trunk ecomorph anoles [1]. Their MCC tree is reproduced here, and the posterior support values show uncertainty in the branching structure of various deep clades. There are many combinations of ways to resolve these uncertain splits. We wanted to see which alternative trees were supported by the data.

In our recent paper [2] we present a method for handling phylogenetic uncertainty and incongruence. It takes a set of trees and “maps” them into a simple plot where similar trees are grouped together and more different trees are placed further apart. Where many similar trees are clustered together, contour lines indicate the density of points in that region. We began the development of our method theoretically, making sure we had designed a robust mathematical definition for tree distances which would correspond to biological intuition and lend itself to good quality map projections. Then, working closely with biologists, we fine-tuned our method for specific applications with real data and wrote the R package treescape [3] so that anyone can use it – there’s even a handy web app version which requires no knowledge of R.

treescape MDS plot: each point represents a tree, and proximity of points represents similarity of trees. 1000 trees are plotted here, many identical, so contour lines indicate density of points. Colours correspond to clusters of similar trees.

treescape MDS plot: each point represents a tree, and proximity of points represents similarity of trees. 1000 trees are plotted here, many of which are identical, so contour lines indicate the density of points. Colours correspond to clusters of similar trees.

When we applied our method to the trees from the analysis of Geneva et al. [4], we found that there were distinct “clusters” of equally likely tree topologies. It is reassuring that the MCC tree belongs to the largest of these clusters (highlighted on the plot by a yellow triangle), but clearly it cannot represent all of the likely tree shapes on its own. By taking a representative tree from each of the six or so tight clusters, we obtain a more thorough summary of the range of trees supported by the analysis. Such representative trees, taken from the geometric “centre” of each cluster, are credible summary trees with real branch lengths, unlike trees from other summary methods which can suffer from strange behaviour such as negative branch lengths.

We find that there are alternative placements of certain taxa, particularly the ocior, distichus, dominicensis2 clade, and (in our supplement) we explore some of the knock-on effects of using these different tree shapes when analysing the evolution of the anoles, specifically their geographical origins and transitions in their dewlap colour. For instance, we show here a representative tree from each of two different clusters on the map. The trees support ocior, distichus, and dominicensis2 being more closely related to anoles from the East of Hispaniola (the North paleo-island) or the South-West (the South paleo-island) respectively. Both evolutionary histories are supported by the data; in the absence of further research, there is no reason to exclude any of the alternative representative trees identified by our method.

Representative tree from top left cluster

Representative tree from top right cluster

[1] Geneva, A. J., Hilton, J., Noll, S. and Glor, R. E. (2015). Multilocus phylogenetic analyses of Hispaniolan and Bahamian trunk anoles (distichus species group). Molecular Phylogenetics and Evolution, 87:105-117.

[2] Kendall, M. and Colijn, C. (2016) Mapping phylogenetic trees to reveal distinct patterns of evolution. Molecular Biology and Evolution, first published online June 24, 2016. DOI: 10.1093/molbev/msw124

[3] Jombart T., Kendall M., Almagro-Garcia J., Colijn C. (2015). treescape: statistical exploration of landscapes of phylogenetic trees. R package version 1.9.17.

[4] Geneva A. J., Hilton J., Noll, S. and Glor, R. E. (2015). Data from: Multilocus phylogenetic analyses of Hispaniolan and Bahamian trunk anoles (distichus species group). Dryad Digital Repository.