Category: New Research Page 7 of 66

Evolution 2019: On the Origin of Anolis Sex Chromosomes

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Emmanuel D’Agostino presenting his undergraduate research at Evolution 2019.

Emmanuel D’Agostino, a (recently graduated) undergraduate in the Losos lab at Harvard  presented his undergraduate thesis at Evolution 2019. Working with Colin Donihue, Anthony Geneva, and Jonathan Losos, Emmanuel analyzed genetics, morphology, and mating behavior of Anolis sagrei collected from across their Bahamian range. Anolis sagrei differ pretty drastically in ecomorphological and sexually selected traits on different islands throughout the Bahamas. Emmanuel wanted to find out if this differentiation created barriers to mating  among divergent populations on different islands.

Emmanuel analyzed an impressive 184 videos of recently paired males and females from different islands under laboratory conditions. (Emmanuel informs me that there were actually 234 videos but many he could not score because of uncooperative lizards hiding behind the planters and out of view of the camera – who knows what they did back there!). He then quantified latency to mate to see if individuals from different islands would mate freely and if willingness to mate was related to morphological differences. He combined his video analysis with genomic and morphological data to understand how genetically and morphologically distinct populations are.

Emmanuel found that individuals from different populations mate freely, suggesting no effect of premating isolation related to morphological disparity. He also analyzed a large number of linear models to tease apart the relative contributions of genetics and morphology and found that the most important predictor of mating success was relative head size – males with smaller head sizes correlated with increased likelihood of mating success! Intriguingly, in his final analysis he found that males that mated the quickest had decreased offspring survival rates. So even though smaller-headed males may mate more readily, their offspring are less likely to survive.

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

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

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

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

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

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

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

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

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

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

Exercise Can Kill You (If You’re an Anole)!

Green anoles were trained, marked, released, and tracked in New Orleans. Photo by Jerry Husak.

In the US, we spend a lot of money trying to stay fit. This isn’t necessarily a bad thing, since there is a major problem with obesity and type II diabetes in the country. In humans, investment in increased performance abilities via the exercise response is also associated with numerous health benefits, such as decreased incidences of metabolic syndrome, cardiovascular disease, obesity, and diabetes, and aerobic capacity is considered to be an important predictor of longevity. However, it is these “side effects” that make exercise so interesting to an evolutionary biologist, because those wide-ranging, multi-system responses can tell us something about the evolution of animal life histories.

Superior locomotor performance has been shown to be advantageous to a variety of organisms in terms of male combat success, survival, and fitness. In addition, one of the most striking aspects of exercise physiology is how similar the response to exercise is across vertebrate animals, suggesting that the response to exercise is both ancient (yes, even fish respond to exercise!) and adaptive. However, until now, no studies have tested whether non-human animals that invest in increased athletic performance through exercise realize a fitness advantage in nature.

Jerry Husak and Simon Lailvaux set out to test whether superior performance after exercise training would increase survival probability in green anole lizards. Previous work with green anoles showed that they respond to different forms of exercise training, and that enhanced performance results in tradeoffs in other systems, such as reproduction and immnuocompetence. Why? Because performance abilities are energetically expensive to build, maintain, and use.

Urban islands in New Orleans where the study was conducted. Photo by Jerry Husak.

Jerry and Simon conducted their study in a New Orleans urban park that they cleared of existing lizards. They trained 30 lizards (15 male, 15 female) for endurance on a treadmill, 30 lizards for sprinting with weights on a racetrack, and had 30 untrained controls. All were released into isolated, urban islands in New Orleans, LA, USA and monitored for survival over an active season, over winter, and through the next active season. They predicted that training would enhance survival during the active season, but that the associated maintenance costs of training would decrease survival overwinter compared to controls.

This male made it a year in the wilds of New Orleans, but it looks like it was a rough year. Photo by Jerry Husak.

Contrary to expectations, they found that sedentary controls realized a significant survivorship advantage over all time periods compared to trained lizards. Trained lizards had reduced immune systems and lower fat stores, suggesting that in an environment with limited resources, it does not pay to exercise too much. These results suggest that locomotor capacity is currently optimized to maximize survival in green anoles, and that forcing additional investment in performance moves them into a suboptimal phenotypic space relative to their current environmental demands. We as humans can get away with it because we are not food limited. On the other hand, this is why doctors suggest consultation before going on a diet and doing intensive exercise training.

Source: Husak, J.F., and S.P. Lailvaux. 2019. Experimentally enhanced performance decreases survival in nature. Biology Letters 15:20190160. doi: doi.org/10.1098/rsbl.2019.0160.

Of Anoles and Salad: From Steinbeck to Prebagged Lettuce

Lizard in a grocery store salad

“I got an idea and I can’t get rid of it. I go to sleep and it comes right back at me. Never had anything give me so much trouble. It’s kind of a big idea. Maybe it’s full of holes.” – Adam Trask in East of Eden.

Embed from Getty Images

John Steinbeck (1962): The year he won the Nobel Prize in Literature.

So, what was Adam Trask’s big idea in John Steinbeck’s magnum opusEast of Eden”? And, more importantly, how does it relate to anoles? The kernel of an idea that would eventually revolutionize the salad industry—and link anoles to a literary legend—can be found in the fictional dialogue written by Steinbeck in 1952.

“… they’ve dug up a mastodon in Siberia. Been in the ice thousands of years. And the meat’s still good.”  said Adam Trask.

“Mastodon?” inquired Will Hamilton.

“Yes, a kind of elephant that hasn’t lived on the earth for a long time.”

“Meat was still fresh?” asked Will.

“Sweet as a porkchop”  proclaimed Adam.

Steinbeck was born in the Salinas Valley of Central California, known as “America’s Salad Bowl” for its prodigious production of leafy greens. He spent many summers, while away from college at Stanford, working in the vegetable fields near Salinas. Steinbeck’s fondness for his birthplace and working knowledge of the agriculture industry is a cornerstone to many of his novels, especially “East of Eden.”

“… in the cold parts of the country, don’t you think people get to wanting perishable things in the winter—like peas and lettuce and cauliflower? In a big parts of the country they don’t have those things for months and months. And right here in the Salinas Valley we can raise them all the year around.” declared Adam.

“Right here isn’t right there,” said Will. “What’s your idea?”

“… if you chop ice fine and lay a head of lettuce in it and wrap it in waxed paper, in will keep three weeks and come out fresh and good.” said Adam.

“Go on,” said Will cautiously.

“Well, you know the railroads … they’re pretty good. Do you know we could ship lettuce right to the east coast in the middle of winter?”

The perennial availability of perishable vegetables in the United States is now commonplace, but in the early 1900s, it made literary characters like Will Hamilton exclaim to Adam Trask to “let your damned idea die.” In fact, America’s most popular lettuce variety (iceberg) was originally called crisphead, until Salinas Valley growers began packing it with crushed ice and shipping it nationwide. The genesis of Adam Trask’s business plan was obviously fictional, but the idea of shipping lettuce with ice was successful and revolutionary in the early 1900’s; however, the method never quite kept vegetables fresh for long enough.

“What arrived in New York was six carloads of horrible slop with a sizable charge just to get rid of it.” – East of Eden by John Steinbeck.

In the pursuit of profitable ways to ensure lettuce does not turn into “horrible slop,” the next advance in production came from the humble bag. Lettuce can last for days on ice, but a bagged salad can last for a couple of weeks. It’s always difficult to establish the original (or best) anything in the food industry (vis-à-vis famous rivalries such as Pat’s versus Geno’s for cheesesteaks or Pepe’s versus Sally’s for pizza), but the late 1980s in the Salinas Valley is believed to be when and where the first bagged salads were packaged, distributed from, and then sold nationwide. The bagged salad turned a commodity crop whose predictability was in the capricious hands of nature into a consumer good as constant on the shelves of stores as shampoo or Twinkies.

Over the next decades, prepackaged leafy green vegetables boomed. To keep up with demand, growers invented creative ways to automate aspects of the production process, such as mechanically harvesting leafy greens. They also ramped-up the speed across the entire supply chain, such that lettuce could be bagged in the field within minutes of harvest and then sent overnight to supermarkets nationwide. These overlapping vignettes of industrial prepackaged salads provide the backdrop for a distinctly modern human-wildlife interaction: Small wild animals found by customers in prepackaged produce.

In our recent paper, we attempted to shed light on this poorly understood phenomenon by surveying online news articles for reported incidents. In doing so, we found that this is a much more common occurrence than one might think and that incidents encompassed representatives of several vertebrate groups. Most incidents involved amphibians (treefrogs and toads), and then reptiles (lizards and snakes), mammals (rodents), and birds. Anoles were the most common lizard that we could identify from the pictures and descriptions provided in the reports. The anole incidents included Green Fruit Loop, the aptly named Green Anole that became a class pet at Riverside Elementary in New Jersey. We suggested that the likely source of Green Anoles among the incidents was Florida because not only is the species is common there, but by 2012 the state was the third largest producer of leafy green vegetables in the United States, behind only California and Arizona.

Figure 1 from Hughes et al. (2019): Taxonomic and temporal breakdown for 40 incidents of extemporaneous wild animals found by customers in prepackaged produce items purchased in the United States. A) Vertebrate diversity among incidents; B) Annual distribution of incidents; and C) Monthly distribution of incidents.

 

An interesting social element emerged from my deep-dive into the trenches of the internet. I found that these incidents were shrouded in uncertainty and thus reporters often relied on anecdotes to discuss and describe them. One common urban myth was that these incidents almost never happen and the second was that if they happen, then it was because the produce was organic. In contrast to these popular views, we found that at least 40 incidents were reported since 2003—so, not exactly rare—and that less than 30% of incidents involved organic produce—most actually came from conventionally grown crops. For greater context and more details, see the Discussion of our paper where we address: 1) why these unfounded views may have persisted; 2) spatial, taxonomic, and seasonal patterns to our findings; 3) our results in the context of competing demands imposed upon the produce industry; and 4) the biosecurity concerns relating to the unintentional translocation of wild amphibians.

Modern agriculture has taken significant steps towards industrialization since the time that John Steinbeck penned Adam Task’s revolutionary idea (see Epilogue). Industrialization of food production will help to address the problems associated with feeding 9 billion people, a figure that is projected for the human population by 2050. Wild vertebrates in prepackaged produce, however, may be one symptom of an overburdened and overstretched produce production system. Any solution to this problem will not likely come from greater controls for wildlife, such as the currently employed “scorched earth” approach, but rather from the decentralization of agriculture. We suggest that the best approach would be to first invest in research aimed at studying a wide segment of biodiversity near agricultural lands, which will help growers assess potential intrusion risks of more species, and second to adopt quality control methods that account for a greater diversity of wildlife to improve screening at more stages in the produce supply chain.

Epilogue:

The birth of Adam Trask’s plan was fictional, but the growth of that idea, as depicted in the novel, is a great example of John Steinbeck’s (often overlooked) scientific mind. While many people my age read “Of Mice and Men” in high school and got to know Steinbeck the literary genius, they may not know Steinbeck the scientist. Ed Ricketts was a marine biologist that became a lifelong friend to Steinbeck when he moved to Monterey in the 1930s. The relationship between the writer and the scientist was one of mutual respect and admiration. At one point, they even undertook a six-week specimen-collecting expedition to the Gulf of California, which resulted in two published books. Not only was Ricketts the basis for Steinbeck’s character “Doc” in several novels (e.g., “Cannery Row”), but the influence he had on Steinbeck is unmistakable in many of his other works, including “East of Eden.” Adam Trask, for example, spawned his idea for preserving lettuce with ice from a scientific expedition that found a frozen mastodon in Siberia, and he read about this finding, refrigeration science, and bacterial growth in articles from “Atlantic Monthly,” “National Geographic,” and “Scientific American.” The mentioning of these specific journal titles in “East of Eden” was by no coincidence as they would have been the same ones that Steinbeck saw, and likely read, in Rickett’s lab, a place that he visited frequently. At the time of Ricketts death in 1948 (which sent Steinbeck into a depression), the two were planning another collecting expedition to British Columbia and another book.

Island Lizards are Expert Sunbathers, and It’s Slowing Their Evolution.

Anolis chloris soaks up the sun while displaying.

If you’ve ever spent some time in the Caribbean, you might have noticed that humans are not the only organisms soaking up the sun. Anoles – diminutive little tree lizards – spend much of their day shuttling in and out of shade. But, according to a new study in Evolution led by Dr. Martha Muñoz at Virginia Tech and Jhan Salazar at Universidad Icesi, this behavioral “thermoregulation” isn’t just affecting their body temperature. Surprisingly, it’s also slowing their evolution.

The idea that evolution can be slow on islands is actually somewhat strange. Ever since Darwin’s journey to the Galapagos, islands have been recognized as hotspots of rapid evolution, resulting in many ecologically diverse species. The reason why evolution often goes into overdrive on islands has to do with the ecological opportunity presented by simplified environments. When organisms wash up on remote islands, they find themselves freed of their usual competitors and predators, which frees them to rapidly diversify to fill new niches. This phenomenon of faster evolution is often referred to as the “island effect.”

Yet, the researchers discovered that physiological evolution in Anolis lizards is actually much slower on islands than on the mainland. What is causing evolution to stall? According to Dr. Muñoz, the same ecological opportunity that frees island organisms from predators also facilitates behavioral thermoregulation. “Whereas mainland lizards spend most of their time hiding from predators, island lizards move around more, and are able to spend much of their day precisely shuttling between sun and shade,” she says. If it gets too hot, island lizards simply go find a shady spot. If it gets too cold, they can dash onto a sunny perch. By thermoregulating, island lizards are not just buffering themselves from thermal variation. They are effectively shielding themselves from natural selection. If lizards aren’t exposed to extreme temperatures, then selection on physiology is weakened. The result? Slower rates of physiological evolution. Effectively, island lizards use behavioral thermoregulation like SPF against natural selection!

Jhan Salazar notes that, “Our results show that faster evolution on islands is not a general rule.”  This slower physiological evolution on islands stands in stark contrast to morphology, which has been shown to evolve faster in island anoles. When it comes to morphology and physiology on islands, it seems we are looking at different sides of the same coin. The same ecological release from predators and competition that allowed for the truly impressive amount of morphological diversification that has appeared quickly among island anoles, seems to additionally allow for more behavioral thermoregulation which slows physiological evolution.

“We are discovering that organisms are the architects of their own selective environments,” says Muñoz, “meaning that behavior and evolution are locked together in a delicate dance. This pas de deux tells us something important about how diversity arises in nature.”

Jhan Salazar holds an anole from Colombia.

 

Concrete Escape: Increased Wariness of Anoles when Escaping from Cement Walls

 

Fig. 1. Anoles perched on various manmade surfaces 

Lizards in the city are everywhere! Often you see them on buildings, statues, benches and other objects (Fig 1). These manmade structures are very different from natural substrates and thus might affect their locomotor ability and escape responses. This observation led me to develop questions around how lizards respond to incoming threats when using these artificial structures. I am very grateful that I got to “get my feet wet” tackling some of these questions during my master’s degree as a member of the Kolbe Lab in the University of Rhode Island.

In our recent paper, we contrasted the escape response of Anolis cristatellus in forests versus cities, and within the latter, between lizards perched on natural versus manmade surfaces. We selected this question because we believed that the heterogeneity of habitat structure in the city might influence the decision-making of flight responses. When a predator approaches, an animal should flee when the costs of staying outweigh the energetic costs of fleeing. Consequently, we hypothesized that the cost of flight varies when the animal is perched on smooth surfaces. However, we expected that city lizards should have reduced flight responses largely influenced by habituation to humans.

The bad habits of habituation

One of the major hurdles involved designing our project to separate the component of behavioral adjustments to humans versus structural habitat differences when contrasting escape responses. The literature often has used the concept of habituation as a discussion point when contrasting flight responses of habitats that differ in human activity. Only a few studies have attempted to quantify how human activity might influence escape responses. We explored this concept by sampling lizards perched on trees at edges of a forest trail or sidewalk that were frequently visited by pedestrians and cyclers. Lizards perched closest to the trail or sidewalk should be more exposed to human activity and respond with reduced flight initiation distance. We found that forest lizards perched at the edge of the trail had shorter flight initiation distances (Fig. 2). Lizards perched 4m away from the trail had longer flight responses. In contrast, city lizards sampled at trees along a sidewalk showed no difference in flight response with increasing distance from the sidewalk. With this, we were able to show how habituation influenced escape responses, possibly driven by the degree lizards were able to see human activity. At 4m from the forest trail, we had very limited visibility of the trail. In contrast, in the sidewalk at 8m away from the sidewalk, we could see the sidewalk, the road and the sidewalk at the other side of the road. However, more work specifically directed to tackle the concept of habituation is needed to understand its role in facilitating the successful colonization of urban habitats.

Fig. 2. Log flight initiation distance of lizards sampled with increasing distance away from a trail in the forest or a sidewalk in the city.

The wall

City lizards were abundantly using cement and metal structures. For this reason, we compared escape responses of forest lizards on trees to city lizards on cement, metal and trees. Most of the cement structures were large buildings, whereas metal often included fence posts and light fixtures. Both metal and cement are smoother than bark and greatly reduce stability during locomotion. When lizards run vertically on smooth surfaces, they are more likely to slip and fall. We hypothesized that such locomotor constraints should increase the cost of flight and thus lizards on manmade surfaces should have longer flight initiation distances. We found that forest lizards had the longest flight initiation distance (Fig 3). Surprisingly, we found that there was no difference in flight response between city lizards perched on trees and those on metal posts. Metal perches were often cylindrical and lizards could circle around the perch, breaking away from the line of sight. In contrast, cement walls were often long and required lizards to either slowly move up and out of reach or sprint longer distances to circle towards the next connecting wall. The ability to quickly hide with a short burst of movement decreased the cost of flight on metal posts.

Fig. 3. Flight initiation distance of forest anoles perch on trees and urban anoles perched on trees, metal posts and cement walls.

Escape in the city

We found that even though sprinting performance is lower on artificial perches, lizards often perch on these surfaces. It’s likely that behavioral modulation plays a role in increasing their success in evaluating predation risk when using these perches. If I were to continue this study, I would track individual lizards to contrast their response when perching on the various natural and man-made surfaces. Additionally, multiple tests on marked individuals would allow for a more appropriate test of habituation across these populations.

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