SICB 2019: Anole Setal Morphological Diversity

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On January 7, 2019

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An anole toepad imaged with a scanning electron microscope.

In the endless comparison between the adhesive systems of geckos and anoles, today we learned a bit more about anole toe pads. University of Akron grad student Austin Garner, from the Peter Niewiarowski and Ali Dhinojwala labs, presented a poster on setal morphology across the toe of Anolis (Deiroptyx) equestris or the Cuban Knight anole. Like a lot of studies on toe pads, the inspiration for this work can be traced back to a previous study by Tony Russell (Johnson and Russell. 2009. Journal of Anatomy). In their 2009 study, Johnson and Russell found that the more distal lamellae of Rhoptropus geckos were more narrow and that their distal setae were longer, lower in diameter, and more densely packed within and across lamellae. This study came to shape our knowledge of within-toe gecko setal morphology.

Today Garner presented preliminary data evaluating the same patterns in an anole. Although their numbers are very preliminary (N=2), it suggests some interesting deviations from Rhoptropus. The more distal lamellae of equestris are narrower, similar to Rhoptropus. Distal setae are also more densely packed, but setae seem to be the longest and have the widest diameter in the middle of the lamellae, and in the middle of the toe, which is very different than what was observed in Rhoptropus. 

If this pattern holds as Garner et al. increase their sample size, it will have interesting implications for how we think about toe detachment in geckos and anoles and well as how the two groups navigate rough and smooth surfaces. I am really excited to see what patterns emerge from the study and so stay tuned to see how their results shake out!

SICB 2019: The Life and Death of an Extralimital Population of Invasive Brown Anoles

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On January 6, 2019

In New Research

Brown anoles are invasive throughout the southeastern United States and are often transported via the nursery trade.

As invasive species expand across landscapes, they may engage in new interactions including with native competitors and prey as well as encountering novel environmental conditions such as different temperatures or patterns of rainfall. It is often difficult to observe the process of how invasive species which are dispersing across landscapes are affected by these novel conditions, because it may be difficult to find edge populations of invaders, and those extralimital populations which do not survive may have disappeared before scientists can observe them.

In southern Florida, many anole species have been introduced and are expanding their ranges, perhaps none more prolifically so than the brown anole (Anolis sagrei). In the past 75 years or so, brown anoles have occupied all of peninsular Florida, the eastern seaboard of Georgia, and Gulf Coast habitats through Louisiana. Many of these expansions are thought to occur via hitchhikers on cars or via the nursery trade, in which potted plants with adults or eggs are transported to new areas. These introductions may fail for many reasons (e.g., inhospitable environments, low numbers of colonizers, intentional extirpation by humans), but these processes of dispersal, establishment, and extirpation are difficult to study. Dan Warner, a professor at Auburn University, took advantage of a known extralimital population of brown anoles in a greenhouse in central Alabama to study the survival of a population created through this type of dispersal.

This population of anoles existed well north of its continuous invasive range in the United States and was exposed to much colder winter conditions than other studied populations.  It was present at the greenhouse from at least 2006, and so survived for at least 10 generations, long enough for adaptation to these novel thermal conditions to potentially occur. Working with a team of undergraduates, graduate students, and post-docs, Dan assessed the thermal conditions in the greenhouse environment, conducted mark-recapture studies of the population, and measured thermal tolerances of lizards.

Dr. Amélie Fargevieille and Jenna Pruett representing the Warner Lab at SICB 2019.

At SICB 2019, Dr. Amélie Fargevieille and Jenna Pruett presented results from the study, showing that the greenhouse population included all life stages of lizards and reached a total size of >1000 individuals. While one might expect that these northern lizards would have altered critical thermal limits, the Warner lab showed that both the upper and lower thermal limits of these lizards (the temperatures at which their movements became uncoordinated), were the same as those found in lizards from warmer, southern populations. These results indicate that existence in a colder northern climate for >10 years did not lead to adaptive changes in thermal limits, perhaps due to the population occupying a thermally-buffered habitat, i.e., the greenhouse.

While hurricanes have facilitated several fascinating studies of anole adaptation (e.g., Schoener et al., 2017, Donihue et al., 2018), they may also take these opportunities away. In the case of this population, Hurricane Irma blew off the greenhouse roof in 2017 (which remained unrepaired), exposing this population to the rigors of a central Alabama winter. Multiple surveys in 2018 confirmed that there were no survivors of this previously robust population. Dataloggers confirmed that, even in the most sheltered microhabitats that remained, temperatures dropped below the critical thermal minima of brown anoles, presumably extirpating the entire population.

Recent Extinction of a Viable Tropical Lizard Population from a Temperate Area WARNER, DA*; HALL, JM; HULBERT, A; TIATRAGUL, S; PRUETT, J; MITCHELL, TS; Auburn University.

SICB 2019: Mitochondria Effects on Endurance and Metabolic Rate

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On January 6, 2019

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Animals have to perform a lot of complex tasks within their environment in order to reproduce and survive. To perform these tasks, animals often rely on their ability to move throughout their environment, and animals that do this often are often better fit within their environment. That’s why exercise is so important, ladies and gentlemen! Frequent exercise will increase your ability to run fast or run far, but it often comes at a cost. For one, increased exercise response is met with a reduction in your ability to fight an infection (i.e. immunocompetence) or reproduce.

To further understand the effects of exercise on animals in general, Kara Reardon, a student of Jerry Husak’s at the University of St. Thomas, devised an experiment to understand how increases in cellular mitochondria (the powerhouse of the cell!) influence performance after endurance training. They provided green anoles (Anolis carolinensis) with pyrroloquinoline quinone (PQQ) a training supplement to artificially increase their mitochondria production and found that PQQ (and a higher level of mitochondria) didn’t necessarily influence endurance capacity directly, but found that it lowered metabolic rates in their lizards. They also found that muscle metabolism was not affected by training, but that exercise overall increased the performance capacities of green anoles. Next up, they are going to quantify the genes involved in their observed endurance enhancements in these anoles. Great stuff from Reardon and Husak!

SICB 2019: Impacts of Artificial Light at Night on Brown Anoles

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On January 6, 2019

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As I’m sure we are all aware, humans are causing a lot of significant changes to their surrounding environments. These changes can include habitat loss or fragmentation or urbanization just to name a few. However, one novel component of anthropogenic change is the introduction of artificial light into ecosystems that were otherwise dark. Artificial light at night (ALAN) is a new pressure that many organisms haven’t necessarily dealt with before humans rose to industrial fame. The impacts of ALAN on species across the globe is something more people are realizing can be severe and harmful to populations of wild animals. ALAN is capable of altering many important ecological factors for species, including their susceptibility to predation, access to food, sleep, hormones, and reproduction.

Chris Thawley, an NSF postdoctoral researcher in the lab of Jason Kolbe at the University of Rhode Island, devised a field experiment to test for the impacts of ALAN on brown anoles (Anolis sagrei) from southern Florida. Previously, Thawley and colleagues found in the lab that ALAN increases growth in female brown anoles and causes them to initiate egg-laying earlier, thereby increasing their reproductive output. But in this study, they aimed to quantify how ALAN affects anoles in the field, to further ground-truth their laboratory results.

Thawley and colleagues traveled to southern Florida, marked over 200 individual brown anoles with individual beads, and monitored their sensitivity and orientation to ALAN. They found that anoles are exposed to a significant amount of ALAN at their sleeping perches, but that anoles didn’t necessarily exhibit behavioral avoidance of ALAN. They also performed physiological analyses and found that ALAN reduced plasma glucose (a good proxy for energy availability) in the bloodstream of these lizards by approximately 10%, a huge energetic cost for these lizards. Thawley and colleagues plan to continue adding individual lizards to their already impressive dataset to provide a holistic story, including ecological, behavioral, physiological costs of ALAN on these brown anoles. Stay tuned!!

SICB 2019: Do Bark Anoles Show Behavioral Syndromes?

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On January 5, 2019

In New Research

Daisy Horr, an undergraduate researcher at Trinity University, discusses how bark anole behavior varies across several different social contexts.

Animals often use diverse behavioral repertoires to adjust to new, unexpected, or changing conditions very quickly. While it may seem like individuals could always use the best behavior for any given situation, we know that instead behaviors are often related within an individual. In other words, an individual’s behaviors are not always independent and may represent an underlying “behavioral syndrome” or correlated set of behavioral responses to related environmental conditions. These behavioral syndromes are also sometimes called “personalities” (though application of this word to animals can be a bit controversial!). So, for instance, an individual that has a “bold” behavioral syndrome might take little time to explore a new habitat or consume a novel food item more quickly, but also be more likely to stay active in the presence of a predator rather than hiding (the safer option!).

While anoles have been the focus of much behavioral research, we still lack an  understanding of the diverse behavioral phenotypes, including behavioral syndromes, which are displayed by a variety of anole species. The bark anole, Anolis distichus, is native to Hispaniola but also found in southern Florida where it has been introduced. While small, bark anoles can be quite feisty, and are known for their dramatic display behavior in the presence of male and female conspecifics.

Male bark anoles demonstrate pushup displays prior to engaging in combat.

Taking advantage of the bark anole’s willingness to put on a show, Daisy Horr, an undergraduate student and McNair Scholar in Michele Johnson’s lab at Trinity University, led a group of fellow researchers in assessing whether these anoles show behavioral syndromes. To do this, Daisy and her collaborators measured the degree to which male bark anole behaviors were repeatable across three different contexts: trials with another male present, trials with a female present, and solo trials in which no other anoles were present. They measured variables quantifying movement as well as display behaviors such as pushups and dewlap extensions during these trials. The team also wanted to see whether the measured behavioral traits were linked to morphological and physiological variables.

Daisy and colleagues found no support for the idea that behavior was linked to morphology, including size of the body, head, and dewlap, and mass of the whole body, the liver, and fat pads (structures holding fat as energy reserves), or the hematocrit of the lizards, a metric quantifying how many red cells are present in the blood. Bark anoles did show some level of behavioral consistency, however. Movement behaviors were quite repeatable even between trials with and without conspecifics. Display behaviors, however, including pushups and displays, were repeatable within, but not across contexts. This work suggests that bark anoles have consistent behavioral syndromes in some contexts. Looking forward, research into behavioral syndromes in anoles could offer insights into how behavior may vary with habitat use, ability to invade novel environments, or selection on behavior itself!

SICB 2019: Sexual Differences in Relative Lengths of Toes

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On January 5, 2019

In New Research

Today I had the pleasure of attending an excellent talk by University of Florida undergraduate Griffin McNamara. I was really impressed with the work he presented, especially for an undergraduate.

McNamara was investigating the ratio in digit length between the 2nd and 4th digits. This is interesting because in mammals, especially humans, this ratio is sex specific, with men typically having longer ring fingers than pointer fingers. A lot of research has looked into the developmental reasons for this, with a likely relationship to hormone exposure of the developing fetus. Applying these ideas to anoles makes sense because the toe of anoles are somewhat unique in lizards, as we all know here. McNamara is looking into if sexual dimorphism in 2nd and 4th digit length was also present for anoles.

McNamara wasn’t the first person to measure this in anoles, but he was the first to use cleared and stained specimens, which likely greatly improved his ability to accurately measure digit length. Interestingly, he found that the pattern was reversed, with males having longer 2nd digits, not longer 4th digits as in mammals. In addition, this pattern didn’t show up until a lizard’s teenage years, with juvenile anoles not showing a difference between the sexes. Using cell staining to visualize dividing cells, he was able to narrow down the digit discrepancy to growth in the 2nd phalanx during sexual maturity.

Suspecting that this late onset dimorphism might still be related to hormone exposure, McNamara got his fingers on some testosterone-treated female anoles from collaborators and found that they had “masculinized” digit ratios, although not as much as true males.

I thought this was a great study, combining old school cleared-and-stained approaches with cell biology and experimental endocrinology. It also opens up lots of interesting questions. Is there an adaptive reason that mammals and lizards have sexually dimorphic digit lengths? Is it just a quirk of development? Does this digit length reversal have anything to do with the fact that the shape of anoles’ rear feet is already kind of mirrored as compared to our hands?

Advances in Herpetology and Evolutionary Biology: Essays in Honor of Ernest E. Williams Available Online

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On January 3, 2019

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I don’t know how long this has been the case, but you can download it, or chapters within it, at the Biodiversity Heritage Library.

Enormous Growths/Endolymphatic Sacs on the Neck of a Green Anole

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On December 31, 2018

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Can anyone advise our correspondent in North Carolina who writes about the anole above with enormous growths that may be endolympathic sacs out of control:

Maybe you have some ideas about this growth, which I originally thought were calcium storage seen in anoles, but this just looks like it is going to pop any second.  I bred this girl about 2.5 years ago and she usually lives with my boss unless he goes on vacation, which is when I take care of her.  I also still have her Dad and sister (long story and I’ll never do it again!).  I let the other eight (!) babies that I raised and Mom, who was used to the wild, go.  This girl has always been very hyper and green all the time and has laid a bunch of eggs this past spring and started getting these pockets (thought calcium).  But now the one side is sooo big!  She gets almost the same care as my two (Dad and sister), except maybe a little less sunlight (mine are at a window).  I was worried it is an abscess or parasite or something.  I asked someone at the NCSU vet school and he wasn’t sure.  Oh, she hasn’t been eating well, either, the last few days.

Attached is the photo of her and also a fun one for Christmas that was part of our Christmas card.  We rescued Dad out of a spider web when he was maybe a few days old.  He was dragging his hindlegs, but then regained his strength a few weeks later and we couldn’t let him go at that point.  The lady he made the other 10 babies with is a different story.  My husband found her inside our house and I told him to let her go, but instead he put her in with “Gimpy.”  They had sex the same night :).

The Life of Ernest E. Williams

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On December 30, 2018

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For some reason, this obituary of Ernest Williams is going around the internet again, 9+ years after it was published in the Harvard Gazette.

Ernest Edward Williams

Faculty of Arts and Sciences — Memorial Minute

At a Meeting of the Faculty of Arts and Sciences on May 19, 2009, the following Minute was placed upon the records.

Ernest Williams was a man of many contrasts. Biology at Harvard in the third quarter of the last century was full of outsized personalities—titans in the field with strong opinions and no reservations about expressing them. In such company, Williams appeared a wallflower, seemingly wishing to be anywhere but in the midst of their arguments. Yet, one-on-one, Williams had an incisive wit and a dry sarcasm—discussions with him were always stimulating and provocative as he never missed a chance to challenge one’s thinking, sometimes quite pointedly.

To some, Williams’s work came across as old-fashioned. His subject, systematics — the study of the evolutionary relationships of species—is among the oldest in science, and his papers — florid and opinionated and, above all, long—recalled an approach to scholarship no longer in vogue. Yet much of his work was boldly innovative; some papers are still widely cited, and in several cases his work was well ahead of its time, presaging approaches to the study of evolutionary biology that were not to catch on for several decades.

Ernest Edward Williams was born January 7, 1914, in Easton, Pennsylvania, the only child of middle-aged parents. Like many boys, particularly of that time, he grew up loving nature and spent many hours capturing salamanders and other creatures. After attending Lafayette College, Williams joined the Army, serving in Europe during World War II. Upon his return, Williams entered graduate school at Columbia University, where he was the last graduate student of the great anatomist William King Gregory.

Williams’s doctoral thesis focused on the structure of the neck vertebrae of turtles and how variation among species reflects their evolutionary heritage. The work demonstrated the combination of careful attention to detail with the ability to interpret results in the broader context that was to characterize Williams’s career. More than fifty years later the work is still foundational in understanding the evolution of turtle diversity.

In 1950, after completing his degree, Williams moved to Harvard, where he initially served as a laboratory coordinator for the anatomy course of the legendary paleontologist Alfred Sherwood Romer, then subsequently was appointed as an assistant professor and made coordinator of a General Education course on evolution. The Museum of Comparative Zoology’s Curator of Herpetology, Arthur Loveridge, retired in 1957, and Williams was appointed to take his place.  In 1970 Williams rose to the rank of professor and in 1972 became Alexander Agassiz Professor of Zoology.

Williams initially focused on continuing his work on turtle systematics, leading to a series of publications including a still-important treatise published with Loveridge in 1957. Williams soon realized, however, that the museum’s collections were inadequate for the detailed analysis he conceived, which required large samples from many populations. This recognition that the museum’s herpetological collections were wide in scope, but lacking in depth, led Williams in two directions. First, it compelled him to work greatly to expand the Herpetology Department’s holdings, ultimately leading to a quadrupling of the department’s collections (to more than 300,000 specimens) by the time he retired as curator in 1980, making the Museum of Comparative Zoology (MCZ) one of the greatest herpetological repositories in the world. Second, it led Williams’s attention to focus on lizards in the genus Anolis, a very species-rich group from the Caribbean and Central and South America. A previous curator of herpetology and director of the MCZ, Thomas Barbour, had extensively collected anoles in the Caribbean; Williams, whose focus was much more evolutionarily-oriented than most systematists of the day, recognized that this group could be a model for studying large-scale evolutionary and biogeographical phenomena.

And, indeed, they were, and still are. Williams recognized that anoles have diversified for the most part independently on each of the major islands of the Caribbean (Cuba, Hispaniola, Jamaica, and Puerto Rico); most remarkably, the end-result of these evolutionary radiations has been very similar, with the same set of habitat specialists — which Williams labeled “ecomorphs,” a term now widely employed in evolutionary biology — evolving independently on each island. Such convergence of entire faunas is a rare phenomenon and Anolis has become a textbook example.

Williams’s work on anole evolution synthesized a wide variety of fields, including biogeography, functional morphology, population genetics, behavior, and ecology. Yet, Williams was a systematist by training, with little background in most of these areas. The primary means by which Williams orchestrated this broad-based investigation of anole diversity was his ability to identify the best organismally minded graduate students in Harvard’s biology department, regardless of their specific interests. As a result, the list of Williams’s graduate students reads like a Who’s Who in ecology and evolutionary biology.

At a time when the MCZ’s curators had little say in curricular matters, Williams pioneered a highly popular course on vertebrate biology. This course, which Williams taught for many years, helped keep organismal biology alive at Harvard and was a crucial step in the creation of the Department of Organismic and Evolutionary Biology (OEB).

Williams was not the most gentle-hearted of advisors. Gruff and very critical, he had high standards, expected students and colleagues to meet them, and was not shy about letting them know when they had not. Words of praise were not handed out liberally, but were cherished when received. With undergraduates, however, Williams showed a different side, being supportive and encouraging when needed and available at any time for discussion and advice. A number of Harvard undergraduates who worked with him have gone on to become evolutionary biologists, and several have continued to work on anoles, in many cases following up on ideas he initially conceived.

Williams remained active after his retirement from the Harvard faculty in 1984, continuing his evolutionary and systematic studies. Eventually, he moved back to his native Pennsylvania, where he died in 1998, taking his encyclopedic font of knowledge with him. Nonetheless, his spirit and ideas live on in the form of his many academic descendants, which include many prominent active scientists, several members of the U.S. National Academy of Sciences, a high-ranking U.S. government official, and the current curator of herpetology of the MCZ.

Respectfully submitted,

A. W. Crompton
Karel F. Liem
Jonathan Losos, Chair

Laws of the Lizard Premieres on the Smithsonian Channel Next Week

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On December 22, 2018

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More information on Laws of the Lizard here.

The documentary, by Days Edge Productions, is all about anoles and the scientists who study them. Accompanying the  film is a 7-part series of short webisodes, The Lizard’s Tale. Here’s the first one:

 

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