SICB 2019: Crocodile Rocking (Different Snout Lengths) Is Something Shocking

Zachary Morris presents his research entitled “The role of craniofacial growth zones in shaping crocodylian snouts.”

Evolution of the crocodylian skull is driven by developmental changes. While embryos share many similarities, at some point within development they diverge into unique ecomorphs. Prior studies in American alligators (Alligator mississippiensis) showed that the snout is a source for early facial proliferation, wherein later stages lack growth plates that resemble post-hatching anole lizards. Snouts of crocodilians are described as moderate, blunt, and slender. Snout structure is related to dietary and ecological differences; for example, long, slender snouted crocodiles such as the Tomistoma (Tomistoma schlegelii) feed largely on fish. Heterochrony of slender-snouted crocodiles is responsible for continued elongation of the embryonic snout.

Zachary Morris of Harvard University following his great talk at SICB 2019.

To further understand forces behind these developmental changes, Zachary Morris, a current PhD student of Dr. Stephanie Pierce at Harvard University, began by asking the questions “When does this difference (in skulls) become apparent?” and “What are the cellular dynamics of snout elongation?” He presented his work on Saturday at the 2019 SICB conference and shared his experimental approach to answering such questions. To do this, he traveled to Imperial College London to work with Dr. Arkhat Abzhanov.

In answering his initial question, Morris incubated A. mississippiensis, dwarf crocodile (Osteolaemus tetraspis), and T. schlegelii embryos to developmental stages 14 and 17. These time-points were selected based on Ferguson staging. He could then examine snout/head length ratios to determine when skull differences, such as elongation, became apparent. At stage 14, no differences among blunt, moderate, or slender-snouted crocodilians were visible. However, at stage 17, he found that slender elongation began. To investigate his latter question, he followed the same procedure, but was able to calculate cell proliferation rate for tissue regions utilizing injection of EdU in ovo. He found that while elongation patterns such as facial shape were apparent during stage 17, early cell proliferation rate at the same stage was not apparent. His findings suggest that blunt species types (such as O. tetraspis) have decreased cell proliferation along the tip of the snout in comparison to slender species types (such as T. schlegelii).

In the future, Morris hopes to investigate whether cell proliferation at the tip of the snout is maintained in Tomistoma and if there is greater proliferation at lateral edges of facial structures in broader-snouted crocodilians. While these modern-day dinosaurs derived species-specific morphological differences from actual dinosaurs, the evolutionary processes by which these occurred remains the target of Zachary Morris’ interesting and exciting research.

SICB 2019: Is the Exercise Response Adaptive?

We tend to think of exercise as a human activity–training our bodies in specific way to accomplish tasks, maintain strength and endurance, and live a healthier lifestyle. Wild animals exercise just as often if not more than humans, but the benefits to animal exercise have been somewhat contentious in biology. The responses to organismal exercise are very conserved with respect to evolutionary change and speciation. Those responses include an increase in performance capacity (such as speed or endurance), but often times trades-off with some other physiological trait, such as immunocompetence. With this trade-off looming, one outstanding question remains: does the exercise response enhance reproductive success and survival? Can we call this response “adaptive”?

To test this idea, Jerry Husak from the University of St. Thomas and his co-author, Simon Lailvaux at the University of New Orleans, measured the exercise response in 90 green anoles (Anolis carolinensis). They had 30 control lizards, 30 lizards trained with speed trials, and 30 lizards trained with endurance trials. They found that overall, exercise enhanced performance for all lizards relative to the controls, but training decreased the ability of a lizard to fight off an infection. They found that lizards that had been trained did not exhibit increases in movement rates, and also found that over time, trained lizards exhibited decreased survival relative to the controls! Is exercise actually bad for lizards?! Green anoles were twice as likely to survive when they were not trained, and differences in lizard body condition might be intimately linked with their probability of survival. Husak and Lailvaux are going to continue to test the idea that the exercise response confers some benefit to lizards outside of performance. Stay tuned!

SICB 2019: Sex-Biased Gene expression in Brown Anoles

Members of the same species share a common genome, the same set of genes and regulatory networks that build the proteins responsible for phenotypic diversity. However, that means that both of the sexes share a common genome, and that is an issue when males of a species are sensitive to their own environmental stimuli, and when females are required to invest a lot of their energy towards reproduction and rearing offspring. Species are often sexually dimorphic as well, where either the male or the female will be larger than their inter-sex counterpart, and this has to do with what ecological tasks each sex is responsible for. Do you have to defend a territory? You better be big! Do you want to create a lot of high-quality offspring? You better not invest that much energy into your own growth! It’s an interesting question in biology today: what happens genetically when a sexually-dimorphic species develops to adulthood?

To answer this question Albert Chung, a graduate student at Georgia Southern University, and his colleagues Robert Cox and Christian Cox designed an experiment to quantify changes in gene regulation in brown anoles throughout ontogeny and quantify how changes in gene regulation produce sexual dimorphism. They quantified gene expression at four different time points until adulthood across three different tissue types (brain, liver, and muscle) using RNA sequencing (RNAseq). Chung and colleagues found that sex-biased gene expression exhibits age specificity, with different age classes exhibiting different patterns of sexual dimorphism in gene expression. They also found that the number of sex-biased genes increases throughout development, important for a species to be able to develop both a larger sex and a smaller sex. In addition, sex-biased gene expression also varies among the different tissue types, with the liver exhibiting an increase in sex-biased genes throughout development, potentially to increase growth in male brown anoles compared to females! Chung spoke in the Raymond Huey Best Student Paper Award session for the Division of Ecology and Evolution and delivered a fantastic presentation. We look forward to learning more about the development of sexual dimorphism (especially in anoles!) from Albert and his co-authors.

SICB 2019: The Effect of Sinusoidal and Fluctuating Developmental Temperatures on Anole Embryos

Ectotherms such as lizards often take extreme care when it comes to laying their eggs. Eggs are incredibly sensitive! When female lizards don’t retain their eggs and give live births (we call this viviparous), female lizards will seek out the perfect temperature and moisture conditions for her eggs to develop and hatch. Oftentimes, when researchers use anoles in the laboratory for a variety of experiments, they incubate eggs at the temperature that these eggs experience in their natural environment. However, many studies only use a constant, mean temperature, rather than using a more realistic diel cycle of fluctuating temperatures over time. However, does that matter at all? It’s an important question for a variety of anole biologists that raise eggs to hatching: does the thermal regime of your incubator matter when it comes to offspring phenotype?

Josh Hall, a Ph.D. student at Auburn University under Dan Warner, set out to address just that question! He raised brown anole eggs in one of four distinct thermal treatments: a constant temperature, a repeated sinusoidal (sine wave) fluctuating temperature, a fluctuating temperature parameterized by the mean daily fluctuations these lizards experience in the field, and natural environmental conditions. He did this for both a cool developmental temperature (reflecting eggs developing earlier in the reproductive season) and a warmer developmental temperature (reflecting eggs developing later in the reproductive season). Even Josh didn’t recommend doing so many treatments! However, the amount of work that went into these treatments is impressive.

Hall and Warner found that natural temperature treatments increased the developmental rate of brown anole eggs only at cooler temperatures, and actually decreased the developmental rate at warmer temperatures. They didn’t find any other effects of any treatment on egg phenotypes. They also found that natural temperature treatments increased the endurance of hatchlings compared to the constant temperature treatment  at cooler temperatures. I was really struck by this study: it seems really obvious that eggs would do better in the lab when developed at temperatures that they experience in the field, but an experiment like this is so rarely performed because it requires so much intensive care and work! Can’t wait to hear more about how different developmental conditions affect anoles from Hall and Warner!

SICB 2019: Does a Tropical Anole Evolve When Colonizing a Novel Habitat?

Anolis apletophallus from Panama, a well-studied species from the Panama mainland.

Over the past 15 to 20 years, the study of evolution has undergone something of a paradigm shift. Whereas scientists used to believe that evolution in most animals was a slow process, only observable over longer timescales, we now know that evolution is fast. Meaningful change can occur in many types of traits, including morphology and physiology, in just a handful of generations of a given organism. With this shift in our understanding, many biologists have begun conducting experiments which attempt to observe evolutionary processes in action, and shed light on how evolutionary mechanisms play out in the real world.

Dan Nicholson, a student in Rob Knell’s lab at Queen Mary University of London, worked with Mike Logan and a team of researchers to do just this in a tropical anole, Anolis apletophallus. Dan and his colleagues caught over 400 individual anoles from the mainland and introduced them to a novel environment: four small, anole-free islands formed when the Panama Canal was created. Two of these islands were similar to mainland habitats, while two had wider types of vegetation. Prior to placement on these islands, Dan measured a suite of characters of these individuals, including perch height, size, leg length, head, and toe morphology, enabling him to observe any changes in the distribution of these traits over time.

After leaving the anoles on their new tropical island homes for a year, Dan returned to recapture the survivors and measure both them and their offspring. By comparing the traits of the surviving lizards and their young with those of the population founders, Dan could observe changes in traits as well as measure natural selection on them. At SICB 2019, Dan reported that he found that anoles on islands with wider vegetation did indeed use these broader perches and that anoles also perched closer to the ground. Correspondingly, he found that toe pad size decreased and that hindlimb lengths were longer on some islands, potentially allowing lizards to better exploit lower, broader perches. 

Anoles on all islands also showed a reduction in head depth. The reason is unclear, but Dan is looking into whether differences in competition or the prey community are potentially driving this pattern. Finally, measuring selection was very difficult and analyses proved problematic, though in some cases selection estimates do seem to match with observed changes in morphological characters. Dan and his team are hoping that adding data from another generation of anoles will clarify these effects, so stay tuned!

Keep track of the latest from Dan on Twitter: @DanJNicholson

Natural Selection on Morphology in a Tropical Lizard After a Rapid Shift in Habitat Structure NICHOLSON, DJ*; LOGAN, ML; COX, C; CHUNG, A; DEGON, Z; DUBOIS, M; NEEL, L; CURLIS, JD; MCMILLAN, WO; GARNER, T; KNELL, RJ; Queen Mary University London

SICB 2019: Anole Setal Morphological Diversity

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

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

 

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

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?

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!

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