Category: New Research Page 20 of 67

Evolution 2016: Polar Vortex Revisited

Shane Campbell-Staton giving his talk at Evolution 2016

Shane Campbell-Staton giving his talk at Evolution 2016

We’ve heard about the effects of polar vortexes here on Anole Annals before. The infamous 2013/2014 event brought record-breaking snow and low temperatures to the Southern U.S., leaving people and animals both a little chilled. This created the perfect opportunity for Shane Campbell-Staton to investigate the effects of such extreme events on thermal tolerance of the native Carolina Anole, Anolis carolinensis. Shane also spoke about this at SICB earlier this year, and AA contributor Martha Muñoz covered the talk pretty thoroughly here on Anole Annals. Nevertheless, I’ll summarize some key points here in case you missed it.

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An unlucky lizard during the polar vortex snow storms in the South.

Shane got lucky in the sense that he had measured thermal tolerance in August 2013 for populations affected by the polar vortex, 5 months before the event. Typically, the cold arctic air is tightly constrained around the North pole, but periodically the boundaries weaken and the cool air expands southward. These events are not regular, so Shane had no idea one was coming that winter or that it would extend so far south. It was serendipitous that his study populations, 3 in Texas and 1 in Oklahoma, were impacted by the extreme weather event. This species, particularly in the Southern portion of its range, is not used to low temperatures and reports came in of anoles dying off during the storm.

Air temperatures for January 5-7, 2014, compared to the 1981-2010 average. Map by NOAA Climate.gov

So Shane returned in August of 2014 and sampled again, curious as to how this cold impacted thermal tolerance. He found that tolerance to low temperatures, measured as critical thermal minimum (CTmin), was lower in some populations after the event! Even more, the difference was greatest in the Southernmost population (Brownsville, Texas). Shane returned again in the fall of 2014 to see if this effect persisted or if it was simply a plastic response to the event. He found that the populations sampled in 2014, and presumably their offspring, still had lower critical thermal minimums. This result suggests that the extreme cold weather had caused an evolutionary shift in cold tolerance via natural selection: only the animals that could tolerate the cold temperatures survived and passed on their cold-tolerance genes. Shane went on to conduct a common garden study to verify that the trait was not simply a plastic response. He found that the lower CTmin persisted in lab-reared animals: strong evidence that these shifts had a genetic basis.

Lastly, Shane looked at the functional genomics of cold tolerance. Using liver tissues to obtain transcriptomes (representing expressed genes), he found several gene modules associated with thermal tolerance including some associated with respiratory electron transport chain, lipid metabolism, carbohydrate metabolism, and angiogenesis/blood coagulation. He also found that the gene expression patterns in the Southern populations affected by the storm resembled the Northern populations that more regularly experience cool temperatures, indicating a common genetically based adaptive response across populations.

Evolution 2016: Rapid Morphological Evolution in Urban Environments

IMG_2376We as a species are rapidly changing the global environment. The changes that get the most press are those related to climate, but we are also changing the structure of environments through land development. This leads to many important questions, one of which is whether or not the novel environments that we construct can drive evolutionary change. Kristin Winchell, a graduate student in Liam Revell’s lab at UMass Boston, has been addressing this question in the Puerto Rican lizard Anolis cristatellus, which is common in urban settings. Kristin hypothesized that urban environments should select for longer legs and greater surface area of lamellae (the morphological structures on anole toes that let them grip flat surfaces). Her reasoning was that long legs should allow animals to run faster, which should be beneficial in cities where perches and refuges are further apart than in dense natural forests. Greater surface area of lamellae should be beneficial for better grip of smooth man-made surfaces. Kristin compared morphological traits of multiple pairs of urban/natural environment populations and her hypotheses were supported. Not only that, but differences between populations were maintained in individuals developed under common garden conditions, consistent with a genetic basis of the differences. You can see these results in Kristin’s excellent recent paper in Evolution. Kristin also presented some new preliminary results that directly link the morphological changes she has observed to performance on man-made surfaces. Overall, Kristin’s work indicates that urban environments can be a potent force of rapid microevolutionary change and highlights that we are not only changing the abiotic landscape of the globe, but the evolutionary landscape as well.

Evolution 2016: Using Field Experiments to Understand Life-History Trade-Offs

Anolis sagrei. Photo by Alex Gunderson

Anolis sagrei. Photo by Alex Gunderson

The concept of trade-offs, that if you want to increase your performance in one function you have to decrease performance in another, is fundamental to ecology and evolution. However, detecting trade-offs and the underlying mechanisms that give rise to them is extremely difficult. In his talk, Bob Cox summarized years of research that he and his collaborators have done to understand life-history trade-offs in realistic ecological contexts using the brown anole (Anolis sagrei). Bob’s general approach is to experimentally manipulate the reproductive effort of individuals by removing ovaries and testes before releasing them onto cays in the Bahamas. He then estimates important ecological and physiological parameters such as survival, fat reserves, and immune function to see if he can detect trade-offs between reproductive effort and these other traits. In general, he has found that reproductive investment significantly decreases survival and physiological performance and that effects are often contingent upon factors such as the presence or absence of predators. Check out Bob’s website for a more information about his integration of experimental, ecological, and evolutionary studies to understand how trade-offs shape animal life-histories.

Evolution 2016: Using Anoles to Understand Shifts in Forests

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Ivan Prates presents his poster at Evolution 2016.

Here at Evolution 2016 there have been a lot of anole talks and posters. In fact, there have even been several that pretend to not actually be about anoles. Ivan Prates presented a poster which he insisted, despite multiple pictures of anoles and the use of anole DNA, was not actually about anoles… Instead, this poster was actually about the historical extent of Brazilian forest cover (or so he says).

In short, Ivan used genomic data to understand historical patterns of dispersion and distribution of South American anoles in order to infer patterns of rainforest expansion and contraction. He suspected that the geological data gave a false interpretation of rainforest patterns in Amazonia and the Atlantic Forest in Brazil, and that anoles could help tell the true story of how the forests have changed over time. By looking at species with strong genetic signals associated with forest shifts he hypothesized that true forest patterns could be elucidated based on the historical demography of these species.

Ivan and coauthors looked at three species of lizards: Anolis punctatusAnolis ortonii, and Polychrus marmoratus. They used the next-generation sequencing technique Genome by Sequencing (GBS) to answer three main questions: (1) Did all 3 species experience range expansions simultaneously? (2) Did populations expand and contract at similar points in time? (3) How did population sizes vary over time? While all three of these questions are about anoles, don’t forget that this poster was actually about the forest.

Ivan found that the Atlantic Forest individuals composed a monophyletic group nested within the Amazonian lineage. This suggests that the anoles of the Atlantic Forest on the coast actually arose from a single colonization event from Amazonia. The land between Amazonia and the Atlantic forest is presently quite arid compared to the rainforest – more like grassland. This presumably forms a barrier to contemporary dispersal, which implies that historical dispersal must have involved greater habitat connectivity. So Ivan’s results support the hypothesis that the forests experienced a drastic historical expansion creating a contiguous habitat that enabled dispersal around 1 million years ago. Interestingly, the timing for the dispersal of all 3 species was approximately the same. A million years ago seems to have been the ideal time to move to the coast for Brazilian anoles.

Ivan and his colleagues also looked at how populations size changed over time. He found that whereas Anolis punctatus experienced a trend of population expansion, Anolis ortonii and Polychrus marmoratus experienced population contractions. It was surprising to the authors that these species did not respond the same – why did only one of the species experience population expansions? They suspected that the expansion of one species might be related to the population contractions of the others, perhaps because of competition. However, their analysis on synchrony of population trends proved otherwise. They found that although trends within species were synchronized across populations, between species the shifts in demography were asynchronous. In other words, when one species expanded or contracted in population size, the others were stable. Ivan concluded that this was support for the idea that these populations were not influencing each other and that instead there was some other factor independently controlling population size fluctuations – perhaps precipitation patterns.

In conclusion, Ivan told me a lot about the demography of anoles during the Quaternary, and a little about the forest. I look forward to hearing more about his “forest” research on these understudied mainland anoles!

Click for a larger version of Ivan's poster!

Click for a larger version of Ivan’s poster!

Evolution 2016: Ecomorphology in Caribbean Eleutherodactylus Frogs

Common_CoquíStephen Jay Gould famously claimed that evolution is “utterly unpredictable and quite unrepeatable,” and we Anolis biologists have relished in proving that statement wrong. In his talk in Austin this week, Alejandro Gonzalez Voyer of UNAM (with coauthors Alvaro Dugo Cota and Carles Vilá) showed that anoles aren’t the only Caribbean herps to exhibit the independent, repeated evolution of ecomorphs across islands – Eleuthrodactylus frogs have joined the club!

Among the remarkably diverse Caribbean Eleuthrodactylus species, nine ecotypes exist, including terrestrial, leaf-litter, aquatic, riparian, bromelicolous, arboreal, fossorial, cavernicolous, and petricolous specialists. Gonzalez and his coauthors first determined that these ecotypes evolved repeatedly, and showed that their distribution resulted from both invasion across islands and intra-island speciation. They also found that eight of the nine ecotypes cluster in morphological space and exhibit significant convergence. (The ninth, the fossorial ecotype, is composed of a monophyletic clade from Hispaniola and so convergence could not be tested.)

In sum, it appears that Eleutrodactylus ecotypes are indeed ecomorphs, and that evolution may be utterly predictable and quite repeatable after all.

Evolution 2016: Genomic Insights into Anolis carolinensis Phylogeography

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Anoles, in particular Anolis carolinensis, have long been considered an ideal group for studies investigating thermal physiology, reproductive endocrinology, and even regeneration. With the recent publication of the A. carolinensis genome  (see AA posts on this here and here), the possibilities for new genomic studies in this new model species have significantly increased.

Joseph Manthey and co-authors used this new resource to clarify the phylogeographic relationships of A. carolinensis. Previous research on the phylogeography of A. carolinensis using both mitochondrial DNA and nuclear DNA showed that there were 5 clades. However, the relationships between these groups differed between the two approaches. Joseph looked at the genomes of 42 individuals from 26 localities across the native range to determine the true evolutionary relationship between regional groups and to shed light on the demographic histories of the groups. Manthey sequenced 500 loci using an anchored hybrid enrichment approach.

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STRUCTURE analysis showed that the clusters had little admixture

Manthey et al. found that the genomic data predicted 5 genetic groups, in agreement with both the nuclear and mitochondrial analyses previously done. Their results also indicated that the 5 genetic clusters were distinct with little admixture. However, the relationships between groups did not agree with either the mitochondrial or nuclear trees, yet all nodes had extremely high support (93-100%)

Finally, Manthey commented on the likely timing of this diversification and associated demographic trends. Their results indicate that the initial split occurred during the late Miocene or early Pliocene and that the remaining diversification occurred during the Pleistocene. They also found that the most Southern population had a significant number of fixed genes while other populations did not. This suggests that this group was likely the oldest and most stable and supports an “out of Florida” hypothesis of diversification.

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Evolution 2016: “Lightning” Strikes Three Times on Anoles in Afternoon Session: Character Displacement, Performance Trade-Offs and Opsin Evolution Matching Dewlap Color in Anoles

In this afternoon’s round of lightning talks, anoles were the focus of three fantastic (but short!) presentations on adaptation. It’s not easy to summarize a whole project in five minutes, but that’s just what these three speakers did, and each left me wanting to know more!

First, James Boyko, a Masters student working with Luke Mahler at the University of Toronto, described his work on morphological evolution in Lesser Antillean anoles.  When similar species compete over a shared resource, there are two possible outcomes: extinction or divergence (i.e., character displacement). Lesser Antillean anoles are an excellent system in which to study the role of character displacement, as these islands all have either one medium-sized species, or one large and one small species. Further, the species on these islands represent two colonization events – one from the north, and one from the south. James first confirmed the classic pattern on body size evolution, finding that a three peak Ornstein-Uhlenbeck model (i.e., one that predicted large and small lizards on two-species islands, and medium lizards on single-species islands) best fit the observed data (consistent with Butler and King 2004). But when he analyzed 20 other ecologically-significant morphological traits, this three peak model did not predict trait evolution better than a model based on random chance, although the northern and southern clades significantly differed in these morphologies. In summary, to understand the evolution of Lesser Antillean anoles: body size matters, as evolution in body size is clearly an important factor to reduce inter-species competition, but lineage matters too, as body shape was predicted by ancestry.

Next came Ann Cespedes, a Ph.D. student with Simon Lailvaux at the University of New Orleans. Ann is studying functional trade-offs in green anoles (Anolis carolinensis), focusing on relationships between fitness and performance. Many studies have searched for these trade-offs in the past, and some have found them, but others haven’t. Why the discrepancies? Ann proposed that previous studies haven’t always considered sex differences in functional trade-offs, that measuring only two traits (one associated with fitness and one with performance) may not reveal real trade-offs, and that differences in individual quality are often ignored. To consider all of these factors, she measured a suite of performance and morphological traits in 60 male and 60 female green anoles. Illustrating the limitations of examining raw data on sprint speed and endurance, Ann found no suggestion of the predicted trade-off between these traits. But when using a composite measure of all performance measures (sprint speed, bite force, clinging ability, exertion, endurance, jumping ability, and climbing ability) as a control for individual quality, the trade-off between speed and endurance became clear. Males and females also differed in their speed-endurance trade-offs, as body size predicted performance in different traits between the sexes, and body shape predicted male but not female performance. So performance trade-offs do exist, but you have to know how to look for them!

To conclude the session, Alexander Stubbs, a graduate student in Jimmy McGuire’s lab at the University of California, Berkeley, described the differences between opsin gene expression in two Cayman Island anoles: Anolis sagrei (a species with a red dewlap that reflects long wavelength radiation) and Anolis conspersus (a species with a blue dewlap that reflects short wavelength radiation). Alexander proposed that these different dewlap colors might provide different selective pressures on opsins in the two species to allow better color discrimination and angular resolution. Using RNAseq to measure mRNA in the eyes of six males of each species collected at solar noon or at sunset, the results were exciting. As predicted, Anolis conspersus had higher expression of opsins that increase visual sensitivity to UV, blue, and green wavelengths, and Anolis sagrei had higher expression of opsins that increase long wavelength sensitivity. Alexander also found that gene expression different substantially between noon and sunset, and further, there was surprisingly little variation in opsin expression between lizards, in stark contrast to the wildly varying opsin expression observed in humans.

Evolution 2016: It’s Getting Cold in Here!

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Tamara Fetters with her poster at Evolution 2016

Tamara Fetters, from the McGlothlin lab at Virginia Tech, reported on her ongoing work on thermal physiology in Anolis sagrei during the first poster session here at Evolution 2016 in Austin, Texas. Tamara looked at thermal tolerance and sprinting abilities at different temperatures and how that related to the latitude of the population. Specifically, she asked if lower temperatures regularly experienced by the Northern populations influence cold tolerance and performance at those temperatures. She expected that Anolis sagrei, native to Cuba and the Bahamas and introduced into the Southern U.S., would show signs of adaptation to its new, colder home in the more Northern mainland populations compared to the native range island populations in the South.

Tamara’s poster focused on two main experiments. In the first she calculated thermal tolerance to cold temperatures using a classic critical thermal minimum (CTmin) setup: with an ice bath she slowly lowered the body temperature of each animal until it was unable to right itself. This method approximates the minimum temperatures that the animals can handle in the wild. She found a clear trend showing a decrease in the minimum temperature tolerated as latitude increased. In short, Northern populations could handle the cold and Southern populations could not.

In the second experiment, Tamara acclimated the lizards to 6 temperatures ranging from 12-41 °C before running them up a track to calculate sprint speed. Tamara used an impressive 25-50 animals from each of 5 populations! She calculated sprint speed from the high-speed video she took using the program Kinovea. Tamara found that across all temperatures the most Southern population ran the slowest while the most Northern population ran the fastest, with the differences remaining fairly constant.

So what’s next for Tamara? She is planning on rearing animals in a common garden setup with some animals in hot temperatures with low variability between day and night (mimicking the native range, Southern habitats) and some animals in cool temperatures with high variability between day and night (as is experienced in the Northern habitats). She hopes that these studies will help her understand the genetic basis of this thermal tolerance and the extent of plasticity in thermal adaptation.

One last note – Tamara wanted to thank Anole Annals for helping her determine her study locations. She was able to determine which areas were likely to have Anolis sagrei and how far North they have spread because of Anole Annals posts (like this one) and comments.

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Click to view a bigger version of Tamara’s poster

Predation, Food Abundance and Male-male Fighting Drives Natural Variation in Lizard Tail Autotomy

If you have a truly outstanding memory or if you enjoy re-reading old AA articles, you might remember this post on how bolder lizards autotomized their tails more readily to compensate for risky behavior. As unlikely as it is, you might also remember me saying that this study solved one piece of the puzzle by explaining why the propensity of tail autotomy would vary within a population. Two years have since gone by, and I am glad to present to you, my fellow AA readers, another piece of the puzzle: how ecology might shape the variation in tail autotomy among populations.

A side-blotched lizard couple snuggling (or more accurately, avoiding human nuisance that was the researcher)

A side-blotched lizard couple snuggling (or more accurately, avoiding human nuisance that was the researcher)

Which aspects of ecology should we be looking at? Fortunately, the rich literature in tail autotomy helped us identify three main players: predation, food abundance and male-male fighting. Among these three ecological factors, the relevance of predation is the most straightforward: lizards will benefit from autotomizing more readily if predation pressure is high. On the other hand, the importance of food abundance lies in the fact that lizards need resources to grow the tails back, and the rate of regeneration depends on food abundance. Therefore, high food abundance will allow for faster regeneration and likely favors higher propensities for tail autotomy. The inclusion of male-male fighting as a key factor stems from the common observation that the tail is a common target for attack when males engage in territorial combats. In fact, quite a few studies have reported tail autotomy as a consequence of male-male fightings. As fights between males are rarely life-threatening (i.e. autotomy-worthy), tail autotomy under those circumstances would be undesirable. Consequently, environments in which male–male combat is common should favor lower autotomy propensities, with other things being equal.

To test these hypotheses, we first built a theoretical model in which we simultaneously varied predation, food abundance and the degree of male-male fighting and examined the propensity for tail autotomy that conferred the highest survival. Results from the model supported our hypotheses: higher predation and higher food abundance favored higher autotomy propensities, whereas higher intensities of male-male fighting favored the opposite. We then took one further step: we collected data on these three factors from five populations of side-blotched lizards (Uta stansburiana) in the western U.S. and used our model to explain the variation in the propensity for tail autotomy among those populations. It turned out that our model did a pretty good job, and we are confident that the variation in tail autotomy at the population level represents the outcome of ecological adaptations to predation, food abundance and male-male competition.

Are you wondering which of the three factors played the most important role in determining the propensity for tail autotomy (hint: it was NOT predation!)? Are you interested in more details about how we actually constructed the model? If so, you might want to give our recent paper a read:

CHI-YUN KUO and DUNCAN J. IRSCHICK. (2016). Ecology drives natural variation in an extreme antipredator trait: a cost-benefit analysis integrating modelling and field data. Functional Ecology 30: 953-963. doi: 10.1111/1365-2435.12593

Age- and Sex-Specific Variation in Habitat Use by Brown Anoles

Little guys like it narrow. Photo from Daffodil’s Photo Blog.

The influence of habitat use on ecological and evolutionary patterns in Anolis lizards is well documented. Despite extensive work on interspecific variation, how habitat use varies within a species is relatively understudied.

As part of my master’s work in Dan Warner’s lab, we caught and recorded the perch height, width, and substrate (i.e., ground vs. vegetation) of 717 brown anoles (A. sagrei) on a small island in the Halifax River, near Ormond Beach, Florida. The island consisted of two main habitat types (open-canopy and forest) with an intermediate between the two.

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