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This year at SICB, I had the great opportunity to talk about part of my work as a postdoctoral researcher in the lab of Dr. Michael Logan at the University of Nevada, Reno. In collaboration with John David Curlis (University of Michigan), Christian Cox (Florida International University), W. Owen McMillan (Smithsonian Tropical Research Institute), and Carlos Arias (STRI), we have been studying the Panamanian slender anole Anolis apletophallus, which has a dewlap polymorphism: males either have a solid orange dewlap (solid morph) or a white dewlap with an orange spot (bicolor morph). Preliminary results from John David Curlis’ PhD dissertation research suggests that, in our mainland study population, the frequencies of these morphs change in conjunction with understory light levels—the solid morph is more frequently observed in brighter areas where more light reaches the understory, whereas the opposite is true for the bicolor dewlap, which is more frequently observed in darker areas of the forest. Thus, it seems possible that selection is maintaining this polymorphism following the predictions of the sensory drive hypothesis, which states that sexual signals should have characteristics that make them the most transmissible given the physical characteristics of the local habitat.
As part of an effort to understand how this trait is evolving in the wild, I set out to understand the genetic basis of this dewlap polymorphism. To do this, my collaborators and I first assembled the full slender anole genome which we then used as a reference for a pooled population sequencing (Pool-Seq) approach using half individuals with solid dewlaps and half individuals with bicolor dewlaps to identify the genomic region underlying this dewlap polymorphism.
Our genome assembly showed pretty good results (Scaffold N50 154,613,287). The Pool-Seq results presented a clear peak of differentiation between solid and bicolor morph groups that corresponded to a region on Scaffold 3. We have a promising candidate gene within this region that may underly the dewlap polymorphism, but will continue to explore these data further to understand the genetic basis of this charismatic trait.
A mourning gecko (Lepidodactylus lugubris) climbing vertically on glass with the help of its impressive toe pads.
I think most people visiting Anole Annals could argue that the adhesive digits of anoles are some of the most fascinating aspects of their biology (or maybe I’m just biased). Digital adhesion is accomplished through toe pads: a collection a broad, modified plantar scales which bear thousands upon thousands of microscopic, hair-like structures (i.e. setae). Through frictional and van der Waals forces, these collections of setae allow toe pad-bearing lizards to easily access vertical surfaces and exploit habitats many lizards cannot. Shockingly, adhesive toe pads have independently evolved several times across lizard evolutionary history (at least 16 times by recent estimates) — once in the common ancestor of anoles, once in a clade of southeast Asian skinks, and 14 times in geckos. Both within and between the different evolutionary origins of toe pads, there is substantial variation in toe pad size, shape, number of scansors/lamellae, and position of the adhesive apparatus.
In our recent study, my collaborators and I took the first steps to characterize how embryonic development is modified to achieve this incredible diversity. Using embryonic material my coauthor Thom Sanger collected as a postdoctoral researcher in Marty Cohn’s lab, in addition to embryonic material I collected over the course of my Ph.D. training in Tony Gamble‘s lab, we aimed to compare embryonic digit development of ancestrally non-padded lizards with that of anoles and padded geckos. We used a model clade approach to broadly sample anoles and geckos, although some species breed more easily in the lab and have more embryological resources than others. All together, we sampled a range of toe pad morphologies in both clades (trunk-ground and trunk-crown Anolis ecomorphs and leaf-toed and basal pads in geckos). To help polarize the developmental changes leading to the origin of toe pads, we also included two ancestrally padless species in our comparisons. After the collection of these diverse embryos, we used scanning electron microscopy (SEM) to characterize scale morphology of the digits throughout embryonic development.
By comparing embryonic material of anoles and geckos, we essentially span the diversity of squamates in a single comparison.
Because of the ~200 million year divergence between anoles and geckos and dramatic differences in adult morphology, we anticipated that we would see stark differences in the developmental origins of toe pads in these species. To our surprise, we found striking similarities in toe pad development between all of the pad-bearing species we examined. We found that toe pads develop after digit webbing recesses. In all pad-bearing species, ridges that become the adhesive scansors and lamellae first form in the distal half of the digit. Throughout development, new ridges begin forming in the proximal direction while the previous ridges begin to grow laterally. Elaborations and derivations in toe pad form, such as bifurcation, occur in the latter-half of embryonic development. The presumably ancestral pattern of plantar scale development we observed in our leopard gecko and fence lizard embryos (both species lacking adhesive digits) demonstrated that scale ridges form all at once along the length of the digit. These differences are similar to those documented between developing non-padded gecko tails and padded tails of crested geckos. This means that anoles and geckos have converged on a similar developmental process! We suggest that toe pads are initially formed through a major repatterning of digital development and then variation is achieved through relatively minor “tinkering,” through either timing or location of developmental patterns.
Scanning electron micrographs (SEMs) of embryonic lizard digit development, progressing from early development (left) to late development (right). The pad-bearing brown anole (Anolis sagrei) and mourning gecko (Lepidodactylus lugubris) have converged on scansor ridges forming in a distal-to-proximal direction, while the paddles leopard gecko (Eublepharis macularius) has scale rows forming all at once along the length of the digit. Lizard photos courtesy of Dr. Stuart Nielsen.
This is by no means the end of this story. We’ve just scratched the surface and there are a several directions to head in. A logical next step is to characterize histological organization through toe pad development. From there, characterizing the genes involved in toe pad morphogenesis, in tandem with the possibilities of new gene editing technologies, would allow us to test mechanisms of toe pad formation and how variation is generated. And, of course, characterizing toe pad development in other species (such as the secondarily padless Anolis onca) may elucidate further conservation or derivation from the trends we found. This is an exciting time to be a toe pad biologist!
As we know, anoles are ectotherms which could spell trouble under a changing climate. By closely relying on the temperature of their environment to regulate all sorts of physiological processes, anoles may be at risk when the environmental temperature shifts due to climate change. Because of this, many studies have measured traits which describe a lizard’s thermal physiology, and two popular traits are the lizard’s preferred temperature (Tpref) and heat tolerance. But few studies have looked at a) how repeatable these traits are in any individual and b) whether the two are correlated!
Shannan with her poster at SICB 2022 in Phoenix.
Shannan Yates, a graduate student at Tulane University in Dr. Alex Gunderson’s lab endeavored to do just this, and presented the results at SICB this year with a very compelling poster. Shannan hypothesized that if Tpref was measured twice in the same individual, that these temperatures should be repeatable. Secondly, she hypothesized that preferred temperature would be correlated with heat tolerance, as these traits are expected to be phenotypically linked, and individuals with high heat tolerances should prefer higher temperatures.
Interestingly, though, Shannan found quite the opposite! Tpref was neither repeatable nor correlated with heat tolerance! This has important implications for many studies which attempt to quantify these traits in Anolis lizards. Shannan concluded that either thermal preference is flexible, or that the current methods used to study Tpref may affect our measurements. Also, thermal preference may not actually be correlated with thermal tolerance at an individual level, or our current methods are indeed obscuring a relationship.
Shannan’s poster is up on SICB+, so be sure to check out the data for yourself, and check out Shannan on twitter here!
Bob Trivers published his memoirs, Wild Life, six years ago. We discussed it in these pages and pointed to a favorable book review that appeared in Current Biology, a review with which I agree completely, not surpisingly, since I wrote it.
I commend the book to you, but if you want the short story, check out Trivers’ two-page summary of his life from age 13 to 29 just published in Evolutionary Psychology. The abstract is a good indication of what the short paper holds: “This is a brief history of my intellectual life from age 13 to 29 years—and beyond. It encompasses mathematics, US history, and evolutionary biology, especially social theory based on natural selection.”
An Anolis biporcatus enjoys some sun while balancing along a branch with the help of those neat adhesive toepads and claws. Credit Wikimedia Commons.
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In a recently published study, Cortés-Parra et al. (2021) compare the claws and toepads of mainland and island Anolis radiations in examination of “morphotype” diversity across phylogenetic and ecological scales. This study intersects nicely with quite recent work comparing the mainland and island radiations (e.g., Hiue et al. 2021; Patton et al. 2021), and claw morphology (e.g., Yuan et al. 2019, 2020; Falvey et al. 2020).
New literature alert!
Claws and toepads in mainland and island Anolis (Squamata: Dactyloidae): Different adaptive radiations with intersectional morphospatial zones
Cortés-Parra, Calderón-Espinosa, and Jerez
Abstract:
Anolis lizards have evolved morphologies in response to different selective factors related to microhabitat use. Morphological diversity exhibits evolutionary patterns that reveal similarities and unique regional traits among the mainland and island environments and among Greater Antilles and Lesser Antilles islands. In the Greater Antilles and mainland environments anole species are classified into morphological/ecological groups, that are known as morphotypes (mainland) or ecomorphs (Greater Antilles). Morphotypes are defined only with morphological information; in contrast, for ecomorph assignment both morphology and ethology are required. For mainland species distributed in northwestern South America 10 morphotypes were proposed to include the morphological diversity of 59 species. We obtained data from body size, limbs length, tail length, and the number of lamellae for an additional ten species occurring in the same region and assigned them into morphotypes. We also collected data of the claw and toepad diversity of mainland and island Anolis from northwestern South America and compared it to the claw and toepads morphology recorded for the Greater Antilles and Lesser Antilles islands, under a phylogenetic framework. We found new island morphotypes (MT11–MT13) of Anolis from northwestern South America. When comparing claws and toepads morphology among the 13 morphotypes we found that morphological variation of these traits partially corresponds to morphotype groups. For instance, habitat specialist species like Anolis heterodermus, classified in morphotype 4 (MT4), have a characteristic design of broad toepad and reduced claws, and non-unique design of toepads and claws occurs in morphotypes MT1, MT2, MT5, MT10, and MT13. We also compared claws and toepads of fore and hindlimbs within the same individual, and found that even if limbs show differences in claws and toepads, suggesting that they perform differential biomechanical function, the degree of within individual variation is specific and not related to morphotype assignment. Our data supported the convergent and unique regional evolution among mainland and island anoles, and revealed aspects of correlative evolution of functional traits of claws and toepads that probably are related to minor differences in microhabitat use among mainland and island species, as suggested by previously published literature. Lastly, the evolutionary pattern of morphological diversity of claws and toepads of Anolis in the mainland and island environment supports both unique regional traits and common selective and historical factors that have molded Anolis morphological diversity.
Literature Cited:
Cortés‐Parra, C., Calderón‐Espinosa, M. L., & Jerez, A. (2021). Claws and toepads in mainland and island Anolis (Squamata: Dactyloidae): Different adaptive radiations with intersectional morphospatial zones. Journal of anatomy.
Falvey, C. H., Aviles-Rodriguez, K. J., Hagey, T. J., & Winchell, K. M. (2020). The finer points of urban adaptation: intraspecific variation in lizard claw morphology. Biological Journal of the Linnean Society, 131(2), 304-318.
Huie, J. M., Prates, I., Bell, R. C., & de Queiroz, K. (2021). Convergent patterns of adaptive radiation between island and mainland Anolis lizards. Biological Journal of the Linnean Society, 134(1), 85-110.
Patton, A. H., Harmon, L. J., del Rosario Castañeda, M., Frank, H. K., Donihue, C. M., Herrel, A., & Losos, J. B. (2021). When adaptive radiations collide: Different evolutionary trajectories between and within island and mainland lizard clades. Proceedings of the National Academy of Sciences, 118(42).
Yuan, M. L., Wake, M. H., & Wang, I. J. (2019). Phenotypic integration between claw and toepad traits promotes microhabitat specialization in the Anolis adaptive radiation. Evolution, 73(2), 231-244.
Yuan, M. L., Jung, C., Wake, M. H., & Wang, I. J. (2020). Habitat use, interspecific competition and phylogenetic history shape the evolution of claw and toepad morphology in Lesser Antillean anoles. Biological Journal of the Linnean Society, 129(3), 630-643.
Dr. Jenna Pruett with the study organism from her SICB talk, Anolis sagrei .
While nesting is ubiquitous across taxa, Dr. Jenna Pruett is interested (like many of us on this site) in non-avian reptiles. Dr. Pruett is currently and NSF Postdoctoral Fellow at University of Colorado – Boulder under Dr. Ambika Kamath and completed her Ph.D. with Dr. Daniel Warner at Auburn University in 2021. For her doctoral work, Dr. Pruett studied nesting behavior in the Cuban brown anole (Anolis sagrei). She found that A. sagrei females tend to nest on the ground, under cover objects (e.g., under rocks), and in areas with high soil moisture and lower temperatures than compared to ambient surroundings. Interestingly, she found that these nest sites were correlated with positive effects on offspring survival.
At SICB 2022, Dr. Pruett discussed a chapter of dissertation research where she was interested in other environmental variables that might influence nesting behavior, such as the presence of predators. The northern curly-tailed lizard (Leiocephalus carinatus) has a shared evolutionary history (i.e., native to Bahamas, invasive in Florida) with A. sagrei. Additionally, A. sagrei is considered a trunk-ground species and L. carinatus is mostly ground-dwelling. Other research suggests that when L. carinatus is present, individual A. sagrei tend to perch higher in the canopy and an increase in mortality is observed (particularly for females).
Dr. Pruett’s experimental set-up from this project.
To address whether predation risk influences A. sagrei nesting behavior, Dr. Pruett designed walk-in cages that were visually separated from each other and contained two nesting options for females: (1) a nest pot above the ground and (2) a nest pot on the ground in a cage with L. carinatus. Some of these cages contained a predator, while some did not. She predicted that females would prefer to nest in above-ground areas when predators were present.
Dr. Pruett found that overall, females tended to prefer laying eggs on the ground prior to predator presence. After predators were added to cages, there was a distinct difference in nesting behavior in cages with and without a predator (i.e., over 50% of eggs laid were above ground when a predator was present). Lastly, when predators were removed, there was a continued upward trend of laying eggs above ground in both treatments. Dr. Pruett suggests that this might result because above-ground pots are a relatively pristine environment to nest, and that if given that option under natural conditions, females might tend to nest above ground as well. Additionally, the above-ground pot may have also gotten more sunlight and more/less moisture that might account for female preference. Dr. Pruett also adds that lizards in cages that were without a predator may have sensed that L. carinatus were in the area (i.e., through mechanisms other than visual) that led them to nest higher.
Dr. Pruett concluded her SICB talk with three remarks: 1) there is an effect of predator presence on A. sagrei nesting behavior, 2) there is an increased preference for above-ground nests in both treatment groups that could be due to other environmental factors, and 3) there need to be more studies on anole nesting, which is a critical component of reproduction, but is understudied in many species. Dr. Pruett is one of the world’s leading researchers in anole nesting behavior and I would highly encourage you to reach out to her with any questions!
“SICB has provided invaluable networking opportunities for me! I met my PhD advisor there, and each year it’s an opportunity to see current research and exchange exciting ideas,” Dr. Pruett says of SICB.
Check out Dr. Pruett’s talk here! Check out Dr. Pruett’s twitter page here!
It’s been a long time since we’ve updated our Meet the Anole Scientists section of Anole Annals, so we’re going to do that now! The last time we did this was back in 2020, so we figured it was about time to put some new faces up on our website. You can see the Meet the Scientists section of our webpage here.
If you are interested in being featured, please fill out the attached Google form here. Thank you for your participation, and we look forward to getting your profile up on the website shortly!
Mr. Wayne Wang from Tulane University.
It’s no surprise that reproductive traits are important for the survival and fitness of species- particularly in the face of changing environments. What I learned from Mr. Wayne Wang’s talk at SICB 2022, though, was that male fertility is often more heat-sensitive than female fertility and even adult thermal tolerance! Wayne is a 3rd year Ph.D. student at Tulane University under Dr. Alex Gunderson and at SICB this year, he discussed his preliminary results on Cuban brown anole (Anolis sagrei) sperm thermal tolerance and mobility.
In some species, the temperature associated with infertility in males is often a better determinant of population distribution than adult thermal tolerance. Additionally, sperm are under strong selection because only few make the journey to fertilize an egg (which means that they are also one of the most highly diverse cell types). Mr. Wang noticed that in the literature, there is a large focus on sperm morphology, rather than physiological traits like mobility or speed. In his talk, he sought to 1) test thermal tolerance of sperm, 2) test repeatability of thermal tolerance, and 3) identify any correlations between sperm and adult thermal tolerance in A. sagrei. He began by rounding up some lizards and copulating them until they ejaculated sperm, which he states is a lot easier process than one might imagine. Sperm were diluted and incubated at various temperatures until videos were recorded to measure sperm motility.
Mr. Wang found that A. sagrei sperm motility did not differ much between 33°C and 41°C; however, at approximately 43°C, there is a steady decline where approaching 48-50°C, none survive. In fact, 50% of sperm stop moving at about 43°C. This experiment was repeated with the same group of lizards during a second week following a seven-day acclimation period. Similar patterns were observed and during week 2, more individuals had a higher percentage of sperm motility. Lastly, no correlations between sperm and adult thermal tolerance were identified–Mr. Wang speculates that this might be because these traits are not linked or his sample size did not allow for enough resolution.
Be sure to check out Wayne Wang’s awesome talk here!
This site has all kinds of useful information! Here’s the site’s story (“about us”):
Our Story
Esri created the Caribbean GeoPortal Program to support an open mapping community across the Caribbean. As a global company, Esri’s distributors and employees have been working across the countries and territories in the Caribbean for many years.
The Caribbean GeoPortal is a comprehensive cloud-based platform that is focused on advancing three main goals for the region:
- increasing the capacity of organizations in the region through GIS training and education
- improving collaboration and information sharing among organizations in the region
- providing organizations in the region with the necessary GIS capabilities to support their work