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Surveying Claw and Toepad Diversity Across Anole Adaptive Radiations

An Anolis biporcatus enjoys some sun while balancing along a branch with the help of those neat adhesive toepads and claws.  Credit

An Anolis biporcatus enjoys some sun while balancing along a branch with the help of those neat adhesive toepads and claws.  Credit Wikimedia Commons.

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

In Journal of Anatomy

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 Sciences118(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. Evolution73(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 Society129(3), 630-643.

SICB 2022: Anole Nesting Behavior under Predator-Presence!

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!

“Meet the Scientists” Update: Featuring You!

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!

 

SICB 2022: Let’s Chat about Lizard Sperm!

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!

Caribbean Geography Resource

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

SICB 2022: Lizards and Lead: What’s Going on with Anoles in New Orleans?

The Society for Integrative and Comparative Biology (SICB) conference is a national gem for highlighting research from biologists across the country. This year, over a thousand researchers shared their work in Phoenix, AZ and on online platforms for the 2022 SICB conference. Fourth-year Ph.D. Candidate, Annelise Blanchette, from Tulane University in New Orleans, LA under Drs. Alex Gunderson and Jordan Karubian was one of these presenters. Like Phoenix, New Orleans is a bustling city with everything from high-rise skyscrapers soaking in the Louisiana sun to paved neighborhoods polluted with anthropogenic waste (e.g., Mardi Gras beads). Ms. Blanchette discussed this idea of pollution, particularly the contaminant lead, at SICB 2022 and wanted to know more about the influence of lead on physiological performance of her study species, the Cuban brown anole (Anolis sagrei).

Ms. Annelise Blanchette and her study organism, the brown anole (Anolis sagrei).

Ms. Blanchette’s previous work showed that anoles from areas in New Orleans with high soil lead levels had over 10X the toxicity threshold of lead (in comparison to birds and mammals) in their bloodstreams. She wanted to know how these lizards were influenced physiologically by lead exposure and how that translates to physiological performance by measuring sprint speeds and balancing ability of anoles from these regions. She predicted that there would be an overall negative effect of high bloodstream lead levels and that lizards from these high exposure areas would 1) not be as fast as their counterparts in terms of sprint speed, and 2) have decreased balance, measured by counting the number of times they slipped on a wooden beam.

Measuring balance of anoles by counting number of times individuals slip from the wooden beam.

From her results, she found that there is no correlation between lead exposure and sprint speeds; however, there is a negative effect of lead on balance that may be sex-dependent. In fact, male anoles exposed to low levels of lead had fewer slips (i.e., better balance) than males exposed to high levels of lead. She states “It’s surprising given the incredibly high levels of lead in their bloodstream that the brown anole is coping with the exposure so well.” This work is particularly fascinating because it begins to uncover ways urbanization can influence wildlife in nearby regions though pollution of heavy metals. “… if we don’t find an obvious or devastating affect behaviorally or cognitively in the brown anole, perhaps we’ll find that they have adapted and are less resistant to lead’s detrimental effects – which would be so cool!” Ms. Blanchette says. She hopes that next year, like many other virtual SICB members, she will be able to present her work in person!

You can check out Annelise’s talk from SICB 2022 here! Follow her on Twitter @basicbiologist!

SICB 2022!

The Society for Integrative and Comparative Biology annual conference is happening next week, January 3-8 2022! With a return to in-person events, we are aiming to highlight the breadth of research talks and posters on anoles given by all the amazing junior researchers at the conference!

This post is a call-to-arms: we can’t cover all the presentations without your help! We are looking for interested folks attending the conference that can help the Annals by contributing blog posts featuring these researchers and their anoles. Folks that elected to do the virtual SICB+ option instead of attending in-person are also encouraged to get involved. If you’re interested, please contact Anthony for any additional details or information.

Below is a list of anole presentations happening at SICB 2022- please reach out if I missed any of any of these peaks both your scientific and blogging interests!

Date Session Authors Title
Jan 4 P1 Johnson, M/R*; Murphy, K/M; Warner, D/A The effect of the egg-shell microbiome on embryo development and hatchling phenotypes in an oviparous lizard 
Inter- and Intra-specific Interactions
 Jan 4 8 Kahrl, AF*; Kustra, MC; Reedy, AM; Bhave, R; Seears, HA; Warner, DA; Cox, RM Selection on sperm count, but not on sperm morphology or velocity, in a wild population of Anolis lizards 
Sexual Selection: Competition
 Jan 4 17 Wittman, TN; Robinson, CD; Cox, RM* Genetic variance in phenotypic responsiveness of Anolis lizards to testosterone  
Sexual Selection
 Jan 5 P2 George, J*; Browne, I; Gignac, P; O’Brien, H Designing 3D printed braces for imaging the carolina anole (Anolis carolinensis) dewlap musculature using diceCT  
Biomaterials
 Jan 5 S5 Cheu, AY*; Reed, SA; Mann, SD; Bergmann, PJ Kinematic differences between running on water versus running on land in Anolis sagrei 
S5: Lesser known transitions: organismal form and function across abiotic gradients
 Jan 5 33 Nicholson, DJ*; Knell, RJ; McCrea, R; McMillan, WO; Neel, LK; Chung, AK; Curlis, JD; Garner, TWJ; Cox, CL; Logan, ML Rare climate events and competition constrain establishment success in Anolis lizards 
Terrestrial Population Ecology
 Jan 6 P3 Grossen, TL; Bunnam, AD*; Cohen, RE Circadian gene expression across reproductive phases in the green anole lizard (Anolis carolinensis) brain  
Foraging and Neuroethology
 Jan 6 P3 Gleason, GS*; Gunderson, A Cooking eggs: Testing for Plasticity in the heat tolerance of lizard embryos 
Thermal Biology
 Jan 6 56 Wang, W*; Gunderson, AR Lizard sperm in changing environment: The physiological ecology of sperm thermal performance  
Reproductive Physiology
 Jan 6 67 Wuthrich, KL*; Nagel, A; Swierk, L Rapid body color change provides lizards with facultative crypsis in the eyes of their avian predators 
Sensory Ecology and Signal Evolution
 Jan 6 69 Norris, MC*; Brown, OE; Warner, DA An experimental test of the environmental matching hypothesis in an oviparous lizard 
Micro Eco Evo Devo
 Jan 6 74 Blanchette, A*; Gopal, A; Finkelstein, ME; Karubian, J; Gunderson, AR Lead exposure in the brown anole (Anolis sagrei) in New Orleans, Louisiana 
Anthropogenic and Climate Change Influence on Behavior
 Jan 6 77 Pirani, RM*; Curlis, JD; Arias, C; McMilian, O; Cox, C; Logan, ML Uncovering the ecological and genetic basis of a sexual signal: the dewlap of the Panamanian slender anole (Anolis apletophallus) 
Animal Communication
 Jan 6 77 Johnson, LE*; Ladner, JT; Singhal, S; Losos, JB; Johnson, MA Does lizard display behavior follow the principles of signal efficacy? 
Animal Communication
 Jan 6 83 Bodensteiner, BL*; Muñoz, MM Adaptive radiation without independent stages of trait evolution in a lineage of Caribbean anoles 
DEE Best Student Presentation: Ray Huey Award
 Jan 7 100 Pruett, JE*; Warner, DA The effects of predator presence on nesting behavior and survival in the brown anole (Anolis sagrei) 
Predator-Prey Interactions
 Jan 7 113 Winchell, KM Parallel performance: Functional morphology of Anolis lizards adapted to urban environments 
Adapting to a Changing Environment
Jan 5 45 Muell, MR*; Oaks, JR; Warner, DA The evolution of thermal developmental plasticity across Anolis lizards – a comparative approach 
DPCB Best Student Presentation: David & Marvalee Wake Award
Jan 6 P3 Lagorio, AD*; Fields, M; Fortner, J; Mackareth, E; Perez, C; McGechie, F; Wilken, A; Leal, M; Ward, CV; Middleton , KM; Holliday , CM Adventures in 3D musculoskeletal modeling methods in the heads of Anolis 
Skull Morphology
 Jan 6 P3 Yates, S.S*; Gunderson, A Repeatability and correlation among thermal traits in the lizard Anolis sagrei 
Thermal Biology
 Jan 6 77 Rej, J.E*; Gunderson, A.R Thermal dependence of species interactions: does temperature effect competitive outcomes between native and invasive Anolis lizards? 
Animal Communication
Jan 7 S10 Foster, KL*; Selvitella, AM Anolis ecomorph biomechanics across arboreal environments: What can machine learning tell us about behavioral plasticity in lizards? 
S10: Integrating ecology and biomechanics to investigate patterns of phenotypic diversity: Evolution, development, and functional traits

#DidYouAnole – Anolis allogus


Photo: Alex Alfil, iNaturalist

Hello!

Happy Holidays and Happy Anole Eve!

I took a break for my birthday, and then it was a holiday, then finals, then I had to travel, but now I’m back and it’s almost a holiday again. Before another holiday I did wanna share a short anole post! I’ve also missed doing this and I’ve been thinking about what anole to do since I got to see the anole specimens at the London Natural History Museum.

I picked a festive little Cuban anole, Anolis allogus, also called the Spanish Flag anole or Bueycito anole (after a village where it can be found).

The males of this trunk-ground anole species have an SVL of ~60 mm, while females are about ~49 mm. Its distribution is sporadic but it’s found mostly in the east of Cuba. They follow the typical trunk-ground anole coloration of light or dark grey-brown tones, with striping on their tails, and marbling on their sides. Male Bueycito anoles have pale yellow dewlaps with either a center dot or lateral center stripes of bright red/red-orange. Females have smaller pale yellow dewlaps.


Photo: Alex Alfil, iNaturalist

Spanish flag anoles have been recorded predating on a species of Blindsnake. Check it out here!

I know this was short but I just wanted to say hi really quickly and Happy New Year!

The Genomic Undercarriage of Thermal Plasticity in Puerto Rican Anoles

Anolis cristatellus (pictured; Wikimedia Commons) continues to prove itself as a model organism for examining thermal biology evolution, particularly in a comparative context of forest versus city-dwelling populations. Recent research by Campbell-Staton et al. (2021) aims to uncover how differential gene expression modulates adaptive and maladaptive plasticity in these populations.

In a recently published study, Shane Campbell-Staton and company continue their comparative investigation of urban-forest anole thermal biology. Employing a combination of wild-caught and common-garden-reared urban and forest populations of Anolis cristatellus, Campbell-Staton et al. (2021) tease apart the role of selection in mediating adaptive and maladaptive thermal tolerance plasticity using a fine-toothed transcriptomic comb.

New literature alert!

Selection on adaptive and maladaptive gene expression plasticity during thermal adaptation to urban heat islands

 

In Nature Communications

Campbell-Staton, Velotta, and Winchell

Abstract

Phenotypic plasticity enables a single genotype to produce multiple phenotypes in response to environmental variation. Plasticity may play a critical role in the colonization of novel environments, but its role in adaptive evolution is controversial. Here we suggest that rapid parallel regulatory adaptation of Anolis lizards to urban heat islands is due primarily to selection for reduced and/or reversed heat-induced plasticity that is maladaptive in urban thermal conditions. We identify evidence for polygenic selection across genes of the skeletal muscle transcriptome associated with heat tolerance. Forest lizards raised in common garden conditions exhibit heat-induced changes in expression of these genes that largely correlate with decreased heat tolerance, consistent with maladaptive regulatory response to high-temperature environments. In contrast, urban lizards display reduced gene expression plasticity after heat challenge in common garden and a significant increase in gene expression change that is congruent with greater heat tolerance, a putatively adaptive state in warmer urban environments. Genes displaying maladaptive heat-induced plasticity repeatedly show greater genetic divergence between urban and forest habitats than those displaying adaptive plasticity. These results highlight the role of selection against maladaptive regulatory plasticity during rapid adaptive modification of complex systems in the wild.

Short Faces, Two Faces, No Faces: Lizards Heads Are Susceptible to Embryonic Thermal Stress

Examples of malformed embryos

Examples of embryos with normal and abnormal craniofacial development

Embryos are not just little organisms encapsulated within their eggs. Embryonic development is dynamic; the embryo transitions from one to a few undifferentiated cells to a stage where the various parts like arms, legs, and faces become apparent to a form that resembles the species that will eventually emerge. A panoply of signaling events and rapid rates of cell division are all tightly choreographed to make sure that development proceeds in a predictable, species-specific fashion.

But this dynamism of development also makes the embryo susceptible to environmental perturbation. Heat, chemical exposure, and pathogens can all disrupt normal embryonic development, sending the embryo down paths that may lead to fatality or reduced fitness. In our recently published study, my colleagues, students, and I demonstrate that heat stress, paralleling what will likely be experienced during the 21st century, can induce structural malformations to the brain and face of lizard embryos.

In 2014 and 2015 I was a post-doc in the Cohn Lab at the University of Florida. At the time, I had been dissecting and observing anole embryos for approximately 14 years. Throughout those 14 years I had observed only a handful of malformed embryos, maybe on the order of 10-20 embryos after collecting thousands of embryos from numerous anole species. Yet, in the summers of 2014 and 2015, while working alongside then graduate student Bonnie Kircher, I collected more malformed Anolis sagrei embryos than I had in all of my previous years. I certainly didn’t realize it in the moment as malformed embryos were still relatively rare compared to the total number of embryos we were collecting. But, by the end of my time in Florida the number jumped out at me. Sometimes the rate of development seemed to depart from the normal sequence of development. Other times the embryo was clearly not well and would likely not survive to hatching. Even as other projects accelerated, my interest in these malformed embryos remained piqued.  When I began my faculty position Loyola University Chicago, I decided to invest the lab’s time and resources into determining whether this pattern was real or just a chance observation.

In spite of other options­–unique genetic mutation running rampant in Gainesville populations of brown anoles seems highly unlikely–I decided to investigate the effects of heat stress on embryonic development. The effects of global warming had been widely discussed as a threat to ecotherm populations and anoles have been at the center of both field and lab observations since the outset. A number of studies have also shown reduced hatching success from lizards incubated at relatively high temperatures. Relating this back to my observations in Florida, it also occurred to me that Bonnie and I used a different collection strategy for our breeding colony those years; we would regularly replenish or add to the colony from field-caught lizards throughout the summer. This raised the possibility that the embryos developing within the gravid females were exposed to the environmental heat stress before being deposited into our waiting hands. Luckily, brown anoles are prolific egg producers, providing my lab with the ability to test whether heat stress induces embryonic malformations under different incubation regimes.

Embryos incubated under conditions reflecting those observed in shady nest sites exhibit malformations in only one to two embryos out of every 100 live embryos. These nest sites tend to be relatively stable in temperature, rarely rising about 30 degrees Celsius. However, embryonic heat stress induces malformations in 10-30% of embryos exposed to incubation conditions that parallel nest sites that would be located in sunny locations. These putative nest sites reach temperatures above 36 degrees Celsius, the critical thermal temperature for the embryos, for up to eight hours per days. The malformations we observed were not evenly spread across the body. Instead, we saw the greatest concentration in the brain and face of the developing lizards. Most malformations included a change in facial proportion, from subtle changes in facial length to pronounced brachycephaly and/or clefting. In one case, the entire face and forebrain were ablated in the embryo! When it comes to the induction of structural malformations, the most sensitive period of development is around oviposition, including the time that the egg is still within the female. Although we do not yet know how many of these embryos would successfully hatch, our experiments do raise concerns about the long-term impacts of global warming on ectotherm development.

Extreme, but rare malformations

Examples of extreme, but rare malformations observed in eggs reared at elevated temperatures.

The consistent pattern of thermal-induced neural and facial anomalies made us think that there may be a common underlying cause of these changes, leading us to create and test a new model of embryonic thermal stress. Based on our understanding of amniote craniofacial development, we predicted that disruption to Hedgehog signaling, one of the earliest signaling pathways needed for facial development, could create the full spectrum of observed malformations. After measuring processes up and downstream of Hedgehog signaling (e.g., cell death and signaling within the presumptive facial cells respectively), it does, in fact, appear that Hedgehog signaling is disrupted in the face of embryos experiencing thermal stress. Depending on the degree of response by a particular embryo, everything from normal to extremely malformed embryo could be induced. At this time, it appears that our model holds for brown anoles and may be applicable in species far beyond anoles and lizards.

A developmental model of embryonic thermal stress

In our proposed model, heat stress affects Hedgehog signaling, causing a disruption to normal facial morphogenesis.

There remains much to learn about normal and abnormal facial development in lizards. We do not yet know what other signaling pathways are equally disrupted during thermal stress or whether there are endogenous buffering mechanisms that help to maintain normal development in the face of external stress. Perhaps one of the most important discussions that needs to occur is how we study rare events. These events could be uncommon, but extreme heat events that exceed the “normal” conditions typically observed in the wild. These are increasing in regularity and may have significant impacts on ectotherms later in the 21st century. Alternatively, the rare events could be the emergence of malformed embryos which occur in only a fraction of individuals, even when the average phenotype is not dramatically altered. For species such as the brown anole, this may not be alarming. But for species with relatively few viable hatchings each season, embryonic heat stress could have dramatic impacts on their long-term viability. These developmental perspectives  are needed to fully understand the ways that global change will affect the lives and longevity of lizards and other ectotherms.

Embryos in the age of anthropogenic change

Embryos are impacted by a range of challenges associated with anthropogenic change. See more in Sanger 2021, Integrative developmental biology in the age of anthropogenic change

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