SICB 2015: Skull Shape Optimized for Feeding in Lizards

If you’ve ever had a lizard chomp down on your finger, you know that lizard skulls are well-designed for biting!

Anolis lizards have a skull optimized for feeding. Photo of A. evermanni by Michele Johnson.

Ross et al. showed that Anolis lizards have a skull optimized for feeding. Photo of A. evermanni by Michele Johnson.

Dr. Callum Ross, a biomechanist focusing on feeding systems at the University of Chicago, presented a talk at SICB on Monday describing differences in in vivo bone strain between mammal and lizard skulls.  In mammals, the shape of the skull causes strain during feeding to be exerted differently on different bones: the frontal and parietal bones, those that cover the human forehead and back of the head, experience very low strains compared to the maxilla and mandible and zygomatic arches, the bones that support the jaw. Because of this variation in force distribution, the top of the mammalian skull is not optimized to dissipate feeding forces. In contrast, the structuring of lizard skulls is dramatically different. Whereas the mammalian skull is designed to protect the large mammalian brains, lizard skulls contain much smaller brains . To determine how strain gradients are distributed across lizard skulls during feeding, Ross measured strain magnitude in vivo across four lizard species, Tupinambis merianae, Anolis equestris, Gecko gecko, and Iguana iguana. Ross and his colleagues found that lizards experience much higher strains on top of the cranium, the same place at which mammals experienced very low strain, demonstrating a skull design that is more optimized for feeding. He also found that maximum frontal bone sheer strain was highest in Anolis equestris! These results are amazing because they demonstrate a clear morphological trade-off between optimization for feeding in lizards versus optimization for protecting the large mammalian brain.

Note: This post was written by Bonnie Kircher, a graduate student studying anole development in Marty Cohn’s lab at the University of Florida.

SICB 2015: Diet and Body Condition in Brown Anoles

Brown anole photo by Dan Warner.

Although there is a vast literature on how resource availability affects physiology, behavior, and reproduction (among many other things), we know surprisingly little about the composition of individual diets in nature. To truly know whether you are what you eat, you have to understand what it is you are eating. Dan Warner from the University of Alabama at Birmingham set out to do just that with some very interesting preliminary data on an island population of brown anoles in Florida. He trapped potential prey in two very different habitat types on the island: interior forest and open shoreline. The shoreline had mostly marine-sourced prey items (amphipods), whereas the forest had more terrestrial insects, like roaches. Dr. Warner then wanted to know if these differences in diet would affect body composition of anoles in those habitats.

The methods here are the best part. Dr. Warner used Quantitative Magnetic Resonance (QMR) technology, typically used for rodent lab animals, to determine body composition. He found that there was a very strong match between the QMR estimates of lean and fat mass compared to chemical carcass analysis of the same individuals. And, the QMR measures only take about 5 minutes to do! This non-invasive, non-lethal way to estimate body composition has huge implications for studies that seek to tie those characteristics to components of organismal fitness, namely survival and reproductive success. It doesn’t work to track survival on individuals sacrificed for chemical carcass analysis. He also suggests that this now-validated method will be important to test whether typical measures of body condition (such as mass-length residuals) are actually good estimates. It doesn’t sound good for our typical measures of condition, but he will tell that story soon!

Returning to diet’s effect on body composition, the results showed that lizards in the interior of the island had more fat mass and less lean mass than lizards found on the shoreline. He plans to continue the research by repeating it on replicate islands with similar habitat types, as well as look at long-term consequences of variation in body composition. This new approach will open the door for fascinating research to come, so stay tuned!

SICB 2015: The Ecomorphology of Lygosomine Skinks

As evidenced by the large number of SICB 2015 posts flooding Anole Annals, anoles are very well represented at this year’s meeting.  However,  presentations on other reptilian species have also been abundant. On Sunday afternoon during SICB 2015, Kathleen Foster, a graduate student in Tim Higham’s lab at the University of California, Riverside, presented a poster titled “Ecomorphology of lygosomine skinks: the impact of habitat use on limb length.”

Limb lengths vary dramatically among lyosomine skinks! Figure courtesy of Kathleen Foster.

Limb lengths vary dramatically among lyosomine skinks! Figure courtesy of Kathleen Foster.

Habitat structure plays an extremely important role in shaping the morphology and behavior of animals. Despite the fact that Anolis ecomorphs are one of the most studied and beloved examples of habitat specialization, habitat specialization certainly occurs in other reptile taxa. Foster used lygosomine skinks, a group of lizards that both ecologically and morphologically diverse, to examine the relationship between limb length and microhabitat use. Skinks in this group occupy microhabitats ranging from leaf-litter to cliffs and tree trunks, and the animals themselves can be stocky or elongated, suggesting an ecomorphological relationship. Using morphological data from 103 species of lygosomine skinks, Foster examined the relationship between limb dimensions and habitat use. She found that rock dwelling and arboreal species have longer limbs of equal lengths compared to terrestrial species. However, Foster also found that static stability (an increased distance between the center of mass and the edge of the base of support) did not correlate with habitat use. Foster hypothesized that these longer limbs provide advantages for climbing on curved, vertical surfaces, yet do not offer the additional advantage of increasing stability. In short, differential microhabitat use explains morphological patterns observed in lygosomine skink limbs!

Note: This post was written by Bonnie Kircher, a graduate student studying anole development in Marty Cohn’s lab at the University of Florida.

SICB 2015: Diet and Exercise Affect Resource Allocation in Green Anoles

When resources are limited, organisms are often faced with trade-offs between energetically-expensive traits. Haley Ferguson, a recent graduate from Jerry Husak’s lab at the University of St. Thomas, presented a poster at SICB this week on an impressively comprehensive study investigating whether trade-offs exist among performance, reproduction, and immune function in the green anole (Anolis carolinensis). In her experiment, Haley divided green anoles into four treatment groups. One group experienced a normal diet (3-4 crickets, 4 times a week) and natural activity regime; one had a restricted diet (1 cricket, 4 times a week) and natural activity; one had a normal diet and strenuous exercise regime (running to exhaustion on a treadmill); and the final group had restricted diet and strenuous exercise.

Based on predictions from life history theory (see figure below), Haley and Jerry predicted that individuals who use more resources for locomotor activity will have fewer resources available for immune function or reproduction. Their results strongly supported this prediction.  First, they showed that exercise training and diet restriction both inhibited the lizards’ capacity to grow in terms of size and mass. Immune function (measured by PHA swelling response and plasma bacterial killing assays) was also compromised in both trained and diet-restricted lizards.  Female egg size and number, and male dewlap size and bite force were also reduced in lizards experiencing diet restrictions and exercise training. Surprisingly, Haley found that restricting lizard diet alone caused a more profound effect on immune function and reproductive output than training alone. Finally, to measure the trade-off between training and diet, Haley measured lizard endurance (time until exhaustion on a treadmill) in each group. She found endurance was higher in the trained groups regardless of a diet restriction. Future work in the Husak lab will follow up on these results by testing trade-offs among all of these traits among lizards with varying testosterone levels.

Predicted relationships among performance, life history, and immune traits (Ferguson and Husak).

Predicted relationships among performance, life history, and immune traits (Ferguson and Husak).

Note: This post was written by Brittney Andre, a research technician studying lizard behavior and physiology in the Johnson lab at Trinity University, and Michele Johnson.

SICB 2015: Ecomorphology in Ecuadorian Anoles

Andres Mármol-Guijaro presenting his SICB poster.

Andres Mármol-Guijaro presenting his SICB poster.

Ecomorphological studies of the diverse Anolis genus provide us with valuable insights to the evolutionary ecology of this group, but we know much more about ecomorphology in Caribbean anoles than in the mainland anole species in Central and South America. In his undergraduate thesis research, Andrés Mármol-Guijaro aimed to start filling in this gap.  Working with Dr. Omar Torres-Carvajal at Pontifica Universidad Católica del Ecuador, Andrés studied morphological features associated with clinging ability in Ecuadorian anoles. Andrés measured toe pad area, clinging ability and perch height of seven Anolis species (five in the Dactyloa clade and two in the Norops clade) that occur in the Ecuadorian Amazon River basin and the Western slopes of the Ecuadorian Andes. He found that neither relative toe pad area nor relative perch height were associated with clinging ability in the Ecuadorian anoles, in contrast to the positive relationships among these traits in Caribbean anoles. Evolutionary differences among phylogenetic lineages may partially explain this variation in ecomorphology between mainland and Caribbean anoles, but additional studies of the diverse mainland groups will help to clarify this.  Andrés invites us all to Ecuador to continue studies of this amazing anole fauna!

Note: This post was written by Lauren Davis, an undergraduate student studying lizard behavior at Trinity University.

SICB 2015: Award-Winning Talk on Gene Flow in Different Thermal Environments

Matt explains his methods.

Matt explains his methods.

The winner of this year’s Division of Ecology and Evolution Huey Award, Matt McElroy, gave an interesting presentation on gene flow and the Bogert Effect in Anolis cristatellus in Puerto Rico. Roughly, the Bogert effect says that thermoregulatory behaviors may shield a species from selection pressures on physiological processes experienced in different thermal environments. Therefore, divergent selection is expected to be weak in thermoregulating species, which can adjust their behavior to maintain a consistent body temperature in a range of thermal habitats. Alternatively, thermoconformers’ body temperatures match that of the environment, and so face strong divergent selection when exposed to new thermal habitats. Gene flow is expected to be high across thermal gradients for the thermoregulators and low for the thermoconformers.

Matt investigated the phylogeographic population structure and gene flow in A. cristatellus on the island of Puerto Rico, discovering three distinct populations. The southwestern population, in the arid rain shadow, was most divergent from the other two. He also conducted trasects up the mountain (a decreasing temperature gradient), finding that genes were moving out of the arid zones, but not the other way. If the Bogert effect held true, we would expect gene flow in both directions in this thermoregulating species; perhaps there is strong selection on cool adapted genotypes in warm habitats, but not vice versa. Matt suggested that higher population densities in lower elevations may influence the uni-directional flow, or that habitat destruction (e.g. hurricanes, agriculture) creates open, sunny patches, allowing the low-elevation populations (warm-adapted) to exploit elevations that they would not have been able to otherwise.

SICB 2015: Trade-Offs Between Pre- and Post-Copulatory Sexual Selection

The focus on sexual selection in reptiles continued yesterday when Ariel Kahrl, a graduate student in Bob Cox’s lab at the University of Virginia, gave her presentation on investment tradeoffs between pre- and post-copulatory sexual selection. She predicted that investment in male-male competition (an important component of pre-copulatory sexual selection) constrains an organism’s ability to invest in post-copulatory selection such as sperm competition. To test this hypothesis across squamates, Ariel performed a meta-analysis using data from 143 species (111 lizards and 32 snakes), and she reported her results in the DCPB (Division of Comparative Physiology and Biochemistry) Wake Award competition for Best Student Presentation. Using male-biased sexual size dimorphism (SSD) as a proxy for pre-copulatory selection and relative testis size as a proxy for sperm competition, Ariel found that both these traits were negatively correlated across the group – that is, species with relatively larger male body size had relatively smaller testes. In other words, in species where males invest more in access to females, the less they invest in sperm! This pattern was strongest among territorial lizards (like anoles). So, it appears that there are significant trade-offs between pre- and post-copulatory selection in squamates.

Ariel is following up on this work with a large-scale comparative analysis of sperm morphology in anoles, to determine if the interaction between pre- and post-copulatory selection shapes sperm evolution. She ended her talk showing how impressively variable sperm traits are among anoles – perhaps a sneak peek for her talk next year?

Anolis sperm! Photo from Ariel Karhl's website.

Anolis sperm! Photo from Ariel Kahrl’s website.

SICB 2015: Lizards in a Warming World: Ectotherm Plasticity in Changing Thermal Environments

While it wasn’t technically a talk about anoles, we’re sure AA readers will want to know the latest work from Alex Gunderson (pictured below), currently a postdoc with Jonathon Stillman at UC Berkeley and SFSU. Yesterday at SICB, Alex described his work on thermal plasticity in five major ectotherm clades (insects, crustaceans, fish, amphibians, and reptiles). Using acclimatization response ratios (ARR) for hundreds of species from these groups, Alex tested the hypothesis that animals in more variable thermal environments would exhibit greater flexibility in thermal acclimation. While he did not find support for that relationship, he did find that habitat type has a strong association with plasticity, as freshwater and marine species have more thermal flexibility than terrestrial species (like our favorite anoles). Next, he extracted the standard deviation of weekly temperatures from the NOAA database, and found that terrestrial animals had more plastic responses to cold tolerance (critical thermal minimum or ‘CTmin’), but not heat tolerance (critical thermal maximum or ‘CTmax’). Additionally, he found and there was no relationship between standard deviation of weekly temperatures and tolerance traits in aquatic species. Thus, terrestrial species had greater plasticity to lower temperatures than higher temperatures. Overall, he found that many types of ectotherms have relatively low capacity for acclimation. This result suggests that plasticity in acclimatization responses will not allow animals to compensate for rising temperatures across the planet, and behavioral responses will instead become more critical.

Alex Gunderson, themal ecologist. Photo from his website.

Alex Gunderson, thermal ecologist. Photo from his website.

SICB 2015: Anolis proboscis Display Behavior

Anolis proboscis, showing the male-specific proboscis. Photo by D. Luke Mahler.

A longtime favorite here at Anole Annals, the Ecuadorian Horned Anole (Anolis proboscis) made an appearance at SICB. Diego Quirola and colleagues from Pontificia Universidad Católica del Ecuador described the use of the proboscis during social interactions. They captured male and female anoles and videotaped staged male-male and male-female interactions. From the videos they were able to quantify behavioral patterns of these fascinating lizards. They did some very anole-like behavior, but they definitely have a flair all their own! With such a fascinating, chameleonic appendage one would expect some important functions of the proboscis, and one would not be disappointed. Watching videos that Diego had on display revealed social behavior very reminiscent of chameleons, with males puffing up, curling their tails, and swaying while doing the more typical anole dewlap extensions.

Then there’s the proboscis. This structure, much like the dewlap, is used during both courtship and agonistic interactions. In both contexts, males actually lift the proboscis. Yes, they can move the proboscis up and down, something not seen in chameleons with rostral appendages (no, we don’t know how they do it!). Diego suggests that the proboscis is lifted to either stimulate females or allow the male to bite the nape as other lizards do while copulating. Males also display a behavior called “proboscis flourishing” where the proboscis is prominently displayed while moving the head side to side. During agonistic interactions it may serve as a dominance indicator, though they are still working on those analyses. Proboscis anoles seem to be at the low end of aggression for anoles, but males occasionally fight and lock jaws. During male fights the proboscis likely gets in the way, and it appears to be purposely lifted during these fights. It’s possible that they lift it to keep the rival male from latching onto their snout, or it could be moved so that they can get better bites in. I was very much looking forward to learning more about these anoles, and I was not disappointed. As more work is done on these fascinating anoles we’ll be able to better understand why it has evolved such an interesting, and un-anole-like appendage, as well as the unique behavior that is associated with it.

SICB 2015: Use it or Lose it: A Study of Dewlap Size Plasticity in Green Anoles

Anolis carolinensis dewlapping. Photo by Cowenby available on Wikipedia.

Anolis carolinensis dewlapping. Photo by Cowenby available on Wikipedia.

On Sunday, Simon Lailvaux of the University of New Orleans gave one of the first anole talks of the SICB meeting, on his work examining the mechanisms underlying seasonal fluctuations in dewlap size. Simon began the talk by describing observations from field and lab studies (Irschick et al. 2006) that revealed that during the summer breeding season, when male anoles extend the dewlap frequently during behavioral displays, male dewlaps are much larger than during the winter nonbreeding season when the dewlap is used rarely. Simon and his lab then conducted a dietary-restriction study to test the hypothesis that this seasonal plasticity is due to resource availability, but found that diet was not associated with dewlap size (Lailvaux et al. 2012).  So, the search for the mechanism underlying this change in dewlap size was on.

Along with several colleagues from Trinity University – Jack Leifer (a materials engineer) and anolologists Bonnie Kircher and Michele Johnson (full disclosure – that’s yours truly), Simon and colleagues then conducted a laboratory experiment to determine whether reduced dewlap size related to less use in the nonbreeding season. To conduct the experiment, the researchers prevented dewlap extension in one set of male green anoles by tying dental floss loosely around their throats, and compared the dewlap size and skin elasticity of those lizards to an unrestrained control group that could dewlap at will. They found that dewlap size in the restrained group continually decreased over time, as compared to unrestrained lizards that, again, exhibited larger dewlaps in the breeding season. Together, these results suggest that use of the dewlap is directly related to its size. Then, the researchers measured the elasticity of dewlap and non-dewlap (belly) skin, and found that the dewlap is more elastic than belly skin, and that both types of skin samples were more elastic in the summer breeding season than in the winter. Because skin is a dynamic tissue whose mechanical properties are altered by sex steroid hormones, Simon suggested that dewlap size plasticity may be the result of seasonal endocrine fluctuations, combined with behavioral use of the structure.

These results suggest so many next steps.  Look for the upcoming manuscript describing this work in more detail!

References

Irschick, D.J., Ramos, M., Buckley, C., Elstrott, J., Carlisle, E.,Lailvaux, S.P., Bloch, N., Herrel, A. and Vanhooydonck, B. 2006. Are morphology -> performance relationships invariant across different seasons? A test with the green anole lizard (Anolis carolinensis). Oikos 114: 49-59.

Lailvaux, S.P., Gilbert, R.L. and Edwards, J.R. 2012. A performance-based cost to honest signaling in male green anole lizards (Anolis carolinensis). Proceedings of the Royal Society of London B: Biological Sciences 279: 2841-2848

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