Anole Annals

Anolis sagrei, the almost-ubiquitous brown anole, has spread across a broad geographical range that spans most of the Caribbean. The populations across this range, however, vary extensively in morphological traits. Graham Reynolds, currently a postdoc working with Liam Revell and Jonathan Losos, summarized this morphological variation and described a large-scale phylogeographic study of population differentiation in brown anoles in a talk at SICB on Tuesday.

The context of Graham’s study arose from Lister’s classic 1976 paper showing variation in the number of toe pad lamellae in brown anole populations from different Caribbean islands. Lister found that average lamellae number corresponded to average perch height. More recently, Veronica Gomez-Pourroy’s masters thesis work showed that brown anole morphology varies across mainland Central America, the Swan Islands of Honduras, and the Caribbean.

Graham’s genetic work expanded on the results of Kolbe et al. (2004) and included  samples collected by a large number of collaborators working in 95 localities throughout the Caribbean Basin. Using multilocus nuclear and mitochondrial data, Graham found a large split between the Eastern and Western Cuban clades of brown anoles. Populations from the Bahamas clustered with the Western Cuban clade, and populations from the Swan Islands and Central America were most related to populations from the southern populations of the Eastern Cuban clade.

Graham’s overall aim is to integrate morphology, behavior, and genetics from local to regional scales. Anoles seem to be the perfect group with which to tackle this goal!

A photo of Graham Reynolds holding a Hispaniolan boa. Photo from his website.

The substrate in which an egg develops affects the desiccation tolerance of the hatchling. Photo by Matt Lovern.

Anyone who has set up an anole breeding colony in the lab knows how critical it is to provide the lizards with an appropriate substrate, with the right moisture content, for egg laying and incubation. Yet, in the field, lizards utilize a wide range of available egg-laying substrates. Graduate student Corey Cates in Dan Warner’s lab at the University of Alabama, Birmingham, considered the fitness implications of different egg substrates in a talk in the DEE (Division of Ecology and Evolution) Huey Award Competition for Best Student Presentation at SICB this week.

Corey studied populations of brown anoles (Anolis sagrei) on spoil islands in Tomoka State Park in Florida. Some of these islands contain organic soil and others are covered in broken shell pieces – substrates that differ in both physical structure and moisture content. Corey collected eggs from a laboratory population and incubated them in the lab under “wet” and “dry” conditions in both substrates. He then measured hatching rate, hatchling size, and desiccation tolerance, and his experimental results were striking: hatchlings from the dry soil treatment lost less water than the other treatments in the desiccation tolerance test! When Corey released the hatchlings in the field onto the different types of islands, he found that dry soil hatchlings had higher success than hatchlings from the other treatments on the dry (shell) islands, whereas wet and dry treatment hatchlings survived equally well on wet (soil) islands. Corey also found that the moisture level of the incubation substrate was more critical to hatchling success than the substrate type.

Overall, the adaptive significance of the plastic responses demonstrated in this study is intriguing. Corey’s next steps will include a study of one of the possible mechanisms underlying these results – whether scale number differs between hatchlings in the different moisture treatments.

Juvenile anoles seem to utilize very different habitats than adults of the same species. Could this be a product of intraspecific competition between age classes?

Juvenile brown anole. Photo originally posted by Nick Cairns on AA.

David Delaney, a master’s student in Dan Warner’s lab at the University of Alabama, Birmingham, set out to answer this question using brown anoles (Anolis sagrei), and presented a poster describing his experimental study at SICB this week. He manipulated the densities of adult lizards cohabiting with 6 juvenile lizards within mesh enclosures containing artificial trees in five treatment groups. These groups were: (1) no adults; (2) 1 adult male; (3) 1 adult female; (4) 3 adult males; (5) 3 adult females. Unexpectedly, adult density did not affect the microhabitat use (perch height, perch width, or substrate composition) of juvenile lizards in the enclosures.  However, when three adult male lizards were present, juvenile survival rate decreased and larger juveniles were more likely to survive. These results are intriguing because adult males are a selective force on juveniles, yet in this study, juveniles did not alter their microhabitat use in response to adults. The next question, then, is what is causing the distinct habitat use differences between adults and juveniles in the wild?

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

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

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.

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!

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.

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.

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).

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.

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.

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 Kahrl’s website.