I am an Associate Professor at the Univeresity of St. Thomas in St. Paul, MN. My research focuses on understanding how the processes of natural and sexual selection shape physiological and morphological traits. I study anoles to understand life-history tradeoffs and how endocrine systems evolve to modulate social behavior.
Anolis sagrei has impressive sexual size dimorphism, but what causes it? (Photo by Bob Reed)
Sexual dimorphism is always a hot topic at SICB, and this year it was no exception for anoles (1, 2). Christian Cox, a postdoc in the laboratory of Bob Cox (no relation) at the University of Virginia, sought to explain how testosterone might lead to phenotypic divergence in a number of sexually dimorphic traits. As many of us are aware, sexual dimorphism varies widely among lizard species, and evolutionary shifts to and away from dimorphism are common, including in anoles. Testosterone has been shown to be an important regulator of growth in several lizard species, so Cox experimentally tested this effect in Anolis sagrei.
Both males and females were given a testosterone or blank implant and allowed to grow to maturation. One group was manipulated as juveniles, just as phenotypic divergence was beginning, and the other group was manipulated as subadults after divergence. Testosterone addition increased growth in body size and mass, increased metabolic rate, increased dewlap size, and changed dewlap coloration in both sexes and both juveniles and subadults. Fat storage was reduced as expected, in both sexes and age classes. These results are intriguing, because a sex difference in testosterone production may play a role in the degradation of between-sex genetic correlations. The next question is how that happens, as both sexes produce testosterone, just to different extents.
Although sexual dimorphism is found in many animal species, the mechanisms by which it evolves remains a hot topic. Selection may favor different phenotypes in the two sexes, but sharing a genome may put constraints on if and how sexual dimorphism might evolve. Many anoles have sexual dimorphism, of course, but the degree to which they are dimorphic varies quite dramatically. Robert Cox studied how between-sex genetic correlations in Anolis sagrei, a very dimorphic species, might degrade over ontogeny to result in divergent male and female phenotypes.
Anolis sagrei displays marked sexual dimorphism. (photo from Bob Cox’s website)
Using a large breeding colony of brown anoles from the Bahamas, Cox found that between-sex genetic correlations were lowest for traits that are the most dimorphic, like body size. Even more interestingly, the correlations change as the individuals get older. Whereas juvenile anoles have high between-sex genetic correlations for most traits, those correlations decrease around sexual maturation, most strongly in those traits that are dimorphic. This suggests that the pronounced divergence in phenotype seen in adults is associated with a degradation of the between-sex genetic correlations for those traits. Cox is currently exploring what mechanisms lead to this degradation, and is especially interested in whether testosterone is a major player.
A non-anole regular on Anole Annals (e.g., 1, 2, 3) made an appearance at SICB this year. Not the species itself, but a fascinating presentation by Ambika Kamath on population variation in dewlap dimorphism in Sitana ponticeriana. Kamath presented information on display behavior for three color variants of Sitana: uncolored, colored, and intermediate. She wondered whether the three geographically separated variants display differently and whether the dewlap variation might be due to environment or sexual selection.
Coloured-fanned, intermediate-fanned, and white-fanned male Sitana ponticeriana. Photographs by Shrikant Ranade, Jahnavi Pai, and Jitendra Katre respectively.
By studying eight populations of this species, Kamath found that the three variants did indeed display differently. The colored variants had long displays with remarkable head turns and twists (wow, there was some amazing video!). The uncolored variants had body position changes, but no head turns and twists. Finally, the intermediate variants simply had short displays with no head turns or body position changes. Multivariate analysis of behavior clearly separated the populations based on color variant. Also, they flick that throatfan VERY quickly!
Based on the available data, it seems unlikely that environmental variation in habitat type or vegetation explains the variants, but sexual selection does appear possible. Colored dewlaps are associated with male-biased sexual dimorphism, whereas the uncolored variants have no dimorphism or female-larger dimorphism. Further, scaling of dewlap area to body size revealed that the colored and intermediate variants have evolved large dewlaps in different ways. This also supports Kamath’s proposal that there are multiple origins of large dewlaps and colorful dewlaps within the distribution of this widespread species. Future research will no doubt be of interest to us at Anole Annals and beyond!
A figure from Quinn’s poster, showing alternative possible energy budgets in green anoles (click for a better view).
Animals allocate energy that they acquire to a variety of bodily functions and activities. Some of the more important allocations are those toward metabolism and growth, though the relative allocations to these is unclear. McKenzie Quinn, an undergraduate student working with Michele Johnson at Trinity University, presented her work in the third poster session on the dynamic energy budget of green anole lizards. She quantified food intake, excretion, growth, and resting metabolic rate (RMR, the energy required for basic maintenance) of individual lizards over 40 days to create a predictive model to describe how they allocate energy. If metabolism receives a large allocation, then RMR and/or body mass are expected to be significant predictors of energy use. On the other hand, if growth is more important, then aspects of body length (snout-vent length, SVL) are expected to be better predictors.
Interestingly, she found that RMR and body mass were not included in the best model of energy use. Instead, their model building (with AIC criteria, if you’re interested) showed that a decreasing nonlinear function of SVL was the best model. This suggests that metabolic functions are a small, non-significant part of these lizards’ dynamic energy budget. This work was conducted on adult males, so it will of course be interesting to see how this approach might apply to younger individuals or females. However, this is useful information to know for those who wonder how anoles allocate energy in their daily lives.
A figure from Eric Mueller’s poster showing the conserved pathway of how growth hormone may affect body size.
Anyone familiar with Anolis lizards is aware of the dramatic variation in body size. Think dwarf twig anole and crown giant. Although the ecological and evolutionary processes that can lead to such variation in body size have been studied, it is still unknown what physiological mechanism explains the variation we see today. Eric Mueller, a graduate student at Southern Illinois University – Edwardsville, presented a poster asking just that question. Specifically, do differences in circulating levels of plasma growth hormone regulate evolutionary changes in body size among anole species of differing size and morphology?
Anolis carolinensis (L) and A. equestris (R) have dramatic differences in body size but not in growth hormone levels. (photo 1, 2) Species not to scale.
Growth hormone (GH) is secreted by the pituitary gland and has many functions in the body, including promoting muscle and bone growth and increasing protein synthesis (among many, many other things!). It seems a logical candidate mechanism to investigate when it comes to explaining variation in body size. Mueller looked at GH levels in three anoles of varying size: A. equestris, A. carolinensis, and A. sagrei. GH was higher in A. equestris and A. carolinensis than A. sagrei, supporting his hypothesis. However, there was no difference in GH levels between A. equestris and A. carolinensis despite dramatic differences in adult body size. Looking within species, GH levels were positively correlated with SVL only in A. equestris, and not the other two species.
Although differences in circulating GH may explain some size differences among anole species, as in other studies of anole hormones, things don’t seem to be simple. Mueller hypothesized that other aspects of the GH pathway may be more important. For example, GH receptors, Insulin-like Growth Factor (IGF) levels, and IGF-binding proteins should be examined for a full picture. The GH-IGF axis also interacts with other hormone pathways, such as testosterone, making this a very complex issue. Since endocrine systems are so multi-faceted, and multiple components have the possibility to evolve independently, there is lots of potential for future research that seeks to explain species differences in body size.
It was a real pleasure to see Dr. Ray Huey give a presentation that was inspired by research he and his collaborators began in the 1970s on seasonality of reproduction and behavioral thermoregulation in Puerto Rican Anolis cristatellus. Almost 40 years after the publication of that work, Huey and many of the same colleagues (and some new ones) returned to the same areas in Puerto Rico to examine how very fine-scale variation in thermal environment (a few meters!) might lead to variation in reproduction. The investigators (Otero, Huey, and Gorman) studied how reproduction differed between open areas (where lizards carefully thermoregulate) and forested areas (where lizards are thermoconformers) and found striking differences between them. Females in open habitats reproduced most of the year, whereas females in the neighboring forest decreased reproductive in a much more seasonal manner. Differences were largest from October – December, with females in forested habitats essentially shutting down reproduction during those months. This finding was true at two different sites.
These striking differences in reproductive phenology are similar in magnitude to differences seen along elevational gradients, but the difference here is the scale. The females that Huey compared were literally only a few meters away from each other. One important take-home message from these data is that reproduction can vary at the microgeographic scale just as it can at larger geographic scales. While the latter type of study is now common, the former isn’t. Future work should consider how small-scale variation in microhabitat use might influence reproduction so that we can better understand how general this phenomenon is.
One final point that Huey made was how collaborations can not only be an integral part of research, but also a source of personal reward as those collaborations continue over time and result in great friendships. He encouraged young investigators to keep this in mind as they progress through their academic careers.
Editor’s note: this research project has been the subject of previous posts [1,2].
Arginine vasotocin, the reptilian homolog to vasopressin is a potent modulator of social behavior. (photos from Wikipedia)
For many of us, hearing about arginine vasotocin (AVT), or its mammalian homolog vasopressin, conjures up memories from a physiology class about water balance and the antidiuretic effects of the vasopressin system. However, AVT is also a potent neuromodulator and neurotransmitter in the brain that has strong effects on social behavior, such as parental care and pair bonding. Although most of this behavioral research has been done in mammals and birds, it appears that AVT might have similar behavioral functions in anoles! Leslie Dunham, a graduate student at Georgia State University, experimentally assessed the effects of AVT on male and female green anole behavior. By comparing lizards injected with either AVT or a control solution, Dunham was able to examine the effects of AVT on aggression and courtship in males. The behavior of individuals in the two experimental groups was then assessed in the following contexts: aggression toward a mirror, aggression toward another male, and courtship toward a female. She found:
Decreased aggression toward a mirror.
No difference in aggression toward a size-matched male.
No difference in courtship behavior directed at a female.
AVT decreases aggression in other vertebrates, but the lack of an effect on courtship in anoles suggests that AVT may modulate behavior differently in male anoles compared to fish and birds.
But wait, there’s more! Not to be outdone by other types of vertebrates, females in the courtship trials showed some very interesting behavior. Although Dunham focused on the effects of AVT on male behavior, she also measured female behavior during the trials. She found that females displayed more toward males treated with AVT compared to control males. This was despite any detectable behavioral difference between the male treatment groups. Why is this? Although the answer is still unknown, Dunham proposed some plausible and testable hypotheses for what might be happening. First, there may be subtle changes in behavior brought about by AVT that weren’t detected. Second, there may be a role for chemical communication between the sexes during courtship that wasn’t measured. Anoles, and iguanian lizards in general, aren’t known for their reliance on chemical communication, so this possibility is sure to spark some interesting future research.
What’s going on inside their heads? The four anole species of South Bimini, The Bahamas.
Whenever I stand in the forest on South Bimini in the Bahamas, I’m always struck by the similarity of these anoles to those I’ve worked with elsewhere in the Greater Antilles. Yes, that’s the whole idea behind the ecomorph concept, but as many have pointed out recently, habitat use and morphological convergence are only part of the story. Along with the classic divergence and convergence in body size and shape, the ecomorphs also show intriguing convergence in sexual size dimorphism and social behavior. It’s this latter aspect of the Caribbean anoles that interests me. How has this convergence in behavior, though it’s not perfect, happened? Have the proximate mechanisms that are responsible for anole behavior evolved in the same way on the various islands in the various ecomorphs? From a larger perspective we are asking, how do neuroendocrine systems evolve? That’s what my students and I are trying to figure out, and that’s why we’re in the Bahamas right now.
A few years back, Matt Lovern and I started a project examining circulating steroid hormone levels in four anole assemblages (The Bahamas, Puerto Rico, Dominican Republic, and Jamaica). Based on a plethora of work in a variety of vertebrate species and their testosterone-behavior relationships, we predicted that we would find consistent intra-island differences among ecomorphs in testosterone (and corticosterone), with the ever-charismatic trunk-ground anoles showing the highest levels. Boy, were we in for a surprise. We did find species differences, and we even found consistent ecomorph differences, but not like we expected. Unlike the mainland green anole (Anolis carolinensis) and the introduced brown anole (Anolis sagrei) on the mainland (yes, the apparent difference in testosterone levels between mainland and Caribbean brown anoles is probably a separate, interesting story!), trunk-ground anoles in the Caribbean have very low baseline testosterone levels. Twig anoles, on the other hand, are super-juiced with testosterone. I won’t give the whole story away, as we are working on getting it published, but the take-home message is that hormones are only part of the story, and testosterone likely plays very different roles in the behavior of the various species and ecomorphs. While this may not sound surprising to some, in some ways it is, because typically people only focus on circulating hormone levels to explain behavior, and testosterone levels tend to be pretty good predictors at a large scale. Although many proclaim that it’s not the hormones but the receptors, nobody has examined hormone receptor distributions in target tissues across a large number of closely related species. Again, that’s what we’re trying to do here in the Bahamas (and elsewhere).
We’ve been spending our time here on Bimini collecting brains for analysis of several potential regulators of social behavior in multiple brain regions known to be important in anole aggression and courtship behavior. My student Allison, who is here with me now, got some funding to spend the rest of the summer back in Minnesota sectioning and staining brains from the four ecomorphs here on Bimini. We’ve also been conducting “GnRH challenges” on these species to determine whether the baseline levels of testosterone that we’ve measured are as high as they can go. That is, when we physiologically stimulate the hypothalamus-pituitary-gonad axis to produce more testosterone, is it capable of doing so, and are there differences among species in that response? I’ll be spending the rest of my summer running those samples to find out. This will complement the social challenges that Matt Lovern and I conducted in the Dominican Republic last year on Anolis cybotes and Anolis coelestinus, examining whether social challenges result in increased testosterone.Stay tuned to see what we find!
Anoles have served as great model organisms in studies of adaptive radiation and how form and function are molded by selection, but they have also been the center-piece for some of the most interesting (and classic) research on how the brain modulates aggression to determine dominance. For example, work by Cliff Summers and his laboratory (among others) over the years has provided great detail concerning how adrenal catecholamines and glucocorticoids, produced during “stressful” aggressive interactions, interact with serotonergic activity in the hippocampus to determine social rank. These neuroendocrine processes are outwardly expressed, in a sense, by the familiar eyespot seen prominently during male green anole (Anolis carolinensis) interactions. The formation of the eyespot is stimulated by catecholamines, and the latency of eyespot formation is dependent on serotonergic activity, which is influenced by glucocorticoid secretion. Males that develop the eyespot sooner tend to be dominant, and once eyespots have appeared in one combatant, aggression in the rival tends to be inhibited. At least that’s the way it seems to work in A. carolinensis.
