We perviously learned about new research on the mechanisms of dorsal crest erection in the brown anole, Anolis sagrei, being done by the Rand Lab at Carleton College. This is a interesting new research area with relevance to our understanding of anole signaling and anatomy that is being carried out by Rand and a team of impressive undergraduate students. Rand Lab student, Morgan Gerace, presented a second Rand Lab poster on this topic at SICB 2015. Following up on the first poster, in which the authors found no evidence of the involvement of muscles, cartilage, or vascular sinus in crest erection, Morgan tested whether crest erection is due to an inflammatory response. By injecting male anoles with the an adernegenic receptor antagonist, interfering with the lizard’s fight-or-flight response, Morgan determined that crest erection may be the result of an inflammatory-like response. Conversely, injection of with epinephrine, essentially supercharging the fight-or-flight response, facilitated a crest erection response. This exciting work by this set of motivated undergraduates draws new attention to the physiological control mechanisms of this under-studied display mechanism.
Author: Thomas Sanger Page 2 of 6
Thom Sanger is an Assistant Professor at Loyola University in Chicago. His lab specializes on understanding the developmental bases of Anolis lizard diversity.
Squamates vary widely in the magnitude and direction of body size dimorphism, which refers to the tendency for the sexes to exhibit different body sizes. Some lineages possess male-baised dimorphism while others have female-baised. The effects of testosterone on mediating sexual size dimorphism in different squamate lineages has long been the study of the Cox lab at the University of Virginia. Christian Cox (of no relation to his advisor) has now reported some exciting steps forward in the search for the mechanisms regulating body size dimorphism in the brown anole, Anolis sagrei. Cox is in the process of carrying out a transcriptome-wide analysis of the genes responsible for sexual dimorphism, with particular focus on examining the genes along the insulin growth factor-growth hormone axis (IGH-GH), which is the same pathway that was reported about yesterday. In his experiment Cox implanted testosterone pellets under the skin of juvenile male and female lizards and then looked for differences in size and gene expression. Increased levels of circulating testosterone prompted increases in body size in both males and females grew to larger sizes, indicating that females have not lost the ability the respond to testosterone. But to better understand the growth axis controlling this difference Cox took a large step forward by also comparing gene expression in the liver of experimental (implant) and control (intact) animals. As the liver is a major regulator of growth via its regulation of the IGH-GH, Cox expected that this tissue would respond to testosterone treatment. This is precisely what Cox found. Specifically, he found a number of genes that are naturally regulated in different ways in males and females and additional genes that responded to the testosterone treatments. To conclude, Cox pointed out that an important next step will be to compare castrated lizards to those intact lizards with the testosterone implant to more clearly elucidate the gene network directly responding to testosterone. But perhaps the most exciting work will come with Cox and his collaborators examining the growth mechanisms of species with male-baised and female-baised patterns of dimorphism to more thoroughly understand how evolution has reshaped these gene regulatory networks during squamate evolution.
From the diminutive twig anole to the monstrous crown-griant anoles, Anolis lizards vary dramatically in their body size. Much research has focused on the patterns of body size variation among Caribbean species, how changes in body size are correlated with habitat differences among species, and rates of body size evolution upon invasion to new islands, yet an important question remains to be addressed in this body of literature, “how do anoles change body size?” S. Griffis and Dr. D. Jennings of Southern Illinois University at Edwardville are attempting to address this among Cuban anoles by searching for DNA sequence differences in known growth factories. But they are using what might be considered an unlikely model for lizard body size variation: dogs. Several years ago, Elaine Ostrander’s lab at the NIH uncovered that coding differences in the growth factors IGF were responsible for the body size variation in dogs. To a mechanist like myself, it was a surprise that this variation could be traced to coding differences in the genes, not to the levels of circulating growth factors. The authors of this poster are following Ostrander’s lead by looking for coding differences in genes involved with the IGF growth axis. But to keep their options open they are also collecting data on circulating hormone levels. When complete, if there are differences in the IGF growth axis contributing to differences in body size, Griffis and Jennings will find it.
On the first day of SICB 2015 Robert Cox gave an interesting talk about reproductive investment and sexual selection in lizards. At the center of his talk was the striking notion that males and females are different biologically, yet should still be integrated into cohesive theories of sexual selection. According to Dr. Cox, past theory has generated mutually exclusive ideas about the costs of reproduction for each sex. Whereas theories about females have focused on life history and investment in the egg and offspring, theories about males have focused on mating investment. Cox stressed that this is overly simplified and doesn’t reflect biological reality, as males and females also share many of the same costs of reproduction as well. Issues like growth, survivorship, energy storage, and parasite load are shared between the sexes. Dr. Cox is now trying to test how sex-specific reproductive mechanisms affect these shared reproductive constraints by surgically removing the gonads of each sex. Preliminary analyses show that parasite load appears to be a shared effect among the sexes regardless of the underlying mechanism (testosterone derived from testes versus estrogen derived from the ovaries). Studies directly comparing the underlying mechanisms of sexual dimorphic anatomy, physiology, and behavior are critical for the further development of sexual selection theory and for improving our understanding of anoles. Studies like Dr. Cox’s are an important step in that direction.
How do lizards move in nature? Note the added emphasis on “in nature.” For many years people have studied the mechanics and patterns of of lizard movement and anoles have played an important role in this research. But today Jerry Husak of the University of St. Thomas in St. Paul reminded us that most of this research has focused on characterizing maximum performance ability, despite the fact that animals rarely achieve this level of activity in nature. For example, most of the time many lizards are merely scurrying about on the ground and not sprinting at their full ability. Hence, although measuring maximal spring speed in the lab is a common theme, this measurement may not actually reflect what animals do in nature. Dr. Husak also stressed to the audience that animal locomotion is context dependent. Specifically, a lizard’s speed depends on whether it is moving in grass or over rocks, and whether it is foraging or fleeing from a predator. During his enlightening discussion, which included a description of him trying to sprint on a frozen Minnesota sidewalk, Dr. Husak described a series of biotic and abiotic factors that should be incorporated into models of terrestrial lizard movement. Finally, he concluded by challenging our obsession with maximum sprint speed once again by asking whether running at top speed can lead animals to make to costly mistakes. Based on a set of foraging data, he showed that this may be the case. Dr. Husak’s talk highlighted the importance of understanding the natural habits of lizard behavior and performance.
SICB 2015 is off and running and what better way to kick it of than with a lizard talk? Phillip Bergmann of Clark University filled the 8:15 time slot on day one with an intriguing evaluation of broad-scale body shape convergence among squamates. This is a perennial topic on Anole Annals due to the well-studied patterns of convergence among Anolis lizards and, indeed, Dr. Bergmann highlighted anoles early in his talk. He asked whether common functional (ecological) situations lead to body shape convergence at large scales. Rather than search for global patterns of convergence, Dr. Bermann used hypotheses specific to the transformations that occur when lineages transitioned into new habitats. As he pointed out, it is not surprising to find convergence in body shape occurring throughout squamate – after all, convergence is ubiquitous across the tree of life. He concluded his talk highlighting what he feels are some of the most pressing “Big Questions” regarding convergence which included the methods we use to detect convergence, the role of constraints in shaping convergence, and elucidating the mechanisms underlying convergence. Ultimately it was a thought-provoking talk both from the perspective of squamate organismal diversity and the topic of convergence more broadly.
I probably would have never said this a few years ago, but penises are absolutely fascinating. The phalluses of terrestrial vertebrates exhibit an incredible diversity of shapes and sizes with some possessing elaborate coils, barbs, bony spines, and multiple lobes. Many of us learn about the rapid evolution of sexual characters in our undergraduate classrooms, but until recently I, for one, did not fully appreciate the striking diversity of this organ until immersing myself in the subject area.
Many biologists study the penis under the umbrellas of different research disciplines, but relatively little work has been performed to explain its anatomical diversity. For example, how many times has a penis/phallus evolved among terrestrial vertebrates? This may seem like a trivial question, but the diversity in form, function, and physiology in the adult phallus actually makes this question difficult to address. Historically there has been much conjecture, but little data to support whether the mammalian penis, squamate hemipenes, and phallus of turtles, crocodilians, and basal birds share a single evolutionary origin or are independently derived. But where comparative anatomy has struggled, comparative developmental biology has recently forged ahead. Within the last several months two independent groups have published a total of seven new research articles that help us resolve the question of phallus homology.
I previously wrote about a series of five papers published from the Cohn lab (University of Florida) describing the embryology and gene expression patterns for the developing phallus. Since then this group has published a sixth paper synthesizing this wealth of information, using it to lay out a number of outstanding questions regarding phallus development and evolution. More recently, the Tabin lab (Harvard University) published a paper comparing the cellular-level origins of the genitalia in the laboratory mouse, green anole, house snake, chick, and python. I have had the distinct pleasure of working with both groups as their “anole guy.” Although these studies vary widely in their experimental and comparative breadth, together they have shed much needed light on the evolution of vertebrate genitalia. Here my goal is to discuss how this new wave of research changes what we now know, what we don’t know, and what we think we know regarding the evolution of external genitalia among vertebrates. Take a look at the original research papers for details of the developmental analyses, which represent many technical steps forward in our use of anoles as a laboratory model system and intellectual advancements in our understanding of genital development.
During the gradual transition of life onto land, vertebrates evolved the amniotic egg to facilitate their departure from moist environments.
A recent paper by Matt Helmus, Luke Mahler, and Jonathan Losos highlighted the ways in which globalization has influenced the distribution of Caribbean Anolis lizards. At the heart of this research was the relationship between commercial shipping traffic and lizard biogeography. Two more recent observations can now extend these findings well beyond the Caribbean, much, much farther north.
First, Twitter user Vlen Puppehface recently posted a story about a stow away green anole that he found on pallet in Edmonton, Canada. This was a shipment of oil field supplies that originated in Houston, TX and that took ten days to reach its destination. This male green anole survived the trip all the way to Canada and is now housed in a new terrarium. The tweet originally posted October 16th and since then the anole has shed and appears to have adapted well to its new home.
In separate case of stowaway lizards, another anole survived a transatlantic journey to Denmark in a shipment of bananas and was discovered incapacitated on the floor of the stockroom where incoming bananas are fumigated. The photo is too small for me to be certain, but this appears to be an Anolis cybotes female. According to the original post by Randi Duun in the “Anoles” Facebook group, the shipment originated in Colombia, Costa Rica, or the Dominican Republic so this would be consistent with an A. cybotes hitchhiker. It would be interesting to know how long a shipment like this takes, but I bet that it is longer than ten days port-to-port. Regardless, just like the globetrotting green anole, this anole is healthy following its journey, housed in a terrarium and enjoying Danish mealworms.
In contrast to the research described by Helmus et al, it is probably safe to assume that despite the perseverance of these anoles, and any others that make their way towards the arctic circle in subsequent shipments, escapees will not be establishing viable introduced populations.
Regular readers of Anole Annals may remember the “Find the Anole” series that has been popular over the last few years. It has been a while since we enjoyed such fun times, so I wanted to breathe new life into this classic challenge.
Earlier today I visited Dinosaur World in Plant City, Fl. and enjoyed the contrast between Mesozoic and Cenozoic reptile diversity. It was very exciting. Below are two images from their grounds for your enjoyment. Can you find and identify the anoles in these photos? A far bigger challenge may be to identify the dinosaurs illustrated by these statues.
On a separate note, if you are ever passing through central Florida with your families, stop by Dinosaur World. The interpreters were quite good with our kids, there are over 200 life-sized (and colorful) dinosaur statues, they clearly state that the earth is 4.5 billion years old, and there are no humans riding dinosaurs. I was pleasantly surprised by all of this in this part of the country. Its worth a few hours of your time!
There is considerable variation in phallus morphology among the major groups of amniotes (phallus used herein to be inclusive of both the penis and clitoris). Just for starters, while most clades – including mammals, birds, turtles, and crocodilians – have a single midline phallus, squamates have paired hemiphalluses. Although herpetologists have long appreciated morphological variation in the hemipenis for its systematic value, understanding the nuances of anatomical homology, homoplasy, and novelty at this larger scale has not been as widely addressed. Recently, the Cohn lab of the University of Florida (of which I am now a member) undertook this challenge from a developmental perspective, studying development of external genitalia in representatives of each reptilian clade: the ball python (Python regius), the pond slider (Trachemys scripta), three duck species, the American alligator (Alligator mississippiensis), and who else, but the green anole (Anolis carolinensis). A synthetic review of the complete series will have to wait for another post, but reprints of each paper are available on the lab’s website to hold over the most curious. But because of the growing interest in anole nether regions, I will briefly highlight the recent findings regarding hemiphallus development in the green anole.
The Wade lab has previously shown that both male and female green anoles develop similar hemiphalluses during the early stages of genital morphogenesis, which then later differentiate into sex-specific reproductive structures. Building upon this observation, Gredler et al. described the embryology of the green anole hemiphallus from the earliest stages of morphogenesis through sexual differentiation. Hemiphallus development begins around the time of oviposition when three sets of paired swellings appear between the cloaca and the developing hindlimb bud, reminiscent of what is observed in other amniote clades. These swellings expand and meet at the midline to form the external lips of the cloaca or remain lateral to the cloaca and mature into the hemiphalluses. Following morphogenesis, the male hemipenis continues to elongate as it forms its distinctive lobes and sulcus spermaticus while the female hemiclitores gradually regress into the cloaca. Further details of the developmental anatomy of internal reproductive structures and gene expression patterns of several key molecules associated with genital morphogenesis are described in the paper.
Although there is some variation among squamates in the relative timing of the emergence and fusion of the paired swellings associated with hemiphallus development, these results are largely consistent with classical embryological descriptions of squamate genitalia (summarized by Raynaud and Pieu in Biology of the Reptila volume 15). But the revival of this body of literature in a comparative and molecular context brings new research questions to our collective table. As discussed by Gredler et al., the seemingly modular relationship between the genital swellings, cloaca, and limb buds may be particularly interesting in the context of repeated body elongation and limb loss among squamates. Better understanding of the relationship between cloacal and phallus development may also shed new light on the mechanisms of reproductive isolation, the coevolution of male and female reproductive organs, and evolving patterns of sexual conflict. Furthermore, there remain open many mechanistic questions regarding the molecular patterning of the hemiphalluses and which processes are hormone dependent that can now be more thoroughly addressed using the newly available sex-specific molecular markers. Considering the growing literature on hemipenis variation and expanding access to genomic resources in Anolis, these may be particularly fruitful areas for future investigation.