Mechanisms of Invasion and Competition in Anolis sagrei and Anolis carolinensis lizards in southeastern Louisiana

Invasive species can have a variety of effects on the behavior and ecology of native species. Currently in New Orleans, Louisiana, both A. sagrei and A. carolinensis lizards are relatively abundant, but the A. sagrei population is expanding rapidly. I used a combination of laboratory and field studies to investigate factors that might be influencing local dominance of invasive A. sagrei over native A. carolinensis populations, including habitat use, display behavior, interspecific aggressive interactions, and plasticity. When comparing display behavior and habitat use in anole populations across three field sites in southern Louisiana, I found differences in male display behavior of both species, and also that A. carolinensis perched higher when A. sagrei was present. In staged interspecific interactions, I discovered that A. sagrei females achieved consistently higher aggressive scores than A. carolinensis females, suggesting that female interspecific behavior is probably more important than male behavior in driving changes in habitat use. Lastly, I studied plasticity in several morphological and whole-organism performance variables by rearing males and females of each species on two different perch diameters. I found that sprinting performance in A. sagrei was significantly different between treatment groups, although the morphological differences between perch treatments were subtler than those reported in previous studies. I also found that A. carolinensis females exhibited significant differences in both sprinting and clinging performance, despite no significant differences in male or female morphology between perch size treatments, highlighting the potential for both species-specific and sex-specific plasticity

Mechanisms of Invasion and Competition in Anolis sagrei and Anolis carolinensis lizards in southeastern Louisiana

Invasive species can have a variety of effects on the behavior and ecology of native species. Currently in New Orleans, Louisiana, both A. sagrei and A. carolinensis lizards are relatively abundant, but the A. sagrei population is expanding rapidly. I used a combination of laboratory and field studies to investigate factors that might be influencing local dominance of invasive A. sagrei over native A. carolinensis populations, including habitat use, display behavior, interspecific aggressive interactions, and plasticity. When comparing display behavior and habitat use in anole populations across three field sites in southern Louisiana, I found differences in male display behavior of both species, and also that A. carolinensis perched higher when A. sagrei was present. In staged interspecific interactions, I discovered that A. sagrei females achieved consistently higher aggressive scores than A. carolinensis females, suggesting that female interspecific behavior is probably more important than male behavior in driving changes in habitat use. Lastly, I studied plasticity in several morphological and whole-organism performance variables by rearing males and females of each species on two different perch diameters. I found that sprinting performance in A. sagrei was significantly different between treatment groups, although the morphological differences between perch treatments were subtler than those reported in previous studies. I also found that A. carolinensis females exhibited significant differences in both sprinting and clinging performance, despite no significant differences in male or female morphology between perch size treatments, highlighting the potential for both species-specific and sex-specific plasticity

Genomic analysis of macro- and micro-evolution in the reptilia

Recent advances in high-throughput, genomic sequencing allow unprecedented insight into the evolution of biodiversity. Chapter 1 of this thesis is a phylogenetic study of 1,145 sequenced loci, isolated using a novel high-throughput sequence capture methodology to address the phylogenetic position of turtles within tetrapods. The results reported here unambiguously place turtles as sister to archosaurs and resolve this long-standing question. Chapter 2 investigates the genetic basis of colorful pigmentation in the Green anole (Anolis carolinensis) by sequencing complete transcriptomes from the green dorsal, white ventral and pink dewlap skin. Anoles comprise an adaptive radiation of more than 400 species and color plays a central role in their ecology and evolution, but little is known about the genetic basis of colorful pigmentation in any vertebrate. This study identified 1,719 differentially expressed genes among the three differently colored tissues. Twenty-three of these genes are involved in melanin, pteridine, and carotenoid pigmentation pathways that contribute to the coloration of anole skin. Identifying candidate genes for colorful pigmentation is a significant advance that opens the field for comparative analysis in other taxa. To determine if the genes identified in Chapter 2 are involved in population divergence and speciation, Chapter 3 investigates the complete genomes of twenty individuals from two closely related subspecies of Anolis marmoratus. While the two subspecies differ markedly in pigmentation, this study found few genetic differences between populations except in five regions of the genome, which together contained 447 genes. Of these genes, only two, melanophilin (mlph) and 'cluster of differentiation 36' (cd36), are associated with pigmentation. The intersection of the genes identified in Chapter 2 and Chapter 3 includes both cd36 and mlph, suggesting that both are involved in divergence of coloration. Cd36 is of particular interest because it regulates the uptake of carotenoid pigments and is an important candidate gene contributing to carotenoid pigmentation. Together, this research demonstrates the power of genomic approaches to address fundamental questions in systematics, micro-evolution, and speciation. The findings bolster the emerging field of phylogenomics and broadly impact future research into the genetic basis of coloration in vertebrates

Anolis Newsletter VII

Newsletter for the 7th Anolis Symposium, Fairchild Tropical Botanic Gardens, Miami, Florida, 17-18 March 2018. It had been nearly a decade since the previous Anolis symposium was held in Cambridge, MA, at the Museum for Comparative Zoology, Harvard. A reunion of anole biologists en masse was long past due and it was decided that this symposium would be slightly different – we were going to hold it somewhere with anoles! And so, on the weekend of 17-18th March, 2018, nearly 70 anole biologists traveled to sunny south Florida to attend the 7th Anolis Symposium held at the beautiful Fairchild Tropical Botanic Gardens in Miami. In the grounds of the botanical gardens, attendees were presented with a diverse community of six (!) species of anole, both native and non-native, representing four distinct ecomorphs

Out of Florida: mtDNA reveals patterns of migration and Pleistocene range expansion of the Green Anole lizard (Anolis carolinensis)

Anolis carolinensis is an emerging model species and the sole member of its genus native to the United States. Considerable morphological and physiological variation has been described in the species, and the recent sequencing of its genome makes it an attractive system for studies of genome variation. To inform future studies of molecular and phenotypic variation within A. carolinensis, a rigorous account of intraspecific population structure and relatedness is needed. Here, we present the most extensive phylogeographic study of this species to date. Phylogenetic analyses of mitochondrial DNA sequence data support the previous hypothesis of a western Cuban origin of the species. We found five well-supported, geographically distinct mitochondrial haplotype clades throughout the southeastern United States. Most Florida populations fall into one of three divergent clades, whereas the vast majority of populations outside Florida belong to a single, shallowly diverged clade. Genetic boundaries do not correspond to major rivers, but may reflect effects of Pleistocene glaciation events and the Appalachian Mountains on migration and expansion of the species. Phylogeographic signal should be examined using nuclear loci to complement these findings.Organismic and Evolutionary Biolog

Hurricane Irma induces divergent behavioral and hormonal impacts on an urban and forest population of invasive Anolis lizards: evidence for an urban resilience hypothesis

Hurricanes can have both profound short-term effects on animal populations and serve as long-term drivers of evolutionary change. Animals inhabiting varying habitats may differ in their response to hurricane impacts. Increasing evidence sug- gests that animals from urban areas exhibit different behavioral and physiological traits compared to rural counterparts, in- cluding attenuated hormonal stress responses and a lowered propensity for flight behavior. A unique opportunity was pre- sented when Hurricane Irma hit Florida on 10 September 2017 and interrupted a study of invasive brown anoles (Anolis sagrei) at an urban and a forest. Using data collected before and after Hurricane Irma, we documented that forest anoles exhibited a greater avoidance of people and more male territorial behavior for a longer period of time following the hurri- cane. Post-hurricane both populations increased corticosterone concentrations post-capture stress, but urban anoles recov- ered 2 weeks faster than forest conspecifics. A dexamethasone suppression experiment suggested that these population dif- ferences were the result of forest anoles having a less effective negative feedback regulating corticosterone secretion. In the brain, forest anoles had higher corticosterone concentrations within the amygdala and parts of the cortex associated with stress than urban lizards. One explanation may be Hurricane Irma brought flooding and debris that altered the landscape leading to behavioral instability, and urban lizards already exhibited ecological adjustments that permitted a more rapid re- covery (i.e. the ‘urban resilience’ hypothesis). Testing if urban animals are more resilient to natural disasters can inform conservationists interested in understanding their role in facilitating invasive species expansion and what their increasing presence may indicate for animal populations

What makes a lizard invasive? Behavioral and neural correlates of invasion success

To understand what makes an invasive species successful, we must understand the behavioral mechanisms these invaders employ. In this study, I examined traits associated with the “boldness” behavioral syndrome (i.e., aggression, general activity levels, and behavioral flexibility), and the morphology of brain regions associated with those traits. I assessed boldness by conducting a series of four behavioral tests designed to measure aggression towards prey, aggression towards a conspecific, overall activity in an open field test, and flexibility in completing a novel task. I compared these measures in two species pairs: the native green anole (Anolis carolinensis; n = 12) and the invasive Cuban brown anole (Anolis sagrei; n = 15), and the native Texas banded gecko (Coleonyx brevis; n = 4) and the invasive Mediterranean house gecko (Hemidactylus turcicus; n = 8). I found that the brown anole was “bolder” than the green anole in two of the four behavioral tests conducted, but there was no difference between the two gecko species for any of the behavioral tests conducted. In contrast to my predictions, the native green anole had a larger relative brain mass (a general indicator of behavioral flexibility) and a relative total brain volume than the invasive brown anole. Green anoles also had larger neuron somas in the ventromedial nucleus of the amygdala and the medial cortex (regions associated with the boldness behaviors), contradicting my predictions. However, the Mediterranean house gecko had a larger relative brain mass than the native Texas banded gecko, consistent with the predicted pattern. I also found several within species relationships between behaviors expressed during the trials and the brain regions with which I predicted they would be associated. Together, these results provide one of the first studies of the relationships between brain and behavior in invasion biology

The effects of social and physical interactions on lizard morphology, behavior, and ecology

Interactions with the physical and social aspects of an animal’s surroundings direct the trajectory of local adaptation and can lead to tremendous diversity within and across taxa. In my dissertation, I explored how interactions between lizards and their environment lead to morphological, behavioral, and ecological diversity. First, I examined how a common, but unexplored habitat characteristic, perch flexibility, affects jumping performance of an arboreal lizard. I found that in the lab, green anole lizards (Anolis carolinensis) did not take advantage of the natural recoil of the flexible perches, and suffered decreased jump distance and takeoff speed as a consequence. Next, I extended my inquiry into how this habitat characteristic affects multiple aspects of behavior and morphology of the lizards in nature, given the potential performance costs associated with flexible perches. Most strikingly, I found that while green anoles used a range of perches in their habitat for most activities, they selectively jumped from relatively non‐flexible perches. Then, I sought to more broadly understand the effects of habitat on the whole organism. I examined associations between habitat structure and complexity on male and female sexual and non-sexual traits, as these would reflect habitat effects on locomotion, foraging ecology, and social interactions. I found that while there was no association between habitat structure and variation in most traits I examined, male body condition decreased with decreasing vertical vegetative complexity. Finally, I focused on the role of social interactions in increasing morphological diversity. I examined the association between genital morphology and male mating type in an alternative mating strategy population of the terrestrial lizard Uta stansburiana. I found that male mating types differed in genital length and complexity, suggesting that strong sexual selection may drive morphological differentiation within populations. Together, my work shows the importance of animal-environment interactions as drivers of diversity and contributes to the broader fields of sexual selection, behavior and evolutionary ecology

Manipulating Testosterone to Assess Links between Behavior, Morphology, and Performance in the Brown Anole Anolis sagrei

Survival and reproductive success are determined by the complex interplay between behavior, physiology, morphology, and performance. When optimal trait combinations along these various phenotypic axes differ between sexes or across seasons, regulatory mechanisms such as sex steroids can often facilitate sex‐specific and/or seasonal trait expression. In this study, we used surgical castration and replacement of exogenous testosterone in adult male brown anoles (Anolis sagrei) to simultaneously examine the effects of testosterone on a suite of morphological (dewlap area, body size), physiological (immune function), behavioral (dewlap, head bob, and push‐up displays), and performance (stamina, sprint speed, bite force) traits. We show that testosterone increases (or castration reduces) growth rate, dewlap area, and bite force. Treatment effects on bite force may simply reflect underlying treatment differences in growth combined with allometry of bite force. Other traits, such as stamina, sprint speed, and rate of behavioral displays, were largely independent of circulating testosterone levels. Although we did not observe significant treatment effects on immune function, we found negative correlations between growth and immune function consistent with the hypothesis that testosterone mediates trade‐offs between these competing aspects of energy allocation. Overall, our results demonstrate that testosterone can exert pleiotropic effects on a variety of morphological, physiological, behavioral, and performance traits that are known to influence survival and reproductive success