Structure and Evolution of Dragon Brains

Abstract

This thesis is about the evolution of brain structure in lizards, with a particular focus on the agamid lizards of the genus Ctenophorus. Achieving this required advancing the methods with which to study lizard brains. Therefore, this thesis is split about equally between developing the tools to study lizard brain structure and the evolution of brain structure in Ctenophorus. Below I present short summaries of each chapter. Full abstracts are presented with each chapter.

Section 1: Development of the framework and tools necessary for the study of the dragon brain Chapter 1 Among vertebrates, reptiles have lagged far behind birds, mammals, fishes and amphibians in neurobiological research. Nonetheless, in the past twenty years there have been significant advances in our understanding of the neurobiology of reptiles, particularly among squamates (lizards and snakes). The first chapter of this thesis presents a broad literature review of lizard brain research. All peer-reviewed publications since the last major review in 1998 are summarized to give a complete overview of the state of the published literature on squamate neurobiology. I use this overview to highlight what is unique about squamate brains and identify gaps that remain in our understanding of these systems. Finally, I provide a framework for future studies that includes exciting new and unanswered questions about squamate brain evolution, structure and function.

Chapter 2 Perfusion is the most common technique for preserving brains for neuroscience research. Standard perfusion techniques were developed primarily for application in mammals, which are traditional neuroscience research models. A perfusion method has never been published for lizards and following mammalian perfusion protocols for lizards results in failed perfusions. In this chapter, I present a modified perfusion protocol suitable for lizards.

Chapter 3 In this chapter we present a magnetic resonance-based atlas for the brain of an agamid lizard, the tawny dragon (Ctenophorus decresii). We use literature sources as well as histological sections to identify and delineate, in three dimensions, the cell regions and fiber tracts visible in this model. This atlas has acted as a guide for measuring and analyzing brains in the subsequent chapters, and as a template with which to automate brain measurements across many individuals from multiple species.

Section 2: Evolutionary patterns in dragon brain structure Chapter 4 Two models have been proposed to explain the patterns observed in evolutionary changes in brain morphology: the concerted model and the mosaic model of brain evolution. It is now well understood that both models are relevant in explaining brain evolution but the relative influence of each mode on brain structure varies between vertebrate groups. It remains unclear what factors favour concerted or mosaic brain evolution. In this chapter, we found evidence for both mosaic and concerted brain evolution in dragon lizards. Brains showed a pattern of concerted brain evolution with respect to the morphological characters. In contrast, they showed a pattern of mosaic brain evolution with respect to ecological and life history characters.

Chapter 5 The role of sexual selection in altering brain organisation and structure over evolutionary time is poorly understood. In this chapter we compare the brains of species under strong and weak sexual selection. Males belonging to species that experience strong sexual selection had a larger medial preoptic nucleus and a smaller ventromedial hypothalamic nucleus. Conversely, females did not show any obvious variation in these brain regions. The medial preoptic nucleus controls male reproductive behaviour while the ventromedial hypothalamic nucleus controls female reproductive behaviour and is also involved in male aggression. Therefore, the primary brain nuclei underlying reproductive behavior evolve in a mosaic fashion in dragons, differently between males and females, likely in response to the strength of sexual selection.

Collectively, these findings describe in detail the structure of an agamid brain and some of the ways in which that structure has changed through evolution. In doing so, these results have highlighted both how labile the brain can be in response to evolution, and how conserved brain structure is in general. Lizards, and reptiles in general, are the most understudied vertebrate group in neuroscience, but there is huge potential for discovery in this field.