An Investigation Into the Ecology and Evolution of Caterpillar Eyespots
Total Page：16
File Type：pdf, Size：1020Kb
An investigation into the ecology and evolution of caterpillar eyespots by Thomas John Hossie A thesis submitted to the Faculty of Graduate and Postdoctoral Affairs in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology Carleton University Ottawa, Ontario © 2014, Thomas John Hossie “Bad Portrait” painted by artist Mandy Stobo based on a photo of a Papilio canadensis caterpillar taken by Thomas Hossie 2 Abstract Eyespots are conspicuous circular patterns on the body of an animal which superficially resemble vertebrate eyes. These odd markings have long captured the interest of biologists and naturalists alike, many of whom have suggested that eyespots mimic the real eyes of dangerous animals and thereby protect prey species from their attackers. Eyespots are particularly widespread and diverse in lepidopteran caterpillars, and these caterpillars with eyespots are typically assumed to be snake-mimics. Yet a dearth of empirical investigation has left us without evidence that eyespots can protect caterpillars, or the ability to substantiate our subjective belief that these caterpillars are mimicking snakes. Using a combination of field and lab experiments my research provides robust empirical evidence demonstrating that eyespots are an adaptation in caterpillars, but reveals that other factors, including body colour and body size, influence their efficacy as a deterrent. Moreover, my work reveals that the defensive posture, which many caterpillars with eyespots adopt when harassed, also provides protection independent from the possession of eyespots. Using an objective measure of mimetic fidelity I showed that this defensive posture is likely a form of behavioural mimicry which increases the caterpillar’s resemblance to viperine snakes when viewed dorsally. Caterpillars from three distinct families showed analogous behavioural mimicry, suggesting strong selection for convergent phenotypes across lepidopteran larvae. Finally I provide an explanation for why some caterpillars have eyespots, and others do not. I show that body size critically influences the evolution of eyespots using a phylogenetically-controlled analysis of Macroglossinae (Sphingidae) caterpillar traits. Using field and lab experiments I reveal that the protective value of eyespots to caterpillars is in fact size-dependent: eyespots are only intimidating to attackers when on large-bodied prey that are already easy to detect, yet eyespots hinder small prey by making them easy to detect and failing to intimidate attackers. I argue that caterpillar eyespots have evolved to serve a mimetic function and were generated and are currently maintained by the innate fear of predator eyes harbored to varying degrees by numerous species of insect-eating birds. 3 Acknowledgements I would like to extend my sincere gratitude to my supervisor Tom Sherratt. He has been an excellent mentor throughout my degree. When I started my doctorate I did not know what the topic of my dissertation would be, but he allowed me the time I needed to develop the research program presented here. Tom gave me the freedom to dictate the direction of my research though all stages, but always provided the critical feedback required to make these projects successful. I am also grateful for his support of the several rewarding opportunities I have had throughout my degree including a month-long field trip to Costa Rica, and numerous conferences (Quebec City, Banff, Ottawa, Newcastle (UK), and Ventura). His feedback on the work included below resulted in substantial improvements and it has been a pleasure having him as a supervisor. My committee members Gabriel Blouin-Demers and Jayne Yack have been enthusiastic and supportive throughout my degree. Jayne in particular pushed me contact Dan Janzen and arrange a trip to Costa Rica which would end up being a highlight of my PhD experience. Dan Janzen and Winnie Hallwachs encouraged my travel to the Área Concervación Guanacaste in Costa Rica, and facilitated my visits to the various collecting stations during my stay. They allowed me to photograph and conduct behaviour tests on the numerous caterpillars at the collecting stations, which introduced me to a diversity of species I would not have otherwise experienced. Dan in particular has provided me with valuable insight into caterpillar eyespots that could not have been gleaned elsewhere. I thank my collaborators John Skelhorn, Akito Kawahara, Jesse Breinholt, Dan Janzen, and Winnie Hallwachs; each of their contributions to 4 this thesis were pieces that I was unable to add myself and have improved the calibre of this research. I would like to thank members of the Sherratt and Gorelick lab for their support and critical feedback, especially Chris Hassall and Richard Webster. Lee Gutowsky and I began our doctorates in Biology at the same time, and lived together for the first year and a half of our degree. I have greatly valued his friendship during my time in Ottawa. Similarly, I have appreciated the company of friends and colleagues Jake Brownscombe, Wayne Knee, Graham Raby, and Jason Thiem. Much of my fieldwork was conducted on land owned by Bill and Eleanor Hossie. They, along with my parents Mary Alice and James Hossie, unwaveringly encouraged my pursuits in biology and were always interested to hear about my research. I attribute much of my interest and appreciation for the natural world to my mother. Finally, I thank my partner Holly Kienzle. She gave up steady work as a teacher and proximity to her friends and family to come join me in Ottawa while I finished my degree. I know it has not always been easy for her, and I appreciate her continued love and support. 5 Co-authorship Statements Several pieces of this thesis document have been published including data chapters 2-5. Chapter 6 is soon to be submitted. Dr. Tom Sherratt was a coauthor on data chapters 2 and 3 which were published in Animal Behaviour (Hossie and Sherratt 2012, 2013), and chapter 4 which was published in Current Zoology (Hossie and Sherratt 2014). Specifically, Dr. Sherratt helped with the experimental design, analysis, and writing of this work. Chapter 5 was a natural history paper that was co-authored by Dr. Winnie Hallwachs, Dr. Daniel Janzen and Dr. Sherratt (Hossie et al 2013). Dr. Hallwachs and Dr. Janzen facilitated the observation that led to the description, provided great insight into the life history and behaviour of the taxa described, contributed photos, and assisted with writing. Dr. Sherratt gave the initial push to publish the description and contributed to the writing of the manuscript. Chapter 6 was co-authored by Dr. John Skelhorn, Dr. Akito Kawahara, Dr. Jesse Breinholt and Dr. Tom Sherratt. Dr. Skelhorn and I collaboratively designed the chick experiment portion of this work, and the actual chick experiment itself was conducted by Dr. Skelhorn. Dr. Kawahara and Dr. Breinholt built the phylogeny that was used in this chapter. Dr. Skelhorn, Dr. Kawahara, Dr. Breinholt, and Dr. Sherratt assisted with the writing of the manuscript. For all data chapters included in this thesis I conducted all of the analyses (excluding phylogeny estimation in Ch. 6), generated all the figures, and drafted all initial and final manuscripts. Chapters 2 and 3 are reprinted herein with the permission of Elsevier. Chapter 4 is reprinted with the permission of Current Zoology, and chapter 5 is reprinted in accordance with the policies of Taylor & Francis. 6 Table of Contents Abstract .......................................................................................................................................... 2 Acknowledgements ....................................................................................................................... 4 Co-authorship Statements ............................................................................................................ 6 Table of Contents .......................................................................................................................... 7 List of Tables ............................................................................................................................... 10 List of Illustrations ...................................................................................................................... 11 Preface .......................................................................................................................................... 16 1 Chapter: A general introduction to topics covered in the thesis ...................................... 19 1.1 A brief introduction to mimicry ................................................................................................. 19 1.2 A brief introduction to eyespots ................................................................................................ 22 1.3 Eyespots in lepidopteran caterpillars ......................................................................................... 25 1.4 Thesis Overview ........................................................................................................................ 38 2 Chapter: Eyespots interact with body colour to protect caterpillar-like prey from avian predators ...................................................................................................................................... 41 2.1 Abstract...................................................................................................................................... 42 2.2