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Evolution and Ecology of Termite Nesting Behavior and Its Impact On 1 Evolution and Ecology of Termite Nesting Behavior and Its Impact on Disease Susceptibility A dissertation presented by Marielle Aimée Postava-Davignon to The Department of Biology In partial fulfillment of the requirements for the degree of Doctor of Philosophy in the field of Biology Northeastern University Boston, Massachusetts April, 2010 2 Evolution and Ecology of Termite Nesting Behavior and Its Impact on Disease Susceptibility by Marielle Aimée Postava-Davignon ABSTRACT OF DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology in the Graduate School of Arts and Sciences of Northeastern University, April, 2010 3 Abstract Termites construct nests that are often structurally species-specific. They exhibit a high diversity of nest structures, but their nest evolution is largely unknown. Current hypotheses for the factors that influenced nest evolution include adaptations that improved nest thermoregulation, defense against predators, and competition for limited nest sites. Studies have shown a lower prevalence of pathogens and parasites in arboreal nesting animal species compared to ground nesters. Nest building behavior is plastic and can adapt to changing environments. As termites can detect and avoid pathogens, I hypothesized that the evolution of arboreal termite nests was an adaptation to avoid infection. To test this, bacteria and fungi from nest cores, trails, and surrounding soils of the arboreal nesting Nasutitermes acajutlae were cultured. Abiotic factors such as temperature, relative humidity, and light were measured to elucidate how they influenced the interactions between termites and microbes. Fungi associated with N. acajutlae were identified to determine the potential pathogenic pressures these termites encounter in their nest as compared to the external environment. To determine the effect of nest structure on survival, termites representing the one-piece (Zootermopsis angusticollis), intermediate (Reticulitermes flavipes) and separate (Nasutitermes corniger) type nests were exposed to the fungal entomopathogen Metarhizium anisopliae, and the termites’ survival tracked over a 20-day period in five different artificial nest architectures. A protected nest environment and the benefits of socially mediated immunity within those nests have also been implicated in promoting termite eusocial evolution. In order to test whether immune protein production is socially induced in termites, the SDS-PAGE 4 protein profiles of naïve Z. angusticollis nymphs, and nestmates directly exposed to M. anisopliae were examined following social contact. The results presented in this dissertation demonstrate that arboreal termites have lower nest microbial loads and diversity compared to surrounding soils, and that the degree of social contact as influenced by nest architecture can significantly affect termite survival. This research suggests that pathogens played a role in furthering evolution and ecology of termite nesting behavior, and lays the groundwork for future studies in this area. 5 This dissertation is dedicated to my family. To my parents, who have loved and supported me through all my endeavors. To my sisters, who have given me invaluable guidance, strength, and love. To my brothers-in-law, who watch over and care for me like a true sister. To my niece, whose laughter and bright smile helped get me through tough times. I love you all, and could not have done this without you. 6 Acknowledgements I would like to express my gratitude to the many people without whom this research would not have been possible. My advisor, Rebeca Rosengaus, who introduced me to and led me through the wonderful world of termites, a place to which I otherwise would never have known I truly belonged. My collaborator Claire Fuller for six years of exciting field research, and friendship. My committee members Wendy Smith, Jacqueline Piret and Gwilym Jones for their advice and support. Mark Bulmer for his expertise, and camaraderie. John Stiller and Erica Waddle for their work on fungal identifications. My fellow graduate students Tamara Hartke, Kelley Schultheis, and Lindsey Reichheld for their input and shoulders to lean on. Comfort Chieh and Danny Dijohnson for culturing countless bacterial and fungal samples. Kayla Hamilton and Charlie Ferranti for their work on the Nasutitermes portion of the nest architecture project. Earthwatch SCAP girls 2005-2008 for their hard work in the field on St. John. All other Rosengaus lab members, and graduate students past and present: you are a rare and genuinely fine group of people, and it has been a pleasure working with you. Thank you to Huddart and Redwood Regional Parks, and the Smithsonian Tropical Research Institute for termite collections. Kim Seefeld and the R Development Core Team for assistance with statistics. The Northeastern Biology Department and NSF GK-12 program for financial support. This research was funded by an NSF-CAREER grant (DEB 0447316) awarded to Rebeca Rosengaus, an NSF grant (IBN-0116857) awarded to James Traniello and Rebeca Rosengaus, and by the Durfee Foundation through the Earthwatch Student Challenge Awards Program. 7 Contents Abstract 2 Acknowledgements 6 Contents 7 List of Figures 9 List of Tables 11 1 Introduction 12 1.1 Ancestry and eusocial evolution 13 1.2 Termites in the fossil record 15 1.3 Nest types, classifications, and associated levels of sociality 16 1.4 Nest building behavior 19 1.5 Nest evolution 20 1.6 Selective pressures acting on nest evolution 22 1.7 Pathogenic pressures and the evolution of eusociality 26 1.8 Central aims 28 2 Dynamic interactions between the arboreal Caribbean termite Nasutitermes acajutlae (Holmgren), its associated microbial communities, and the environment 33 2.1 Introduction 34 2.2 Methods 37 2.3 Results 42 8 2.4 Discussion 60 3 Fungi naturally associated with the arboreal nesting Caribbean termite Nasutitermes acajutlae (Holmgren) 66 3.1 Introduction 67 3.2 Methods 69 3.3 Results 72 3.4 Discussion 73 4 The effect of nest architecture on termite susceptibility to a fungal pathogen 87 4.1 Introduction 88 4.2 Methods 95 4.3 Results 103 4.4 Discussion 111 5 Social induction of hemolymph proteins in the dampwood termite Zootermopsis angusticollis (Holmgren) 119 5.1 Introduction 120 5.2 Methods 123 5.3 Results 130 5.4 Discussion 139 6 Overall discussion and conclusions 144 Literature Cited 150 9 List of Figures 1.1 Figure modified from Eggleton and Tayasu (2001) depicting the eight lifeways of termites 30 2.1 Nasutitermes acajutlae arboreal carton nest 43 2.2 Collecting Nasutitermes acajutlae in the field 43 2.3 LogTag data loggers 44 2.4 Examples of fungi cultured from Hurricane Hole trail material on thiostrepton PDA 49 2.5 Mean log transformed cuticular bacterial CFUs/SA ± SE 50 2.6 Mean log transformed substrate bacterial CFUs/g ± SE 51 2.7 Mean log transformed cuticular fungal CFUs/SA ± SE 52 2.8 Mean log transformed substrate fungal CFUs/g ± SE 53 2.9 Correlations between microbial numbers and temperature 54 2.10 Mean nest (core), ambient (trail) and soil temperatures ± SE 55 2.11 Example traces from LogTag data loggers 56 2.12 Correlation between numbers of fungi and amount of light 57 2.13 Mean nest (core), ambient (trail) and soil % moisture ± SE 58 3.1 Examples of fungal genera associated with Nasutitermes acajutlae 78 3.2 Fungal genera and number of occurrences in core, trail, and surrounding soil samples of Nasutitermes acajutlae individuals and nests 80 3.3 Relative similarities of fungi among Nasutitermes acajutlae nests located in different habitats 81 10 3.4 Nodules in a fallen nest of Nasutitermes acajutlae 86 4.1 Natural nests of termites 94 4.2 Example artificial nest architectures 101 4.3 Survival distributions resulting from Cox regressions as a function of treatment (a), species (b), and nest architecture (c) 106 4.4 Survival distributions as a function of nest architecture 108 4.5 Summary of survival across the five nest architectures for Zootermopsis angusticollis (Za), Reticulitermes flavipes (Rf) and Nasutitermes corniger (Nc) 109 4.6 Median nest temperature (a) and % RH (b) across nest architectures 110 5.1 Diagram depicting the timing of hemolymph extractions one and two, and the combinations of treatment groups 131 5.2 Example hemolymph protein profiles from a NCE individual 134 5.3 Median masses of new proteins across direct exposure treatments 135 5.4 Median numbers of new proteins per individual across direct exposure treatments 136 5.5 Median masses of new proteins across naïve treatments 137 5.6 Median numbers of new proteins per individual across naïve treatments 138 11 List of Tables 1.1 A comparison of traits used as indicators of social complexity in termites and their subsocial ancestors 31 1.2 Selective forces implicated in the evolution of social insect nests 32 2.1 Final regression model outputs for bacterial (A) and fungal (B) CFUs 48 2.2 Climatological data for the U.S. Virgin Islands 59 3.1 Identifications of fungi associated with Nasutitermes acajutlae 74 3.2 Jaccard coefficients comparing the similarity of core, trail, and soil fungal genera 77 3.3 Taxonomic groups of fungi associated with Nasutitermes acajutlae 79 4.1 Survival parameters for control and conidia exposed termites of the three study species 107 12 Chapter 1 – Introduction Termites are eusocial roaches (Inward et al., 2007a) and are unique in that they are the only roaches to have evolved eusociality. Termites are of particular interest in studies of eusociality because 1) they are the only insects to have developed eusociality outside the order Hymenoptera, and 2) unlike Hymenopterans, which have haplo-diploid sex determination, termites are diplo-diploid and thus lack the genetic predispositions for the evolution of sterile castes (Thorne, 1997). Investigating the evolutionary history of termites and eusocial development is difficult due to the lack of extant solitary species within the order Isoptera. Instead, factors promoting eusociality must be inferred through studies of the fossil record, the presocial roach ancestors of termites, and different aspects of the biology of extant species, including the degree of complexity of their nests.
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