UNIVERSITY of CALIFORNIA, IRVINE Insights Into Butterfly
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UNIVERSITY OF CALIFORNIA, IRVINE Insights into butterfly ecology and evolution DISSERTATION submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in Biological Sciences by Nélida Beatriz Mercedes Pohl Pohl Dissertation Committee: Associate Professor Adriana D. Briscoe, Chair Professor Diane R. Campbell, co-Chair Professor Timothy J. Bradley 2009 1 © 2009 Nélida Beatriz Mercedes Pohl Pohl 2 The dissertation of Nélida Beatriz Mercedes Pohl Pohl is approved and is acceptable in quality and form for publication on microfilm and in digital formats: ___________________________ ___________________________ Committee Chair ___________________________ Committee co-Chair University of California, Irvine 2009 3 TABLE OF CONTENTS Page LIST OF FIGURES iv LIST OF TABLES v ACKNOWLEDGMENTS vi CURRICULUM VITAE vii ABSTRACT OF THE DISSERTATION ix INTRODUCTION 1 CHAPTER 1: Impact of duplicate gene copies on phylogenetic analysis and divergence time estimates in butterflies 6 Abstract 7 Introduction 9 Materials and Methods 13 Results and Discussion 20 Conclusions 34 CHAPTER 2: Butterflies show flower preferences but not constancy 36 Abstract 37 Introduction 39 Materials and Methods 43 Results 52 Discussion 58 TABLES AND FIGURES 64 REFERENCES 118 4 LIST OF FIGURES Page Figure 1.1 Alignments of UVRh, BRh, LWRh, EF-1α, and COI 64 Figure 1.2 Maximum Parsimony tree 86 Figure 1.3 Maximum Likelihood trees 88 Figure 1.4 Bayesian trees 90 Figure 1.5 Maximum parsimony, maximum likelihood and Bayesian faster trees 92 Figure 1.6 Bayesian estimates of rate multiplier parameter (m) by gene partition 93 Figure 1.7 Bayesian divergence time estimates with slower evolving genes 94 Figure 1.8 Bayesian divergence time estimates with faster evolving genes 95 Figure 2.1 Flower reflectance spectra 110 Figure 2.2 Spontaneous flower preferences 112 Figure 2.3 Spontaneous color preferences 113 Figure 2.4 Spontaneous morphology preferences 114 Figure 2.5 Spontaneous display size preferences 115 Figure 2.6 Seed production 116 5 LIST OF TABLES Page Table 1.1 List of primers 96 Table 1.2 Taxa and genes 98 Table 1.3 Tajima relative rates tests 100 Table 1.4 Partitioned Bremer support values 101 Table 1.5 Penalized likelihood age estimates 102 Table 1.6 Bayesian age estimates 103 Table 1.7 Bayesian age estimates using slower evolving gene copies 104 Table 1.8 Bayesian age estimates using faster evolving gene copies 107 Table 2.1 Tests of butterfly flower constancy behavior 117 6 ACKNOWLEDGEMENTS I would like to thank my committee; Adriana Briscoe, Diane Campbell and Tim Bradley for the support and criticism provided over the years. I’m also grateful to Art Weis for his help during the earlier stages of this dissertation. Stimulating discussions with Francesca Frentiu, Nick Waser and Mary Price generated ideas that improved this work. I thank Jennifer Van Wyk and Zac Davies for their participation in field work, and Marilou Sison-Mangus, Emily Yee and Saif Liswi for their contribution to the laboratory work. Jeffrey Thorne provided helpful assistance with data analyses. Support and funding came from Fulbright-CONICYT, UCI Edward A. Steinhaus Annual Memorial Award, Sigma Xi GIAR, the Lee R. G. Snyder Memorial Fund at RMBL, Southern California Phi Beta Kappa International Student Scholarship, UCI Miguel Velez Fellowship Award, site NSF REU grant DBI 0242960 to RMBL, NSF DEB-9806547, IOS-0646060 and IOS-0819936, and grants from the UCI Undergraduate Research Program. I am also indebted to my family and friends in Chile, and to the new friends I have made in these past five years, for the unconditional love that made me who I am today. 7 CURRICULUM VITAE Nélida Pohl EDUCATION 2009 PhD. Biological Sciences, Department of Ecology and Evolutionary Biology, University of California, Irvine, USA. 2003 MSc. Ecology and Evolutionary Biology, Universidad de Chile 2001 Photography Diploma, Universidad Católica de Chile 2000 BSc. Biological Sciences, Universidad de Chile GRANTS AND FELLOWSHIPS 2007-2008 UCI Miguel Velez Fellowship Award 2007-2008 Southern California Phi Beta Kappa International Student Scholarship 2007 Rocky Mountain Biological Laboratory Snyder grant 2006 Sigma Xi Grants in Aid of Research 2005-2006 UCI Edward A. Steinhaus Annual Memorial Award 2005 Rocky Mountain Biological Laboratory Snyder grant 2003-2007 Government of Chile (CONICYT) fellowship. 2003-2007 Fulbright fellowship. 2002-2003 Graduate Fellowship from the Millenium Center for Advanced studies in Ecology and Biodiversity, Chile. 2002-2003 University of Chile Graduate Thesis Support Grant. PROFESSIONAL APPOINTMENTS 2003-2008 Teaching assistant, Department of Ecology and Evolutionary Biology, University of California, Irvine. 2000-2002 Teaching assistant, Facultad de Ciencias, Universidad de Chile. 2000-2001 Research assistant, Laboratorio de Neurobiología y Biología del Conocer, Departamento de Biología, Universidad de Chile. PRESENTATIONS AT SCIENTIFIC MEETINGS 2008 Conference on the Ecology and Evolution of Plant-Pollinator Interactions, Milwaukee, Wisconsin. 2007 Invited speaker 9th International Pollination Symposium, Ames, Iowa. 2006 7th International Workshop on Molecular Biology and Genetics of the Lepidoptera, Crete, Greece 2006 IX Congreso Latinoamericano de Botánica, Santo Domingo, Republica Dominicana. 2005 NAS Sackler Colloquium on Tapestry of Life, Irvine, CA. 2005 Evolution Conference, Fairbanks, Alaska USA 8 2004 15th Science Conference of Sigma Chapter - Graduate Women in Science. California State University, Fullerton, CA. 2004 Southern California Animal Behavior conference, University of California, Los Angeles, CA. 2003 CalPEG (California Population and Evolutionary Genetics Meeting) University of California, Irvine, CA. 2002 Congreso anual de la Sociedad de Biología de Chile, Puyehue, Chile 2002 VIII Congreso Latinoamericano de Botánica, Cartagena de Indias, Colombia. 2001 Society of Neuroscience Meeting, San Diego, CA. 2001 Congreso anual de la Sociedad de Biología de Chile, Pucón, Chile. PUBLICATIONS Pohl, N, J. Van Wyk, and D.R. Campbell. Butterflies show flower preferences but not constancy. In preparation for Oecologia. Pohl, N, M.P. Sison-Mangus, E.N. Yee, S.W. Liswi and A.D. Briscoe. Impact of duplicate gene copies on phylogenetic analysis and divergence time estimates in butterflies. Submitted to BMC Evolutionary Biology. Medel, R., A. Valiente, C. Botto-Mahan, G. Carvallo, F. Perez, and N. Pohl. & Navarro, L. 2007. The influence of insects and hummingbirds on the geographical variation of the flower phenotype in Mimulus luteus. Ecography 30: 812-818. Pohl, N, G. Carvallo, C. Botto-Mahan, and R. Medel. 2006. Non-additive effects of flower damage and hummingbird pollination on the fecundity of Mimulus luteus. Oecologia 149: 648-655. Botto-Mahan, C., N. Pohl, and R. Medel. 2004. Nectar guide fluctuating asymmetry does not relate to female fitness in Mimulus luteus. Plant Ecology 174: 347 - 352. Herrera, G., M.J. Fernandez, N. Pohl, M. Diaz, F. Bozinovic, and A. Palacios. 2004. Sistema visual en el colibri austral (Sephanoides sephaniodes) y el picaflor cordillerano (Oreotrochilus leucopleurus): electrorretinografia y coloracion. Ornitologia Neotropical 15 (Suppl.): 215-222. Marín, G., J.C. Letelier, P. Henny, E. Sentis, G. Farfán, F. Fredes, N. Pohl, H. Karten, and J. Mpodozis. 2003. Spatial organization of the pigeon tectorotundal pathway: an interdigitating topographic arrangement. The Journal of Comparative Neurology 458: 361-380. 9 ABSTRACT OF THE DISSERTATION Insights into butterfly ecology and evolution By Nélida Beatriz Mercedes Pohl Pohl Doctor of Philosophy in Biological Sciences University of California, Irvine, 2009 Associate Professor Adriana D. Briscoe, Chair Professor Diane R. Campbell, co-Chair This dissertation examined features of the butterfly visual system. The first part used opsin genes, which code for the visual pigment proteins, in reconstruction of butterfly phylogenies. The second part examined butterfly behavioral responses to flower color visual cues. The first goal was to examine the effect of incorporating duplicate opsin gene copies on tree reconstruction and divergence time estimation. Sequences from 5 genes, including 3 opsins, were obtained from 27 taxa. Regardless of the phylogenetic reconstruction method, combined data sets analyses using either slower or faster evolving copies of duplicate genes, as well as individual analyses of blue and long-wavelength opsin genes, which are present in multiple copies in some lineages, resulted in a single topology in agreement with our current understanding of family relationships. Two methods resulted in similar divergence time estimates regardless of whether faster or slower evolving copies were used. Family-level results were congruent with other recent estimates, indicating an age of at least 150 MY for the first familial divergence. These results are consistent with overlapping timeframes for the diversification of butterfly 10 families and angiosperms and suggest the use of duplicate gene copies for phylogenetic reconstruction and divergence time estimation. The second goal was to explore the role of color in flower visiting behavior. This study represented the first field-based attempt with butterflies to phenotypically manipulate flower color and decouple its effect from that of other traits. In order to assess if butterflies possess spontaneous color preferences and if they behave as constant flower visitors, all visits to artificial arrays of Asteraceae flowers