Copyright by Krushnamegh Jagannath Kunte 2008 The Dissertation Committee for Krushnamegh Jagannath Kunte certifies that this is the approved version of the following dissertation: Evolution of sex-limited mimicry in swallowtail butterflies Committee: _____________________________ Lawrence E. Gilbert, Supervisor _____________________________ Thomas Juenger, Co-supervisor _____________________________ Michael Singer ____________________________ Mark Kirkpatrick _____________________________ Alan Lloyd _____________________________ Peter Andolfatto Evolution of sex-limited mimicry in swallowtail butterflies by Krushnamegh Jagannath Kunte, M.Sc. Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin December, 2008 Dedication To Alfred Russel Wallace – naturalist extraordinaire – on the 150th anniversary of his discovery of natural selection, in admiration of his work on Indo-Malayan swallowtail butterflies. Acknowledgements More than ever before in my life, this work is a product of years of collaboration with numerous scientists, butterfly collectors and friends. First and foremost, I thank my advisor Lawrence Gilbert who patiently tolerated my academic wanderings for many years, let me find my feet in the academic world, and provided critical guidance, support and inspiration when I needed it most. Thomas Juenger provided lab facilities, some research funding and a lot of advice about lab work. I give special thanks to Michael Singer for varied academic as well as interesting non- academic discussions. My other committee members: Alan Lloyd, Peter Andolfatto and especially Mark Kirkpatrick, have over the years offered constructive criticism of my ideas and also advice on the way forward. Much wisdom about swallowtail butterflies, mimicry and the molecular methods to study them has trickled down to me from Felix Sperling, Rob Plowes, Harry Pavulaan, David Wright and Tierney Wayne. Thomas Emmel, Jacqueline Miller (both at the McGuire Center for Lepidoptera and Biodiversity, University of Florida at Gainesville) and Naomi Pierce (Museum of Comparative Zoology, Harvard University) kindly granted permission to study and photograph museum specimens, without which this thesis would not be complete. None of the work presented here would have been possible without substantial research funding from the Section of Integrative Biology and two consecutive Continuing Fellowships from the University of Texas. Lastly, my wife Deepa Agashe made learning and scientific discovery in these six long years much more fun with her biological insight, personal understanding and love. Thank you all. v Evolution of sex-limited mimicry in swallowtail butterflies Publication No. ________________ Krushnamegh Jagannath Kunte, PhD. The University of Texas at Austin, 2008 Supervisor: Lawrence E. Gilbert Co-supervisor: Thomas Juenger Many organisms are sexually dimorphic for ecologically and socially important traits. One of the major foci of biology is to understand the evolution of such sexually dimorphic traits. Here I present my work on the evolution of a dimorphic trait, female-limited Batesian mimicry, in Papilio swallowtail butterflies. I begin by developing a character state path network to study the diversity of mimicry types and directionality of trait change during the evolution of female- limited mimicry. My phylogenetic analysis showed that female-limited mimicry has evolved independently in several groups of swallowtails, mainly via single-step character changes from monomorphic non-mimetic ancestors to female-limited mimetic descendents. Mimetic polymorphism has evolved in tandem with female-limited mimicry, the two being tightly correlated among mimetic species. Most traditional explanations of female-limited mimicry and mimetic polymorphism invoke sexual selection. In reviewing these hypotheses, I show that their key assumptions and predictions remain untested, and that sexual selection cannot maintain female polymorphism under some conditions. Sexual selection hypotheses are also unable to explain community ecological aspects of mimicry rings. Hence, I developed a novel model of female-limited vi mimicry based on sex-specific, frequency- and density-dependent advantages of mimicry. This model shows that both-sex mimicry, female-limited mimicry and mimetic polymorphism are favored along a gradient of relative mimic frequency. My ecological data from south Indian mimicry rings support a key prediction of this model. Finally, I employ the patterns of female-limited mimicry among swallowtail butterflies to highlight the contrast between Darwin’s sexual selection model and Wallace’s natural selection model of sexual dimorphism. I show that most of the sexual dimorphism in swallowtail wing color patterns is a product of natural selection for protective female coloration, predominantly in the form of female-limited mimicry. Thus, swallowtails support Wallace’s model of sexual dimorphism, underlining the importance of natural selection. vii Table of Contents List of Figures and Plates …………………………………………………………. x List of Tables ……………………………………………………………………… xi Chapter 1. The diversity and evolution of Batesian mimicry in Papilio swallowtail butterflies Abstract …………………………………………………………………… 1 Introduction ………………………………………………………………. 1 Materials and Methods …………………………………………………… 4 Results …………………………………………………………………….. 8 Discussion ……………………………………………………………….... 10 Chapter 2. Female-limited mimetic polymorphism: A review of theories and a critique of sexual selection as balancing selection Abstract ……………………………………………………………………. 17 Introduction ………….…………………………………………………….. 17 Review of Theories …...……………………………………………………. 19 Chapter 3. A model of female-limited mimicry Abstract …………………………………………………………………….. 31 Introduction ……………………………………………………………….... 31 A model of Batesian mimicry ……………………………………………... 35 Community ecology of mimicry rings and female-limited mimicry ……… 40 Materials and Methods ……………………………………………………... 40 Results …………………………………………………………………….... 43 Discussion ………………………………………………………………….. 45 Chapter 4. Female-limited mimicry and the models of sexual dimorphism Abstract …………………………………………………………………….. 49 Introduction ………………………………………………………………… 49 Materials and Methods ……………………………………………………... 52 Results ……………………………………………………………………… 53 Discussion ………………………………………………………………….. 53 Chapter 5. Experimental investigations of competition and community dynamics in tropical butterfly communities Abstract ……………………………………………………………………. 57 Introduction ………………………………………………………………... 57 Materials and Methods …………………………………………………….. 59 Results ……………………………………………………………………... 63 Discussion …………………………………………………………………. 66 viii Chapter 6. Allometry of proboscis length and its functional significance in butterflies Abstract ……………………………………………………………………. 71 Introduction ………………………………………………………………... 71 Materials and Methods …………………………………………………….. 74 Results ……………………………………………………………………... 75 Discussion …………………………………………………………………. 76 Figures, Tables and Plates ………………………………………………………….. 79 References ………………………………………………………………………….. 112 Vita …………………………………………………………………………………. 132 ix List of Figures and Plates Fig. 1.1 A theoretical character state path network ………………………………… 79 Fig. 1.2 Distribution of mimicry types among Papilio butterflies ..……………….. 80 Fig. 1.3 Frequency of character state changes .…………………………………….. 81 Fig. 3.1 A model of mimicry ………………………………………………………... 82 Fig. 3.2 Mimicry rings in the Western Ghats ………………………………………... 83 Fig. 3.3 Relative frequencies of models and mimics in the mimicry rings …………. 85 Fig. 3.4 Density of models and relative frequency of mimics across mimicry rings in the Western Ghats …………………………………………………. 86 Fig. 3.5 Phenology of naïve birds in the Western Ghats …………………………….. 87 Fig. 4.1 Models of sexual dimorphism and female-limited mimicry …………….…. 88 Fig. 4.2 Correlation of sexual dimorphism with female-limited mimicry, deviation in female wing color patterns, and female polymorphism …...… 89 Fig. 4.3 Exemplary patterns of female-limited mimicry and polymorphism ………. 90 Fig. 5.1 Species rank/abundance plots for Anartia pre-removal and post-removal treatments ……………………………………….. 91 Fig. 5.2 Community composition in the pre- and post-removal treatments ………... 92 Fig. 6.1 The allometric relationship between body length and proboscis length in butterflies ………………………………………………………… 93 Fig. 6.2 Box-plots of relative proboscis lengths of nectar-feeding and non-nectar-feeding species ………………………………………………... 94 Fig. 6.3 The relationship between relative proboscis length and mean handling time for butterflies ………………………………………………. 95 Plate 1 A representative sample of wing color patterns, female-limited mimicry and female polymorphism in Papilio butterflies ………............... 96 x List of Tables Table 3.1 Abundance of individual models and mimics in the Western Ghats mimicry rings. …………………………………………………….. 98 Table 3.2 Insectivorous birds of the Anamalais and their breeding seasons ……... 100 Table 3.3 Mimics and models in the Eastern Himalayan mimicry rings ………….. 101 Table 5.1 Butterfly species on Lantana and Wedelia with their abundance ………. 102 Table 5.2 Differences in the abundance and diversity of butterfly assemblages in relation to competition ………………………………………………… 104 Table 5.3 Differences in foraging behavior of butterflies on the two nectar plants in pre- and post-removal treatments ……………………………… 105 Table 6.1 Morphometric measurements