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Systematics and Biogeography of Leafhoppers in Madagascar

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SYSTEMATICS AND BIOGEOGRAPHY OF LEAFHOPPERS IN MADAGASCAR BY SINDHU MANUBHAI KRISHNANKUTTY DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Entomology in the Graduate College of the University of Illinois at Urbana-Champaign, 2012 Urbana, Illinois Doctoral Committee: Dr. Christopher H. Dietrich, Illinois Natural History Survey, Chair, Director of Research Professor May Berenbaum Professor James Whitfield Dr. Steve Taylor, Illinois Natural History Survey ABSTRACT The biodiversity of Madagascar is well appreciated due to its high level of species richness and endemism. With more natural habitat being destroyed due to colonization and fulfilling essential needs of humans, presently it is considered as one of the priority hotspots for biodiversity conservation. Despite being the most diverse invertebrates in Madagascar, several insect families remain poorly known. Cicadellidae, one of the largest insect families distributed worldwide is one among them. Prior knowledge of leafhopper fauna of Madagascar is based on only five previously published taxonomic studies and very limited sampling. No attempt using phylogenetic methods has been made to understand relationships among the leafhopper genera and to test the monophyly of previously recognized endemic Malagasy taxa. Owing to their Mesozoic origin, moderate dispersal abilities, and spectacular radiation in both New and Old World tropics, leafhoppers are excellent models for biogeographic and evolutionary studies related to the origins of the Malagasy fauna. A recent terrestrial arthropod inventory project in Madagascar conducted by the California Academy of Sciences yielded >60,000 ethanol-preserved leafhopper specimens, including representatives of most previously recorded species as well as many new species. This new material provided an opportunity to examine the phylogeny and biogeography of Malagasy leafhoppers in much greater detail than ever before possible. Specimens of three leafhopper subfamilies, Iassinae, Idiocerinae, and Cicadellinae were selected for study based on their independent evolutionary origins, according to a recently published family-level phylogeny, and their high diversity in samples used in the study. The main objective of this study was to understand the historical biogeography of leafhoppers in Madagascar based on phylogeny. Phylogenetic relationships of the Malagasy fauna of the three selected leafhopper subfamilies to those of other continents were estimated using phylogenetic analyses of DNA sequence data. The phylogenies of these lineages were then used to estimate divergence times in order to test different biogeographic hypotheses and determine the most likely scenario(s) for the origin of the Malagasy leafhopper fauna. The species of two widely distributed leafhopper groups in Madagascar, the endemic idiocerine genus, Nesocerus and the subfamily Mileewinae, were also revised taxonomically and keys, descriptions and illustrations are provided. ii Based on the phylogenetic informativeness within each lineage, different domains of 28S ribosomal RNA (D2, D6, D8, D9, D10), Histone (H3), 12SrRNA (12S) and Cytochrome Oxidase II were sequenced. Phylogenetic analyses based on Parsimony, Maximum Likelihood and Bayesian approaches recovered congruent topologies for each dataset. In Iassinae, analysis of a combined dataset of 28S, histone H3 and 12S nucleotide sequences, Malagasy endemic tribe Platyjassini was recovered as monophyletic and consistently placed as one of the deeper nodes within the subfamily. This suggests that this tribe belongs to an ancient lineage that became isolated and diversified within Madagascar. In Idiocerinae, analysis based on 28S, histone H3 dataset indicated that the Malagasy idiocerine fauna is polyphyletic, with different groups derived from either Asian or African genera, except one endemic genus, Nesocerus, recovered as sister to the rest of the subfamily. Phylogenetic analyses of Cicadellinae based on the D8 region of 28S, COII and Histone recovered the Malagasy fauna in two main clades, one including the genus Madicola and the other including the remaining genera. These to clades were arranged in a paraphyletic grade between the more basal (non-Malagasy) Old World Cicadellinae and the more derived New World fauna. Bayesian divergence time analyses suggest that a combination of Cretaceous vicariance and Cenozoic dispersal shaped the biogeographic history of leafhoppers in Madagascar. The closest non-Malagasy relatives of the Madagascar endemic taxa Platyjassini (Iassinae) and Nesocerus (Idiocerinae) remain unclear. However based on the divergence time estimates, the timing of origin of these groups occurred during Cretaceous when Madagascar was joined with the Seychelles-Indian block and after becoming isolated, these groups underwent extensive diversification within Madagascar. In Idiocerinae, multiple dispersals from Asia and Africa were revealed to have given rise to the remaining Malagasy genera. The split of the Malagasy cicadelline fauna from other Old World Cicadellinae coincided with the period of existence of the Indo-Madagascar block, which may account for the early divergence of this group. The crown age of one of the clades of Malagasy Cicadellinae that includes genera distributed in eastern rainforests is estimated to be around early Eocene (~59 mya). This suggests that the group radiated within Madagascar soon after the emergence of eastern rainforests. An ‘Out of Madagascar’ dispersal to the New World through North Atlantic connections was also hypothesized as the most plausible scenario based on the timing of the split between the Malagasy lineage and the New World fauna. iii Taxonomic revision of the endemic idiocerine genus Nesocerus revealed 29 new species. Morphological phylogenetic analysis of this genus supported the monophyly of this group and recovered two sister clades. Species belonging to one of the clades are widely distributed in eastern humid forests whereas the members of the other clade are mostly restricted to western dry forests. Revision of the subfamily Mileewinae revealed seven new species of Ujna from Madagascar. Species of this genus are placed into three species groups based on morphological characters. Utility of female genitalia characters in taxonomy of this subfamily is reported for the first time. iv ACKNOWLEDGMENTS I would like to express my sincere gratitude to my advisor, Dr. Chris Dietrich for his constant encouragement and support throughout my dissertation. His unending patience and guidance made this journey fruitful and equally exciting. His pleasant personality and insightful prompt feedback has always been stress relief to me. I feel fortunate to have an advisor who gave me the freedom to explore my own and at the same time guidance that helped me to be on right track with more confidence. I would like to thank my committee members, Drs. May Berenbaum, James Whitfield and Steve Taylor for providing advice and critiques that was helpful in improving the quality of my writing. I am grateful to Dr. James Whitfield for providing me an opportunity to work as Teaching Assistant in his course. His immense support, encouragement and sense of humor made that teaching experience memorable. I take this opportunity to thank Dr. May Berenbaum for financially supporting me through teaching assistantships in many semesters. I am truly grateful to Dr. Steve Taylor who has always been kind to provide guidance in my professional development. I am one of the few graduate students who are lucky to have awesome lab members. I specially thank Jamie for his assistance and support over the years. He has been always kind to share his expertise in phylogenetic analyses. Many thanks to Dima for improving my knowledge in using his database and for hilarious jokes during his tea break. Thanks Brendan and Therese for a friendly exciting lab atmosphere! I would like to thank Dani Takiya for helping with identification of Cicadellinae specimens. I would like to thank the entomology department staff, Audra Weinstein and Karen Trame for their tremendous help in dealing with official documents throughout my graduate life. My sincere thanks to Drs. Norman Penny, Brian Fisher (California Academy of Sciences); Adeline Soulier-Perkins (Muséum national d’Histoire naturelle, Paris); Mick Webb (British Natural History Museum); Prathapan Divakaran (Kerala Agricultural University); Shepherd Myers (Bishop Museum) and Jason Cryan (North Carolina Museum of Natural Sciences) for lending leafhopper samples without which this study would have been impossible. I would like to thank my mentor Dr. C. A. Viraktamath (University of Agricultural sciences, Bangalore) for his constant encouragement throughout my career. v I am grateful to Drs. Dai Wu (Northwest A& F University, China) and Jacek Szwedo (Polish Academy of Sciences) for assistance with research papers. I would like to thank Dr. Ken Paige in the department of Animal Biology for letting me use his lab facilities. My thanks to Drs. Julie Urban (North Carolina Museum of Natural Sciences) and Kevin for the sweet memories of Mulu collection trip, which I cherish forever. I am grateful to the department of Entomology, Integrative Biology and department of Molecular and Cellular Biology at University of Illinois for financial assistance through Teaching Assistantships and many small grants during my Ph. D studies. Additional support provided through funding by National Science Foundation PEET grant DEB-0529679
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