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A Genomic Analysis of the Insect Pest Populations of Cowpea in West Africa

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A Genomic Analysis of the Insect Pest Populations of Cowpea in West Africa A GENOMIC ANALYSIS OF THE INSECT PEST POPULATIONS OF COWPEA IN WEST AFRICA BY TOLULOPE ADEBIMPE AGUNBIADE 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, 2014 Urbana, Illinois Doctoral Committee: Professor Barry R. Pittendrigh, Chair, Director of Research Associate Professor George Czapar Associate Professor Bettina Francis Assistant Professor Brian Allan ABSTRACT Cowpea [Vigna unguiculata (L.) Walp (Fabaceae)] is an important and major staple food crop in sub-Saharan Africa, especially in the dry savanna regions of West Africa. The crop provides food, cash, and fodder. As a food crop, cowpea is a primary source of protein for the ever-growing population of both rural and urban dwellers. The fodder and husks from cowpea also form an important source of protein, fiber, and energy for livestock. West Africa accounts for about 80% of the world’s cowpea production. However, insect pests are major constraints to cowpea production in the West African sub-region. The crop is severely attacked at every stage of its growth by different insect pests from the pre-flowering stage right through storage. Damage by insect pests on cowpea can be as high as 80 – 100% if not effectively controlled. Current control measures against the insect pests, which mostly consist of chemical control, are not without limitations. There is a need to develop a more comprehensive IPM strategy against cowpea insect pests by exploiting the knowledge of their biology, location of alternate host plants, and natural enemies, and combining these with the recent advances in genome sequencing technologies. This dissertation consists of five chapters and focuses on the integration of integrated pest management (IPM) and the current trends in genomic sequencing to cowpea IPM in West Africa with the aim of better understanding the insect pest populations of the cowpea crop and defining their population structure and movement patterns. Chapter 1 which serves as the introduction to the whole thesis discusses in detail the advent of the genomics era and how IPM researchers must take advantage of the ii recent development in genomic practices. It introduces the concept of IPM-omics and how this can be applied to cowpea cropping systems in West Africa. It also discusses the effective deployment of the research output to the end-users. Chapters 2 and 3 answer questions regarding the timing and spatial scale of the migration patterns of one of the major insect pests of cowpea in West Africa, the legume pod borer (Maruca vitrata). I applied a set of microsatellite markers (Chapters 2 and 3) and mitochondrial cox1 haplotype data (Chapter 3) to characterize the M. vitrata populations across locations in West Africa [Burkina Faso, Niger and Nigeria (Chapter 2)] and also on four host plants of M. vitrata [cultivated cowpea (Vigna unguiculata), and three alternative host plants - Pueraria phaseoloides, Loncocarpus sericeus, and Tephrosia candida)] in southern Benin (Chapter 3). The findings from the studies in the two chapters enabled a much clearer understanding of the genetic variability, population structure, and gene flow among M. vitrata populations in those countries and the host plants sampled. Chapter 4 compares the mitochondrial genome of M. vitrata from the New World (Puerto Rico) with the mitochondrial genome of the M. vitrata population from the Old World (Burkina Faso), and also with the mitogenomes of other Crambids. Species from the genus Maruca have a wide distribution from northern Australia and East Asia through sub-Saharan Africa to the Caribbean, Central America, and North America. The species are difficult to distinguish morphologically and have been surmised to be a species complex due to cryptic morphological differences. To be able to study evolutionary patterns among Maruca species, I sequenced and assembled the mitochondrial genome of the Maruca subspecies from Puerto Rico and compared this with the mitochondrial iii genomes of M. vitrata from West Africa, and also with other available Crambid mitochondrial genomes. The study enabled the estimation of mutation tendencies in M. vitrata and also the construction of phylogenetic relationships, as well as comparative and molecular genome evolution patterns in M. vitrata. Chapter 5 goes beyond my research on M. vitrata and concentrates on other destructive insect pests of cowpea in West Africa. In West Africa, besides M. vitrata, other serious insect pests also attack the cowpea crop. These insect pests include thrips (Megalurothrips sjostedti), aphids (Aphis craccivora) and pod sucking bug complex, (including Clavigralla tomentosicollis and Anoplocnemis curvipes). Collectively, these pests can wipe out a whole cowpea harvest. Part of the constraint in the application of effective control strategies against these pests is the lack of molecular markers that can enable the characterization of the pest populations. For this study, I applied Roche 454 sequencing technology to generate and subsequently assemble contigs from DNA sequencing reads for A. curvipes, A. craccivora, C. tomentosicollis and M. sjostedti. These were then used to detect polymorphisms in the different populations of these insect pests across West Africa. Findings from this study identified putative single nucleotide polymorphisms (SNPs), which can be used for characterizing the populations of the different insect pests, and also identified candidate genes putatively involved in insecticide resistance, regulation of insect growth, and response to disease transmission. Overall, the output from the studies in this dissertation will facilitate the effective evaluation, modification, and optimization of practical cowpea IPM strategies which will in the short- and long-term help in the monitoring of the insect pest populations as well as aid in making decisions as to how, when, and where to apply appropriate control measures. iv To the loving memory of my father, Oladeji Adeniran, To my mother, Omodunbi Adeniran, To my husband, Olusegun Agunbiade v ACKNOWLEDGMENTS I would like to express my gratitude to my advisor, Dr. Barry Pittendrigh, for his tremendous academic support and invaluable guidance, which helped in the completion of this dissertation. I also appreciate the input, time, and support of the members of my doctoral committee - Dr. George Czapar, Dr. Bettina Francis, and Dr. Brian Allan. I am extremely grateful to Dr. Brad Coates for his insightful comments on the research, and for his critical revision of the manuscripts. I am also grateful to Dr. Kyung Seok Kim, Dr. Weilin Sun, Dr. Carmen Valero, Dr. Venu Margam, and our collaborators in Africa - Dr. Manuele Tamò, Dr. Ibrahim Baoua, Dr. Clementine Dabire-Binso, Dr. Malick Ba, and Dr. Rousseau Djouaka, for their helpful discussions on the research, and feedback on manuscripts. For assistance with obtaining insect samples for the studies in this dissertation, I would like to thank our collaborators in Africa. I also appreciate the assistance of students, and technicians that helped with insect sample collection and processing. I would like to thank both past and current members of the Pittendrigh lab. For assistance with paperwork and the administrative aspects of my graduate study, I would like to thank both past (Audra Weinstein and Karen Trame) and current (Adrienne Harris and Kimberly Leigh) departmental office staff. I am grateful to the Legumes Innovation Lab, formerly Cowpea Collaborative Research Support Program (CRSP), and the Howard Hughes Medical Institute, for providing financial support for my graduate study. Support was provided by the Legumes Innovation Lab by the Bureau for Economic Growth, Agriculture, and Trade, United States Agency for International Development (USAID), under the terms of Grant No. vi EDH-A-00-07-00005. Support by the Howard Hughes Medical Institute was provided through a three-year International Student Research Fellowship. I would like to thank all the people who have provided moral support, friendship, and prayers. Every single act of your kindness and support is appreciated, and you have all made the journey a very memorable one for me. A very special thanks goes to my family for their love, encouragement, and support. My deepest appreciation goes to my wonderful parents, Oladeji and Omodunbi, for their love and encouragement. I am grateful to both of them for laying a solid foundation for me in education, and for all their sacrifices. I also appreciate my siblings, Adebiyi, Adeola, Adetunji, and Olufunke, for their prayers and invaluable support. My special thanks goes to my dear husband, Olusegun, for his love and patience. I am grateful to him for his sacrifices and his unfailing support throughout this journey. In all, I give thanks to God. vii LIST OF PUBLICATIONS ARISING FROM THIS DISSERTATION Agunbiade T, Steele L, Coates B, Gassmann A, Margam V, Ba M, Dabire-Binso C, Baoua I, Bello-Bravo J, Seufferheld F, Sun W, Tamò M, Pittendrigh B (2012) IPM- omics: From genomics to extension for integrated pest management of cowpea. In Boukar O, Coulibaly O, Fatokun C, Lopez K, Tamò M, (Eds.), Improving livelihoods in the cowpea value chain through advancements in science. Proceedings of the 5th World Cowpea Research Conference, pp. 231 – 248 (Chapter 1) Agunbiade TA, Coates BS, Kim KS, Forgacs D, Margam VM, Murdock LL, Ba MN, Binso-Dabire CL, Baoua I, Ishiyaku MF, Tamò M, Pittendrigh BR (2012) The spatial
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