Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior PDF

Preface

The main purpose of this book is to discuss and promote the study of the evolution of fruit fly (Diptera: Tephritidae) behavior. As a basis for this discussion, we review the current state of knowledge and publish considerable new findings on various aspects of fruit fly behavior, phylogeny, and related subjects. Fruit flies are considered one of the most economically important groups of insect pests worldwide, and study of their behavior plays a critical role in their regulation and control. To give only one example, the annual cost of the establishment of the Mediterranean fruit fly in California has been estimated at approximately $1.2 billion by the California Department of Food and Agriculture. We note that the success of one of the most environmentally friendly control measures, the Sterile Insect Technique, hinges on a deep understanding of behavioral mechanisms (i.e., sexual selection) which will be thoroughly discussed in this book.

Given the tremendous economic importance of many species of Tephritidae, the study of fruit flies has been traditionally biased toward applied aspects (e.g., management, monitoring, mass rearing). Nevertheless, their ecological and behavioral plasticity render them ideal study objects to address basic biological and evolutionary questions of interest to a wide audience. Fruit flies have been used as models for the development of general theories on, for example, speciation processes (Bush 1975), mating behavior (Höglund and Alatalo 1995; Eberhard 1996; Shelly and Whittier 1997) and demography (Carey 1993). In the past 15 years, a number of broad-ranging books on fruit fly biology and/or management have been published: Cavalloro (1983; 1986), Mangel et al. (1986), Economopoulos (1987), Robinson and Hooper (1989), Vijaysegaran and Ibrahim (1991), White and Elson-Harris (1992), Aluja (1993), Aluja and Liedo (1993), Calkins et al. (1994), and McPheron and Steck (1996). In these books, one can find isolated chapters (in some cases very short reviews) dealing with behavior of particular genera or groups of fruit fly species, but there is a strong bias toward economically important species. The topics of phylogeny and evolution of behavior are barely addressed and, when so, only superficially. In this book we attempt a more comprehensive and thorough approach, covering all behaviors in a broad range of tephritids, incorporating phylogenies as much as possible. We are therefore confident that this book will bridge an important information gap in a highly visible group of insects and also serve as a blueprint for basic and applied behavioral research on fruit flies and other organisms in the coming years.

Hypotheses of phylogenetic relationships are valuable tools to understand the evolution of any trait in a group of organisms, and their use is becoming widely accepted in the study of animal behavior (see Martins 1996). Promoting their use by students of fruit fly behavior is one of the major goals of this book. Despite the economic importance of fruit flies, few rigorous, comprehensive phylogenies have been published for tephritid groups (see review by Norrbom et al. 1999a). Even for the economically important genera Anastrepha , Bactrocera , Ceratitis , Dacus, and Toxotrypana there are no, or at most partial, phylogenies available. On the other hand, in the last decade analyses of phylogenetic relationships have intensified in systematic work on Tephritidae, and nearly all genera and species of fruit flies worldwide have just been cataloged (Norrbom et al. 1999b). Thus, we felt the time was ripe to ask the world's leading tephritid systematists to tackle this phylogenetic problem. Their response has exceeded our greatest expectations.

Although we must warn the reader that the level of methodology varies from the latest cladistic techniques to "scenario writing," and that some results are still preliminary (but kindly included by the authors at our request), the phylogenetic chapters of this book include analyses to at least a minimal level for nearly all groups of fruit flies whose behavior has been studied to a significant degree. Notably, they include analyses of relationships among the families most closely related tofruit flies and among the higher groups (subfamilies and tribes) within Tephritidae (Korneyev); a preliminary analysis of higher tephritid relationships based on mitochondrial DNA data (Han and McPheron); a review of relationships within the subtribe Carpomyina, which includes Rhagoletis , by far the most intensively studied fruit fly genus in terms of diversity of phylogenetic methods (Smith and Bush); the first comprehensive morphological analysis and the first molecular analysis of Anastrepha and Toxotrypana (Norrbom et al. and McPheron et al.); the first, although preliminary, cladistic analyses of Ceratitis (De Meyer) and Bactrocera and Dacus (White); and the first cladistic analyses of the tribe Trypetini (Han), the subfamily Blepharoneurinae (Norrbom and Condon), and the tephritine tribe Myopitini (Freidberg and Norrbom) and Tephritis group of genera (Merz).

The book is intended to become a general reference. It therefore contains reviews of past and present work but also indicates potential future directions of research. We have asked authors not only to review all past work, but also to make an effort to present novel, unpublished results and to try to foster the conceptual advancement of the field.

This volume is divided into eight sections. Section 1 provides a general framework for the rest of the book. It contains an overview of the phylogeny of the Tephritoidea (Korneyev), a review of the behaviors exhibited by flies in the families most closely related to the Tephritidae (Sivinski), and a historical review of studies on tephritid behavior (Díaz-Fleischer and Aluja).

Each of the next five sections covers the phylogeny and behavior of important groups of tephritids — Blepharoneurinae (Norrbom and Condon; Condon and Norrbom), Phytalmiinae (Dodson), Toxotrypanini (Norrbom et al.; McPheron et al.; Aluja et al.; and Landolt), Carpomyina (Smith and Bush; Prokopy and Papaj), Dacinae (De Meyer; Eberhard; Yuval and Hendrichs; White; Drew and Hancock; Drew and Romig), Trypetini (Han), and Tephritinae (Korneyev; Freidberg and Norrbom; Merz; Headrick and Goeden). The classification of these groups follows that by Korneyev (Chapter 4). A detailed list of genera, following a slightly different classification, is included by Norrbom et al. (1999a). In the exceptional case of the genus Ceratitis there are two separate behavior chapters: one dealing specifically with the sexual behavior of C. capitata (Eberhard), and the other reviewing the other behaviors of this species and all behavior of the other species of Ceratitis (Yuval and Hendrichs). This is because C . capitata is by far the best-studied fruit fly, and a review of only its sexual behavior turned out to be as long as a review of all the remaining behaviors for the whole genus.

The next section of the book deals with specific topics, but on a broader scale than in previous chapters. We asked the authors of most of these chapters to analyze a specific topic based on all relevant data from across the Tephritidae and, where appropriate, to examine it from a phylogenetic viewpoint. The chapters on the evolution of feeding, mating, and oviposition behavior (Drew and Yuval, Sivinski et al., and Díaz-Fleischer et al., respectively) are among the most relevant to the primary goal of the book. They are products of teams of authors, and we wish to recognize here the monumental task of the lead authors in coordinating these chapters. Other chapters in this section include a review of tephritid population structure by Berlocher, which clearly explains a complex subject, and another by Cayol on the changes in sexual behavior and some life history traits generated by inadvertent artificial selection during mass rearing of certain economically important species (e.g., C. capitata , B. cucurbitae , B . dorsalis , A. ludens ). This chapter was of particular interest to us because it addresses a highly applied aspect of fruit fly behavior and ecology. Framing such findings within an evolutionary perspective will be of great value to action programs, whose technical personnel may lack the proper theoretical background to understand the underlying mechanisms behind inadvertent artificial selection during mass rearing, and to allow them to design proper schemes to monitor and avoid it.

Since we wanted to end the book with a bang, we invited Robert Heath and Kenneth Kaneshiro to address topics of great applied and basic interest: Sexual pheromones in tephritid flies and the behavior of a distantly related group of flies ( Drosophila ). Heath and his collaborators have been generating very interesting information on the chemical characterization of the sexual pheromones of several species of Anastrepha . Such information, if investigated in additional species and genera, would be a novel and potentially useful data set for analysis of phylogenetic relationships in fruit flies. The fact that this information will be published here for the first time will no doubt make this chapter one of the most cited pieces of work on fruit fly chemical ecology. Ending this section with an overview of behavior in Drosophila , a group in which phylogenetic relationships are better resolved and the evolution of behavior fairly well understood, allows us both to honor the important contributions of Kenneth Kaneshiro to the study of fruit flies, and to draw interesting parallels between drosophilids and tephritids.

This book clearly has a hybrid nature and many readers are likely to be specialists in one field who are unfamiliar with the jargon used in others. Despite the efforts to review the meaning of some of these terms at the symposium in Xalapa, there was still some loss of communication between taxonomists and behaviorists. The final section of the book therefore contains a glossary of terminology in the areas of systematics, morphology, phylogeny reconstruction, ecology, and behavior (White et al.). We sincerely hope that such information will assist researchers throughout the world and will be of great value in standardizing the terminology used in publications of this nature (a much-needed effort).

Before ending, we would like to highlight some important aspects related to the genesis of this book and to our desire to recognize the pioneering work of D. Elmo Hardy and Ronald J. Prokopy. The idea of putting together a volume like this came when one of us (M.A.) was chairman of the Working Group on Fruit Flies of the International Organization for Biological Control of Noxious Plants and Animals (IOBC). This working group has a long and successful history, thanks largely to the efforts of the distinguished Swiss entomologist, Ernst Boller. M.A. felt the strong urge, as chairman of this group, to contribute something substantial to the field and, at the same time, to honor the rich history of the group. A book on a challenging topic, such as the evolution of fruit fly behavior, seemed like the best solution. As a result of fruitful discussions with A.L.N. and key researchers in the field, it was decided to organize a symposium during which all speakers would bring drafts of their prospective book chapters. The idea was to give everybody a chance to present and discuss the contents of their manuscripts with all other authors and to allow the editors to start working directly with authors during the early stages of the writing process. Fortunately, our hopes were realized and 35 scientists from 14 countries met in Xalapa, Veracruz, Mexico from February 16 to 21, 1998. The symposium, attended by nearly all of the world's top experts on fruit fly taxonomy and behavior, turned out to be a fantastic experience for everybody involved and, as expected, allowed all authors to get a clear idea of what was missing in their chapters. Also, it allowed all participants to discuss in great detail the topic of the symposium and the future book. This was particularly important to those participating in the collaborative effort of writing chapters on the evolution of feeding, mating, and oviposition behaviors. Among many other reasons, we believe that the symposium was worthwhile just to promote collaboration among the many participants who had never met and particularly to promote interaction between the taxonomists and behaviorists. For example, none of us except a few of the taxonomists had ever met Valery Korneyev, a Ukranian who is the most knowledgeable scientist in the area of fruit fly phylogeny and whose work until recently had been published exclusively in Russian.

The fact that this book is dedicated to D. Elmo Hardy and Ronald J. Prokopy should be easily understood. We believe, as do many others, that these two distinguished scientists have had a major impact in the fields of fruit fly behavior and systematics. Recognizing their fundamental contributions seemed to us both an obligation and a natural consequence of the deep respect we have for their work.

We sincerely hope that this volume will motivate many to share our enthusiasm and admiration for this wonderful group of insects, who zealously guard the secrets of their lives. Attempting to unravel these secrets is both motivating and humbling. ¡Vivan las moscas de la fruta! Long live the fruit flies!