The Evolutionary Biology of Flies. David Yeates and Brian Wiegmann, eds. Columbia University Press, New York, 2005. 430 pp., illus. $89.50 (ISBN 0231127006 cloth).
Anyone who's ever visited a feedlot knows about flies. With 120,000 described species in 150 families, the Diptera comprise some 12 percent of known insect diversity, exceeded only by beetles (350,000 species), bees and wasps (125,000 species), and moths and butterflies (150,000 species) (Grimaldi and Engel 2005). But if you're familiar with flies' ubiquity, their unmatched structural, developmental, and ecological diversity, their impact on humans as vectors of disease, and the countless contributions of Drosophila melanogaster to knowledge of modern biology, then you know that flies are important even if you can't abide them. In The Evolutionary Biology of Flies, editors David Yeates, a research systematist at the Australian National Insect Collection, Commonwealth Scientific and Industrial Research Organisation, and Brian Wiegmann, associate professor of entomology at North Carolina State University, and 20 other biologists review many aspects of fly phylogeny and biology with two goals in mind: (1) to document the impact of the study of flies on all aspects of evolutionary biology and (2) to support the case for this order becoming a “model clade” for more intense future examination.
Although cladistic analysis pervades all branches of comparative biology, medicine, and agriculture because of its historical and predictive power, it is not well known that its basic concepts and methods were devised by a dipterist, Willi Hennig, and first published in German in 1950; not until the publication of Hennig's English summary in the Annual Review of Entomology (vol. 10: 97–116) in 1965 and his book Phylogenetic Systematics in 1966 did cladistic analysis come into wide use. Rudolf Meier critically examines the development of Hennig's methods, their increasing influence on the practice of systematic and evolutionary biology, and the later abandonment of some of his principles (e.g., a stem species ceases to exist when it speciates and always gives rise to two descendant species; ranks in the taxonomic hierarchy should be assigned on the basis of their first appearance in the fossil record).
Hennig's numerous comparative studies of wing venation, genitalic structure, and larvae led him to propose many of the higher dipteran taxa recognized today, and others represent important contributions to knowledge of their fossils and biogeography. He also helped significantly in the unraveling of the phylogeny of other insects (Hennig 1969).
Michael Whiting summarizes the convoluted history of evolutionary relationships of the flies to other insects and concludes that the evidence indicates that the Diptera constitute the sister group of the Strepsiptera (twisted-wing insects) within the higher taxon Mecopterida (with scorpionflies and fleas), these, in turn, constituting the sister group of the Amphiesmenoptera (caddisflies, moths, and butterflies) within the subclass Endopterygota (insects that undergo a complete metamorphosis). The editors then subject the 19 currently recognized major lineages of Diptera to a supertree analysis, examine relationships within each clade, and compare the estimated divergence times indicated by their earliest appearance in the fossil record with those inferred from cladistic comparison of homologous nucleotide sequences of nuclear genes. Though these dates agree in sequential order, the molecular data provide earlier estimates than the fossils (e.g., basal Diptera: 248–283 versus 233 million years ago [Ma]; Drosophilidae: 99 versus 30 Ma), as is usual in such comparisons. The editors find strong support for monophyly of some major clades—the Brachycera, Eremoneura, Cyclorrhapha, Schizophora, and Calyptrata—but not for some basal dipteran clades, and less for the acalypterates, a large assemblage of mostly nondescript little flies, including D. melanogaster.
Conrad Labandeira reviews and illustrates 233 million years of dipteran evolution and ecology from the standpoint of his encyclopedic knowledge of their way of life, phylogeny, and fossil record, as well as his analysis of family-level feeding guilds. These he infers from examination of fossil insect and plant assemblages from different levels in the rock record. This evidence suggests that diversification of basal (nematoceran) lineages began in the Upper Triassic, of brachycerans in the Upper Jurassic, of eremoneurans in the Lower Cretaceous just before the major angiosperm radiation of 115 to 95 Ma, and of schizophorans in the Lower Cenozoic. The last of these was partly influenced by the radiation of mammals.
This diversification occurred in a world of changing continental position, climate, and biota following the breakup of Pangaea. Peter Cranston documents how these disruptions continually influenced the distributions of flies and addresses the historical biogeography of various groups of chironomid midges, from ecologic, phenetic, dispersalist, and vicariant points of view. He summarizes the pitfalls of each approach and ends with a detailed historical account of chironomid distributional patterns.
The first insect to have its genome sequenced was D. melanogaster, in the year 2000. This was followed by 12 other Drosophila species, the malaria mosquito Anopheles gambiae, and the yellow fever mosquito Aedes aegypti. Michael Ashburner reviews what is known about dipteran genomes, particularly of D. melanogaster and relatives, and provides copious information on genome size, organization, and composition. Ashburner also discusses transposable elements (treated more fully by Margaret Kidwell). These were originally thought to be selfish DNA, but are now known to induce, rarely, adaptive change in the genomes of recipients; a few are widely used as vectors to transfer genes between species. In addition, Ashburner covers sex chromosomes. These are further discussed by Rob DeSalle and, in greater detail, by Neil Davies and George Roderick. Rob DeSalle addresses from a phylogenetic context the “molecular toolkit” governing development of larval and imaginal body plans in D. melanogaster; the distribution and evolution of early-acting pattern control genes such as bicoid; and the origin of long- and short-germ embryos, wing veins and wing pigmenation, sex determination, and bristle pattern.
Larval flies are among the most diverse and highly specialized of insects, and differ substantially in form and behavior from their adults, particularly in advanced species. They are mostly adapted to life in moist or aquatic habitats. Correlated with this divergence are major structural differences between the larval and adult central nervous system (CNS) and peripheral nervous system, as summarized in an evolutionary context by David Merritt. Unlike the nervous systems of ametabolous and hemimetabolous insects, those of flies and of other advanced holometabolous insects undergo two bouts of neurogenesis: one in the embryo, to generate the larval system, and the other in the late larva and early pupa, to replace it with a quite different imaginal system. The embryonic nerve mother cells (neuroblasts) that produce neurons for the CNS of larvae, rather than degenerating as in other insects, become quiescent in late embryogenesis and reactivate in older larvae to produce imaginal neurons. Though many larval neurons degenerate, most larval motor neurons are respecified to control the dispersive and reproductive behavior of a totally reorganized adult. Moreover, some larval sensory neurons persist thoughout metamorphosis. Because of the seamless continuum in nervous system metamorphosis between basal and derived flies, our extensive genetic and molecular understanding of neurogenesis in D. melanogaster can be applied to other flies.
Other topics addressed comparatively in the book, though not in a phylogenetic context, are sexual selection and the evolution of mating systems (Gerald Wilkinson and Philip Johns), ecological genetics of host use (Kenneth Filchak, Bill Etges, Nora Besansky, and James Feder), the use of molecular markers to investigate cryptic species, and the sites of origin and rates of spread of invasive species (Sonja Scheffer). Roger Kitching, Daniel Bickel, and Sarah Boulter provide feeding-guild analysis at the family level of larval and adult fly assemblages active at different levels and seasons in the rainforests of Papua New Guinea and Queensland, Australia.
The book's dust jacket bears a color photo of a deerfly resting on a marigold. Its page size, format, and heft resemble those of an Annual Review volume, although the print size is smaller. Though it is authoritative, well written, and typo-free, there is little linkage between some chapters, and an obvious divide between those that are historically oriented and those that are process-oriented. The 14 tables and 43 figures are clear and well produced, but some are greatly reduced and require careful study. Most of the essays, which range from brief to encyclopedic, provide suggestions for future work and detailed entry points to the primary literature. Dipterists will profit from having this diverse material in one volume but should read it in conjunction with chapter 12 in Grimaldi and Engel (2005), who provide a far more effective and beautiful overview of dipteran life history and evolution.
