Phylogeny of True Flies (Diptera): A 250 Million Year Old Success Story in Terrestrial Diversification
David K. Yeates, CSIRO Entomology PO Box 1700 Canberra AUSTRALIA.
Rudolf Meier, Department of Biological Sciences, National University of Singapore, SINGAPORE.
Brian Wiegmann, Department of Entomology, North Carolina State University, Raleigh NC USA.
The insect order Diptera (true flies) is one of the most species rich, anatomically varied and ecologically innovative groups of organisms, making up around 12% of the known animal species. An estimated 125,000 species of Diptera have been described, however, the total number of extant fly species is many times greater. The living dipteran species have been classified into about 10,000 genera, 150 families, 22-32 superfamilies, 8-10 infraorders and 2 suborders (Yeates & Wiegmann, 1999). The monophyly of Diptera is well established. Hennig (1973) lists 37 autapomorphies some of which form morphologically complex structures such as the specialized mouthparts adapted for sponging liquids. Traditionally, the best-known autapomorphy is the transformation of the hind wings into halteres, but this character may now be in need of reinterpretation due to recent phylogenetic research suggesting a sister group relationship between Strepsiptera and Diptera (Whiting et al. 1997). This work implies homology between the Diptera halteres and Strepsiptera pseudohalteres. The sister group of Diptera remains unknown. Morphology suggests either Mecoptera, Siphonaptera, or a monophylum consisting of both, but based on the aforementioned molecular evidence the Strepsiptera has to be added to the list of candidate taxa. The first fossils attributable to Diptera are known from the Permian, and a large number of fossil Diptera are known from the Mesozoic (Yeates & Wiegmann, 1999).
Phylogenetic work in the strict sense on Diptera began with Hennig (1973) and Griffiths (1972). Only recently, numerical analyses have started to address the relationships within higher level taxa. Although molecular data has been used increasingly to reconstruct Dipteran phylogenies, most published analyses to date have focussed on questions at a lower-level, generally within particular infraorders. An exception is a recent detailed analysis of Brachycera relationships using over 2 Kb of 28S rDNA (Wiegmann and Yeates in prep.). The results of the last 30 years of phylogenetic research on the higher-level relationships of the Diptera using morphological data have been synthesised by us using supertree techniques. This Diptera supertree forms the framework for the following discussion.
The supertree generally supports recent research and shows that major dipteran higher categories such as Brachycera, Eremoneura, Muscomorpha, Cyclorrhapha, Schizophora, and Calyptrata are monophyletic. Conversely, a number of traditional higher taxa are paraphyletic based on morphological and molecular data. These include the Nematocera, Orthorrhapha, and Achiza. We therefore prefer to use the informal terms Lower Diptera, Lower Brachycera and Lower Cyclorrhapha for these groups. They represent evolutionary grades at the base of major radiations of Diptera, Brachycera, and Cyclorrhapha, respectively.
The paraphyly of the Lower Diptera has been suspected for decades, beginning with Hennig, and demonstrated in recent quantitative cladistic analyses using morphological data (Oosterbroek & Courtney, 1995). There have been only a few comprehensive phylogenetic analyses of the relationships between Lower Dipteran families using morphological and especially molecular data. The position of the tipulids and their relatives has been very unstable; some morphological treatments consider them the basal lineage of Diptera (Hennig, 1973), while others consider them to be closely related to Brachycera (Oosterbroek & Courtney, 1995). The supertree analysis currently favors Ptychopteromorpha+Culicomorpha as the sister group to the remaining Diptera with Blepharicerimorpha and Bibionomorpha being the next lineages to emerge from the Lower Dipteran stem. Close to the grade transition to Brachycera, the Lower Dipteran infraorders are not monophyletic, with Psychodomorpha and Tipulomorpha forming a paraphyletic grouping, the superfamily Tipuloidea being sister to the Brachycera. The arrangement of Tipulomorpha and Psychodomorpha represents a resolution of the incongruence between input trees.
The Brachycera is certainly a monophyletic group, with a large number of undisputed autapomorphies. The phylogeny of the lower Brachycera has been scrutinized intensively over the past 15 years. A recent quantitative reanalysis of morphological characters used to define relationships between the lower Brachyceran families attempted to summarize and synthesize this research (Yeates, 2002). This study revealed weak evidence for the monophyly of a clade containing Xylophagomorpha, Stratiomyomorpha and Tabanomorpha, and weak evidence for a monophyletic Asiloidea, and these findings are reflected in the supertree. The most basal lineage of Brachycera in the supertree analysis contains, Stratiomyomorpha plus (Xylophagomorpha + Tabanomorpha), reflecting the results of recent quantitative cladistic analyses. The infraorder Muscomorpha contains all brachyceran families except those belonging to Stratiomyomorpha, Xylophagomorpha and Tabanomorpha, and is a well-supported clade found on the supertree. The Nemestrinoidea, Asiloidea and Empidoidea are monophyletic, arising from the main stem of the Brachycera in that sequence. Evidence for the monophyly of nemestrinoids and asiloids is not strong, and they appear paraphyletic in some analyses. A number of asiloid families have received critical phylogenetic scrutiny in recent years, partly because of their proximity to Eremoneura.
Eremoneura is the muscomorphan lineage containing Empidoidea + Cyclorrhapha, and is one of the best-supported higher-level brachyceran clades with many synapomorphies. Recent morphological work has emphasised male genitalic characters for phylogenetic reconstruction in Eremoneura, however some analyses of molecular data are beginning to appear. There is strong evidence for the monophyly of the Empidoidea, and the Atelestidae, Hybotidae, Empididae and Microphoridae + Dolichopodidae from both morphological and molecular data.
Cyclorrhaphan monophyly is well supported by characters such as the invagination of the larval head capsule and modifications of the larval mouthparts, as well as pupation within the skin of the last larval instar. These are the most recognizable features of this landmark in dipteran evolution. Over the last 40 years only three workers have attempted to synthesize phylogenetic evidence on cyclorrhaphan relationships in a comprehensive fashion. All studies were not based on explicit data sets and results differed in many regards (Hennig, 1973; Griffiths, 1972; McAlpine, 1989). Exploration of new character systems applied broadly across cyclorrhaphan groups, for example from egg and larval morphology, female genitalia and internal morphology, and nucleotide sequences are urgently needed. There are a number of competing hypotheses regarding the relationships of the families belonging to the Lower Cyclorrhaphan grade, but the Syrphoidea are generally regarded the sister group to the Schizophora.
The monophyletic Schizophora are classified into at least 80 families and comprise just over half the family-level diversity in Diptera. Major reviews of Schizophora phylogeny are the synthetic revisions by Griffiths (1972) and McAlpine (1989) which provided new information while building on Hennig’s earlier research. Griffiths (1972) provided detailed interpretation and scorings of male genital characters along with other morphological features, and McAlpineÕs (1989) fully resolved phylogenetic arrangements draw on most morphological character systems as well fly biology. Based on calypter morphology the Schizophora have been traditionally subdivided into the Acalyptratae and Calyptratae, but it has long been recognised that the calypter is too variable in both groups to be a reliable phylogenetic marker. Although the former is supported on our supertree it is generally regarded as being paraphyletic.
McAlpine (1989) divided the Acalyptratae into 10 superfamilies and these are found in the supertree: Nerioidea, Diopsoidea, Conopoidea, Tephritoidea, Lauxanioidea, Sciomyzoidea, Opomyzoidea, Sphaeroceroidea, Carnoidea, and Ephydroidea. Only few superfamilies are uncontentious (e.g., Ephydroidea, Tephritoidea) while the remaining will probably see some major rearrangements after more intensive phylogenetic scrutiny. Generally, McAlpine’s (1989) classification maintains Hennig’s (1973) groupings while Griffiths (1972) proposes a more radical restructuring. In contrast to the Acalyptratae and despite the lack of complex morphological autapomorphies, the Calyptratae appear monophyletic based on molecular and morphological evidence. Of the three superfamily-level taxa, the Hippoboscoidea are monophyletic, the Oestroidea may be monophyletic, while the Muscoidea is likely paraphyletic.
Advances in understanding the relationships of flies will accelerate with the increasing use of molecular data and quantitatively analysed data matrices. The National Science Foundation has recently funded a five-year collaborative initiative to generate a phylogeny of Diptera (see www.diptera.org). The project will compile gene sequences, full mitochondrial genomes and complete phenotypic character matrices for members of all fly families.
The most important areas for future phylogenetic research in the Diptera are in the Lower Diptera and Schizophora. In the Lower Diptera, resolving the relationships between the infraorders and the position of the craneflies and their relatives (Tipulidae) are critical tasks. The Schizophora also await more focused phylogenetic scrutiny applied to relationships between, and within, the superfamilies as they are currently defined.
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