Male Terminalia of Diptera (Insecta): a Review of Evolutionary Trends, Homology and Phylogenetic Implications

Insect Systematics & Evolution 44 (2013) 373–415 brill.com/ise Male terminalia of Diptera (Insecta): a review of evolutionary trends, homology and phylogenetic implications Bradley J. Sinclaira,*, Jeffrey M. Cummingb and Scott E. Brooksb a Canadian National Collection of Insects and Canadian Food Inspection Agency, Ottawa Plant Laboratory - Entomology, K.W. Neatby Building, Central Experimental Farm, 960 Carling Avenue, Ottawa, ON, Canada K1A 0C6 b Invertebrate Biodiversity, Agriculture and Agri-Food Canada, K.W. Neatby Building, Central Experimental Farm, 960 Carling Avenue, Ottawa, ON, Canada K1A 0C6 *Corresponding author, e-mail: [email protected] Published 25 October 2013 Abstract The male terminalia character system in Diptera is reviewed. The phylogenetic implications of apomor- phic changes are traced on published cladograms. New synapomorphies include: anteroventral parameral apodeme for the Tipulomorpha; parameral sheath encompassing desclerotized aedeagus for Neodiptera (exclusive of Axymyiidae); endoaedeagus for Xylophagomorpha + Tabanomorpha. Apystomyiidae are classified as the sister group to the Eremoneura based on four synapomorphies (lateral ejaculatory pro- cesses absent, subepandrial sclerite extending from base of hypoproct to phallus, bacilliform sclerites extending to tips of the epandrium and surstyli functionally developed, but not articulated) and lack of eremoneuran synapomorphies (i.e., loss of gonostyli, presence of postgonites and phallic plate). The Diptera sperm pump with a functional ejaculatory apodeme is a possible autapomorphy of Diptera, exclusive of Nymphomyiidae and Deuterophlebiidae. Internal details of the male terminalia of Sylvicola and Mycetobia (Anisopodidae), Hilarimorpha (Hilarimorphidae) and Apystomyia (Apystomyiidae) are newly illustrated and homologies of the aedeagus, paramere and sperm pump of the Tipuloidea are clarified. Keywords Diotera; male terminalia; male genitalia; phylogeny; Tipuloidea; Neodiptera; Anisopodidae; Hilari- morphidae; Apystomyiidae Introduction It has been nearly 20 years since the first two authors published the final two parts of the “genitalia trilogy” — an outline of the homologies and phylogenetic implications of male genitalia in Diptera (Wood 1991; Sinclair et al. 1994; Cumming et al. 1995). This special issue of Insect Systematics & Evolution, devoted to the phylogenetic signifi- cance of insect male genitalia, has provided us with the incentive to review various aspects of male terminalia in Diptera (defined as the primary genital segment or © Koninklijke Brill NV, Leiden, 2013 DOI 10.1163/1876312X-04401001 Downloaded from Brill.com09/30/2021 12:01:19PM via free access 374 B.J. Sinclair et al. / Insect Systematics & Evolution 44 (2013) 373–415 segment 9, proctiger, and any modified adjacent anterior sclerites), correct some mis- interpretations and analyze new data. There have been numerous studies on Diptera phylogeny since the early 1990s, due primarily to the rapid rise and popularity of molecular-based analyses, many of which have proposed conflicting phylogenies particularly when compared with morphological data sets. In addition, several studies on the musculature of male terminalia in lower Brachycera and nematocerous Diptera have been published during this period, which are potentially useful in evaluating proposed genitalic homologies. Diptera male terminalia demonstrate the most extreme diversity and greatest varia- bility in structure compared to any other part of the adult dipteran body. It is this extreme morphological diversity that has resulted in difficulties in recognizing homologous structures, particularly at the genus or family level and above. This is especially significant when comparing nematocerous Diptera to cyclorrhaphans. In addition, male terminalia are a key morphological source of characters used to distinguish species in the vast majority of Diptera families and there are few modern taxonomic studies that do not include illustrations of male terminalia to aid in species diagnoses. Comparative studies of Diptera male terminalia and internal anatomy have a long history, dating from the work of Dufour (1851). It is not our intent to provide a detailed history of the many studies and their contributions, as such reviews can be found in Griffiths (1972), Hennig (1973), Wood (1991), Cumming et al. (1995), Shatalkin (1995, 2012) and Zatwarnicki (1996). The following account provides a brief overview and introduction to the major historical studies. Cole (1927) provided a general survey of the diversity of Diptera male terminalia, but his illustrations were small and rather unsatisfactory, as expressed by Hennig (1973). In his textbook on insect morphology, Snodgrass (1935) illustrated males of two species of Diptera in the Tipulidae and Calliphoridae, including musculature, but unfortunately did not recognize the rotation of pregenital sclerites in the calliphorid species. Crampton (1936, 1942, 1944) provided one of the first comprehensive studies of the entire external morphology of the Diptera. He illustrated and described the male terminalia across the order focusing on rotation. External sclerites, pregenital segments and spiracles were illustrated, although he did not show internal connections and structures. In his earlier work, Crampton (1936) detailed the homology of the male terminalia of Cyclorrhapha, recognizing hypopygial circumversion, a term first proposed by Feuerborn (1922) for the characteristic 360° dextral rotation in these flies. He also considered that the surstylus was derived from tergite 9, thereby establishing a tergal or epandrial hypothesis for the origin of these claspers. This interpretation of the surstylus was followed by van Emden & Hennig (1956). Steyskal (1957) introduced the terms protandrium (pregenital) and andrium (terminalia) for descriptions of the postabdomens of acalyptrate Diptera. He presented diagrams of the protandria (ventral view of the pregenital sclerites) illustrating their asymmetry and the position of the spiracles. Subsequently McAlpine (1985) referred to these diagrams of the protandria as protandrograms. Griffiths (1972) presented his periandrial hypothesis on the homology of male cyclorrhaphan Diptera terminalia (see Cumming et al. 1995 for discussion). The main Downloaded from Brill.com09/30/2021 12:01:19PM via free access B.J. Sinclair et al. / Insect Systematics & Evolution 44 (2013) 373–415 375 dorsal genital sclerite was considered to be a replacement sclerite termed the perian- drium. It and the dorsal clasping structures were considered to be derived from sternite 9. Griffiths (1972, 1981, 1990b) based his homology theory on the a priori assump- tion of functional continuity in clasping function throughout the Diptera, such that the ventral claspers on sternite 9 (gonostyli) in the lower Diptera became the dorsal clasping structures in Eremoneura. In his initial studies Hennig (1936, 1958) was apparently undecided on which homology theory to adopt, and was still somewhat undecided in Hennig (1973) (Ulrich pers. comm.). It was not until somewhat later (Hennig 1976) that he clearly decided on a tergal, or “epandrial hypothesis”, and provided details and reasons for his conclusions. In this study, Hennig detailed the male genitalia of the family Lonchopteridae and outlined the evolution of the male terminalia in Brachycera, including the musculature. Ulrich (1972) studied the musculature in two species of Empididae and proposed the fusion hypothesis (with the epandrium fused to the gonocoxites) in his assessment of male genitalic homologies in the Empidoidea. This homology concept, which considered the dorsal claspers to be sternal, was in agreement with the early ideas of Hennig (1936). McAlpine (1981) closely followed the epandrial hypothesis of Hennig (1976), but refined some of the homologies, in particular interpreting the postgonites of Cyclorrhapha as homologous with parameres in the lower Diptera. He also accepted Hennig’s (1976) interpretation that dorsal clasping lobes (surstyli) were derived from a division of the tenth tergite. Griffiths (1981, 1990a) was highly critical of the morphological interpretations and phylogeny in the Manual of Nearctic Diptera (McAlpine 1981, 1989; Wood & Borkent 1989; Woodley 1989). In particular Griffiths (1981) cited the ontogenetic studies of Dobzhansky (1930), Black (1966), and Laugé (1968), which indicate the dorsal clasping lobes are derived from segment 9, as evidence invalidating all of McAlpine’s (1981) epandrial homology interpretations. Wood (1991), Sinclair et al. (1994) and Cumming et al. (1995) presented a detailed survey of male genitalic homologies and traced their phylogenetic implications on cladograms across the order. The unique use of colour combined with the artistry of Ralph Idema (see Cumming et al. 2011) helped to lay out the intricate details among families. Cumming et al. (1995) reviewed the two main competing genitalic homology theories (epandrial versus periandrial) and presented an alternative interpretation of male genitalic homologies (revised epandrial hypothesis), which addressed the weak- nesses of the epandrial hypothesis of McAlpine (1981) that Griffiths (1981) had criti- cized. For example, the outer wall of the surstylus was considered by Cumming et al. (1995) to be derived from tergite 9 and the inner wall from a sclerotization of the intersegmental membrane, rather than segment 10. The musculature of the surstylus as outlined by Ovtshinnikova

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