The evolution and biogeography of the austral horse fly tribe Scionini (Diptera: Tabanidae: Pangoniinae) inferred from multiple mitochondrial and nuclear genes
Graphical abstract
Introduction
The Tabanidae, commonly referred to as horse, deer or march flies, are a large cosmopolitan Dipteran family with nearly 4400 described species (Pape and Thompson, 2012). The family exhibits sexual dimorphism in feeding habits, as adult females are typically blood-feeding, whereas males are nectar feeding. Consequently, female horse flies are principal vectors of many disease-causing microorganisms accumulated in the mouthparts, salivary glands and/or tarsi that are mechanically transferred during feeding. Horse flies spread anaplasmosis (Scoles et al., 2008) and bovine leukaemia virus (Foil et al., 1988) in cattle, equine infectious anaemia in horses (Foil et al., 1984), and the filarial nematode Pelecitus roemeri and trypanosomiases (Reid et al., 2001) in kangaroos and wallabies (Spratt, 1972a, Spratt, 1972b, Spratt, 1974a, Spratt, 1974b, Spratt, 1975). Humans can also be affected by the feeding habits of females, including infections of loiasis, tularaemia and even anthrax (Krinsky, 1976, Foil, 1989).
In contrast, nectar-feeding by adult horse flies reinforces the ecological importance of the family as vital pollinators (Johnson and Morita, 2006, Lessard and Yeates, 2012b, Mackerras, 1957, Mackerras, 1960). Myrtaceae are commonly frequented by horse flies in the southern hemisphere, including Eucalyptus, Grevillea and Melaleuca in Australia, Leptospermum in both Australia and New Zealand, and Luma in South America (Lessard and Yeates, 2012b, Mackerras, 1957, Mackerras, 1960, Tillyard, 1926).
The taxonomy of the Tabanidae is fairly stable as a result of the extensive work of Mackerras, 1954, Mackerras, 1955 who provided a classification scheme that is still in use today. This scheme is based on external and genital characters of adults and includes four subfamilies, with further division into one to four tribes: Chrysopsinae (Bouvieromyiini, Chrysopini and Rhinomyzini), Pangoniinae (Mycteromyiini [added by Coscarón and Philip (1979)], Pangoniini, Philolichini and Scionini), Scepsidinae, and the largest of the subfamilies Tabaninae (Diachlorini, Haematopotini and Tabanini).
The subfamily Pangoniinae has a near global distribution, with members usually possessing a long proboscis and relatively long, slender legs that are well adapted to grasping flowers (Mackerras, 1955). Currently the Pangoniinae consists of four tribes: the Mycteromyiini (Neotropical in distribution), Pangoniini (Australasian, Nearctic, Neotropical and Palearctic), Philolichini (Afrotropical, Australasian and Oriental) and the Scionini (Australasian, Nearctic and Neotropical) (Coscarón and Philip, 1979, Lessard and Yeates, 2011, Lessard and Yeates, 2012a, Lessard and Yeates, 2012b, Mackerras, 1954, Mackerras, 1955, Morita, 2008).
The Scionini are mostly stout, bearded and hairy-eyed flies. The tribe is currently divided into seven genera, of which some are further divided into subgenera (Fig. 1): Anzomyia Lessard, 2012, Caenopangonia Kröber, 1930, Fidena Walker, 1850, Goniops Aldrich, 1892, Pityocera Giglio-Tos, 1896, Scaptia Walker, 1850, and Scione Walker, 1850. The tribe occurs predominantly in the southern hemisphere (Coscarón and Wilkerson, 1985, Coscarón and González, 2001, Coscarón and Iide, 2003, Lessard and Yeates, 2011, Lessard and Yeates, 2012a, Lessard and Yeates, 2012b, Mackerras, 1957, Mackerras, 1960, Mackerras, 1961, Mackerras, 1964, Oldroyd, 1947, Wilkerson and Coscarón, 1984), with the exception of the monotypic genus Goniops that is endemic to the Nearctic. The two peculiar genera, Caenopangonia and Goniops, notably differ from the remainder of Scionini by possessing bare eyes and an extremely widened frons.
The genus Scaptia is the most species-rich of all the Scionini and has an exclusive southern hemisphere distribution in Australia, New Guinea, New Zealand and South America. The genus is further divided into seven subgenera (Fig. 1), including Lepmia Fairchild 1969 (found in Brazil), Pseudomelpia Enderlein, 1922 (Chile), Myioscaptia Mackerras, 1955 (Australia), Palimmecomyia Taylor 1917 (Australia), Plinthina Walker, 1850 (Australia), Scaptia Walker, 1850 (Australia, Chile, Peru, Bolivia, Argentina) and Pseudoscione Lutz in Lutz, Araujo and Fonseca 1918 (Australia, Argentina, Brazil, Chile, New Guinea and New Zealand).
The taxonomy of the family below the tribal level is challenging and the phylogenetic relationships are largely unknown. The identification and classification is hindered by the typical lack of definitive characters for genera and species, particularly demonstrated in the genitalia where large structural differences do not correspond with differences in external morphology, which often cannot aid in species identification (Mackerras, 1955, Mackerras, 1960). Preservation can also impact on common diagnostic characters, such as the augmentation of proboscis length during death (Wilkerson and Coscarón, 1984), which can impede subgeneric diagnoses, or colour fading that can affect species-level identification of specimens (Mackerras, 1960, Mackerras et al., 2008).
Modern workers have found strong support for the monophyly for the Tabanidae, based on both morphological (Mackerras, 1954, Yeates, 2002) and molecular evidence (Morita, 2008, Wiegmann et al., 2000, Wiegmann et al., 2003, Wiegmann et al., 2011). Molecular data has been recently successful in reconstructing phylogenetic histories for the Tabanidae. Wiegmann et al. (2000) used the ribosomal 28S gene to demonstrate the well-supported monophyly of the Tabanidae, with each major subfamily recovering as monophyletic, including two species of the Chrysopsinae, four species of the Tabaninae, and two species of the Pangoniinae, each belonging to the Mycteromyiini and Pangoniini (Wiegmann et al., 2000; Fig. 2, p. 1035). Morita (2008) was the first to explore the phylogenetic relationships of the Tabanidae below the subfamily level using Cytochrome Oxidase Subunit One (COI) and the first fragment of the nuclear protein-coding gene carbamoyl-phosphate synthetase-aspartate transcarbamoylase-dihydroorotase (CAD1; Moulton and Wiegmann, 2004). This previous study demonstrated strong support for the monophyly of each subfamily, however, focused only on the tribes Pangoniini and Philolichini from the subfamily Pangoniinae and did not include members of the tribe Scionini. Other studies on the systematics of the Tabanidae remain extremely limited.
The phylogeny and taxonomy of the Scionini is thus unclear and hindered by the limited availability of reliable morphological characters. Moreover, the original descriptions for many genera are frequently insufficient and provided with little systematic context, with many genera often presented without a formal description or solely mentioned in either a taxonomic key or checklist of species (Enderlein, 1922, Enderlein, 1925, Lutz et al., 1918). The present study employs molecular data to provide the first robust quantitative phylogenetic framework and insight into the evolution of the Scionini, with a focus on the widely dispersed genus Scaptia. It extends the work of Morita (2008) by testing the utility of current morphological classification schemes within the Tabanidae. Divergence time estimation and the fossil record is used to determine whether the current distribution of the Scionini is a result of the sequential fragmentation of the ancient supercontinent of Gondwana, as well as providing insights into the origin of the tribe.
Section snippets
Taxon sampling
Scionini specimens were collected from a range of localities in Australia, New Zealand and the Americas (Table 1). Six out of the seven Scionini genera were sampled, including the monotypic Goniops, four species of Fidena, one species of Pityocera, 7 species of Scione, one species of Anzomyia, and for the subgenera of Scaptia, three species of Scaptia (Myioscaptia), four species of Scaptia (Plinthina), 27 species of Scaptia (Pseudoscione), and 16 species of Scaptia (Scaptia). Specimens were
Results and discussion
Phylogenetic relationships of the Tabanidae are depicted in Fig. 2. All clades are strongly monophyletic (PP > 90, BS > 75) unless otherwise stated. The Bayesian and ML analyses largely agreed with one another, with the exception of the following differences in the ML analysis: Tabanus sp. (BDL149) grouped as sister to Dasybasis (ML bootstrap value [BS] = 74; Fig. 2) instead of the Haematopota + Hybomitra + Tabanus clade (Bayesian posterior probability [PP] = 62); and the unsupported sister relationships
Conclusion
This study successfully reconstructed the phylogenetic relationships of the austral horse fly tribe Scionini using multiple independent molecular markers. Molecular data have proven useful in resolving the systematic relationships of a taxonomically difficult group, despite the limited traditional morphology-based classification schemes, although some deeper nodes within the tribe still remain unclear. The genus Scaptia requires significant taxonomic revision as it currently comprises several
Acknowledgments
Authors would like to thank Shelah Morita (Smithsonian Institute, Washington DC, USA) and Brian Cassel (North Carolina State University, Raleigh, USA) for their collaboration, technical involvement and support. We would also like to acknowledge the field and/or laboratory assistance of Kelly Meiklejohn and James Wallman (University of Wollongong, Australia), Tom Everingham and Peter Cranston (Australian National University, Canberra, Australia), Leigh Nelson, Nicole Gunter, Sara Pinzon-Navarro,
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2014, Infection, Genetics and EvolutionCitation Excerpt :Tabanidae are a cosmopolitan Dipteran family comprising about 4400 species belonging to 144 genera (Roskov et al., 2013). The family includes four subfamilies divided into tribes: Chrysopsinae (Bouvieromyiini, Chrysopsini and Rhinomyzini), Pangoniinae (Mycteromyiini, Pangoniini, Philolichini and Scionini), Scepsidinae and Tabaninae (Diachlorini, Haematopini and Tabanini) (Coscarón and Philip, 1979; Lessard et al., 2013; Mackerras, 1954, 1955). Most of the economically important tabanids are in the Chrysopsinae, particularly the genus Chrysops, and the Tabaninae (Mullens, 2002).