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Taxonomy and Phylogeny of the Asphondylia

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Taxonomy and Phylogeny of the Asphondylia Bucknell University From the SelectedWorks of Warren G. Abrahamson, II 2015 Taxonomy and phylogeny of the Asphondylia species (Diptera: Cecidomyiidae) of North American goldenrods: challenging morphology, complex host associations, and cryptic speciation Netta Dorchin, Tel Aviv University Jeffrey B. Joy, Simon Fraser University Lukas K. Hilke, University of Bonn Michael J. Wise, Roanoke College Warren G. Abrahamson, II, Bucknell University Available at: https://works.bepress.com/warren_abrahamson/154/ bs_bs_banner Zoological Journal of the Linnean Society, 2015, 174, 265–304. With 105 figures Taxonomy and phylogeny of the Asphondylia species (Diptera: Cecidomyiidae) of North American goldenrods: challenging morphology, complex host associations, and cryptic speciation NETTA DORCHIN1*, JEFFREY B. JOY2, LUKAS K. HILKE3, MICHAEL J. WISE4 and WARREN G. ABRAHAMSON5 1Department of Zoology, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel 2Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, BC, Canada V5A 1S6 3University of Bonn, Regina-Pacis-Weg 3, D-53113 Bonn, Germany 4Department of Biology, Roanoke College, Salem VA 24153, USA 5Department of Biology, Bucknell University, Lewisburg, PA 17837, USA Received 12 October 2014; revised 29 November 2014; accepted for publication 15 December 2014 Reproductive isolation and speciation in herbivorous insects may be accomplished via shifts between host-plant resources: either plant species or plant organs. The intimate association between gall-inducing insects and their host plants makes them particularly useful models in the study of speciation. North American goldenrods (Asteraceae: Solidago and Euthamia) support a rich fauna of gall-inducing insects. Although several of these insects have been the subject of studies focusing on speciation and tritrophic interactions, others remain unstudied and undescribed. Among the latter are at least seven species of the large, cosmopolitan gall midge genus Asphondylia Loew (Diptera: Cecidomyiidae), the taxonomy and biology of which are elucidated here for the first time using morphological, molecular, and life-history data. We describe Asphondylia pseudorosa sp. nov., Asphondylia rosulata sp. nov., and Asphondylia silva sp. nov., and redescribe Asphondylia monacha Osten Sacken, 1869 and Asphondylia solidaginis Beutenmüller, 1907, using morphological characters of adults, immature stages, and galls, as well as sequence data from both nuclear and mitochondrial genes. A neotype is designated for A. solidaginis, the type series of which is considered lost. We also provide information on the life history of all species, including a description of two inquilinous cecidomyiids commonly found in the galls, Clinodiplosis comitis sp. nov. and Youngomyia podophyllae (Felt, 1907), and on parasitoid wasps associated with the gall midges. Asphondylia johnsoni Felt, 1908, which was described from an unknown gall on an unknown Solidago host, is assigned to nomina dubia. Our phylogenetic analyses show that some of the Asphondylia species associated with goldenrods induce two different types of galls during their life cycle, some exhibit host alterations, and some do both. In the absence of reliable morphological differences, recognising species boundaries and deciphering host associations of species must rely heavily on mo- lecular data. Our analysis suggests that radiation in this group has been recent and occurred through shifts among host plants. © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 265–304. doi: 10.1111/zoj.12234 ADDITIONAL KEYWORDS: cryptic speciation – gall midges – host association – inquilines – Solidago. *Corresponding author. E-mail: [email protected] © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 265–304 265 266 N. DORCHIN ET AL. INTRODUCTION 2008; Adair et al., 2009), this has been demonstrated only in the genus Asteromyia Felt, 1910 (Heath & Phytophagous insects are well-known models for study- Stireman, 2010; Janson et al., 2010). In general, gall ing diversification and speciation (Futuyma & Agrawal, midge genera with such known associations with fungi 2009; Nosil, 2012). The evolution of host associations have a broader host range and are more diverse than among phytophagous insects has been shown to be gall midge genera that do not exhibit fungal associa- caused by both spatial and temporal shifts between tions, suggesting that the fungus is important in me- host-plant species and within host-plant species (to dif- diating relationships with the host plant (Joy, 2013). ferent plant organs or different time periods of plant The hypothesis that females actively collect conidia in growth; Joy & Crespi, 2012); however, the relative im- specialized structures on their ovipositors (Borkent & portance and the context of between- versus within- Bisset, 1985; Rohfritsch, 1997, 2008) remains untest- host shifts remains unknown. Gall midges (Diptera: ed, and the mechanistic role of the fungus in Cecidomyiidae) are excellent models for studying the Asphondylia galls is still unknown. importance and context of such shifts because of the The life histories of Asphondylia species vary con- intimate nature of their relationships with their host siderably, depending largely on zoogeographical region plants, and because closely related groups of gall midges and host-plant phenology (Yukawa, 1987; Uechi & are known to diversify through shifts between hosts Yukawa, 2006a, b; Tokuda, 2012). Many species are and through shifts between organs within a host- univoltine and enter extended diapause, whereas others plant species (e.g. Jones, Gagné & Barr, 1983; Hawkins, are bi- or multivoltine and present complex host as- Goeden & Gagné, 1986; Joy & Crespi, 2007; Stireman, sociations (reviewed in Tokuda, 2012). The great ma- Devlin & Abbot, 2012). jority of gall-inducing cecidomyiids are considered Asphondylia Loew, 1850 belongs to the tribe monophagous or narrowly oligophagous, but system- Asphondyliini, currently with 505 species, and within atic and molecular studies have revealed some Asphondyliini to the subtribe Asphondyliina, which is Asphondylia species to be polyphagous, as they develop most diverse in the Neotropics (Gagné & Jaschhof, on several host plants from two or more unrelated plant 2014). The subtribe contains 19 genera that share clear families. Documented examples of polyphagous species morphological apomorphies, but no cladistic or other include Asphondylia gennadii Marchal, 1904 (Gagné phylogenetic analysis has been conducted on it to date. & Orphanides, 1992), Asphondylia yushimai Yukawa All genera included in this group other than Asphondylia & Uechi, 2003 (Yukawa et al., 2003), and Asphondylia are small (with between one and 11 species), and most websteri Felt, 1917 (Gagné & Jaschhof, 2014). Some are restricted to South America. By contrast, of these species are multivoltine and alternate between Asphondylia is one of the largest genera in the family hosts that are available at different times of the year Cecidomyiidae, with 320 described species that feed (Tokuda, 2012), whereas others alternate between dif- on a great diversity of plant families worldwide (Gagné ferent organs on the same host plant (Parnell, 1964; & Jaschhof, 2014), and the number of undescribed Plakidas, 1988). On the other end of the scale are groups species in this genus is probably far greater. Despite of strictly monophagous species that are plant-organ descriptions of numerous new Asphondylia species in specific and have apparently radiated, or are in the recent years from South America and Australia process of radiating, in situ on a single plant genus (Veenstra-Quah, Milne & Kolesik, 2007; Kolesik & (Hawkins et al., 1986; Gagné & Waring, 1990; Joy & Veenstra-Quah, 2008; Maia et al., 2008; Maia, Santos Crespi, 2007; Stokes et al., 2012). & Fernandes, 2009; Kolesik, Adair & Eick, 2010), knowl- Asphondylia taxonomy is challenging because adult edge about the fauna of the southern hemisphere is morphology differs little among species. All species share greatly lacking, in particular that of the Afrotropical the neckless, cylindrical antennal flagellomeres in both region, and there is little doubt that it includes hun- sexes, the needle-like ovipositor and conspicuously en- dreds of undescribed species (ND, unpublished data). larged seventh sternite in the female, and the compact The North American fauna of plant-feeding gall midges male genitalia with the spherical gonostyli posi- is relatively well known (Gagné, 1989), but undescribed tioned dorsally rather than apically (Gagné, 1994). The species are still continuously discovered, and many of third-instar larvae possess a well-developed, usually these belong to Asphondylia. four-toothed spatula on the first thoracic segment. All Asphondylia species are gall inducers, and the Because pupation in all Asphondylia species takes place galls are almost always associated with a fungus that inside the gall rather than in the soil, the larvae do lines the inside walls of the gall. Similar associations not need the spatula for digging; thus the function of are known in other cecidomyiid genera, and al- the spatula in this genus is unknown. The pupae are though several studies suggested that the larvae of such characterized by well-developed horn-like antennal bases, ‘ambrosia’ gall midges feed on the fungus rather than a varying number of facial horns,
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