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The Tachinid Sexual Patches (Diptera: Oestroidea: Tachinidae) Pierfilippo Cerretti,1,2 Andrea Di Giulio,3 Roberto Romani,4 Diego J

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The Tachinid Sexual Patches (Diptera: Oestroidea: Tachinidae) Pierfilippo Cerretti,1,2 Andrea Di Giulio,3 Roberto Romani,4 Diego J Acta Zoologica (Stockholm) doi: 10.1111/azo.12085 First report of exocrine epithelial glands in oestroid flies: the tachinid sexual patches (Diptera: Oestroidea: Tachinidae) Pierfilippo Cerretti,1,2 Andrea Di Giulio,3 Roberto Romani,4 Diego J. Inclan,1 Daniel Whitmore,5 Filippo Di Giovanni,2 Massimiliano Scalici3 and Alessandro Minelli6 Abstract 1DAFNAE-Entomologia, Universitadegli Cerretti, P., Di Giulio, A., Romani, R., Inclan, D.J., Whitmore, D., Di Giovanni, F., StudidiPadova,Vialedell’Universita16, Scalici, M. and Minelli, A. 2014. First report of exocrine epithelial glands in oestroid 2 Legnaro, I 35020, Italy; Dipartimento di flies: The tachinid sexual patches (Diptera: Oestroidea: Tachinidae). —Acta Zoolog- Biologia e Biotecnologie ‘Charles Darwin’, ica (Stockholm) 00:000–000. ‘Sapienza’ Universita di Roma, Piazzale A. Moro 5, Rome, I 00185, Italy; 3Diparti- Sexual patches are abdominal areas identifiable by modified setation, present in mento di Scienze, UniversitadegliStudi the males of several groups of Tachinidae (Diptera). We comparatively studied ‘Roma Tre’, Viale G. Marconi 446, Rome, 4 more than 40 species belonging to 24 genera representative of subfamilies known I 00146, Italy; Dipartimento di Scienze to bear these organs, using light microscopy and scanning (SEM) and transmis- Agrarie Alimentari e Ambientali, Universita degli Studi di Perugia, Borgo XX Giugno sion (TEM) electron microscopy. We provide a detailed characterization of the 74, Perugia, I 06121, Italy; 5Department fine structure of the setae and microtrichia composing these sexual patches and of Life Sciences, Natural History Museum, of the underlying epithelium. Study of abdominal sections showed that, close to Cromwell Road, London, SW7 5BD, the patch area, the epidermis forms a thick layer composed of numerous secre- UK; 6Dipartimento di Biologia, Universita tory units of strictly associated cells, ending at the level of cuticular pores at the degli Studi di Padova, Via Ugo Bassi 58B, base of the setae. We hypothesize a secretory function of these structures. The Padova, I 35131, Italy segmental pattern of the sexual patches across the Tachinidae is defined and predictable. We note that almost all the segmental patterns share the presence of Keywords: sexual patches on abdominal tergite 4, underscoring the diversity of male sexual cuticle, Diptera, Tachinidae, epithelial specializations that occur on the fourth abdominal segment of muscomorph flies. glands,evolution,finemorphology,sexual dimorphism, ultrastructure Pierfilippo Cerretti, DAFNAE-Entomologia, Universita degli Studi di Padova, Viale dell’Universita 16, Legnaro, I 35020, Italy. E-mail: pierfilippocerretti@ Accepted for publication: 05 May 2014 yahoo.it oristinae but retrieves only the Exoristinae and the Phasiinae Introduction as monophyletic (Cerretti et al. 2014). The family Tachinidae is one of the most diverse groups of Across all four subfamilies, with few exceptions, adult Diptera and represents the largest group of non-hymenop- tachinids are extremely ‘bristly’.Shape,sizeandarrangement teran parasitoids (Stireman et al. 2006). With nearly 8,500 of setae (chaetotaxy) have been widely used in the past by spe- valid species currently classified in ~1500 genera (cf., O’Hara cialists for the classification of the group and are still used for 2013; and references therein), tachinids are a morphologically identification to genus and species level. However, possible highly diverse group, well represented in a wide variety of hab- additional functions of these setae, other than that of itats in all biogeographical regions (Crosskey 1973, 1976, mechanoreceptors, are still largely unknown. In this study, we 1984; Wood 1987; Tschorsnig and Richter 1998; Cerretti focus on the specialized patches consisting of dense aggrega- 2010; Wood and Zumbado 2010). The family is currently tions of setae on abdominal tergites 3–5, present exclusively in divided into four subfamilies: Phasiinae, Dexiinae, Exoristinae males of certain species in the Phasiinae, the Tachininae and, and Tachininae (Herting 1984; Wood 1987; Herting and more commonly, the Exoristinae. These structures have been Dely-Draskovits 1993; O’Hara and Wood 2004; Cerretti frequently used by taxonomistsasdiagnosticcharactersand 2010), but this arrangement, although widely accepted, still have been referred to in the taxonomic literature as patches needs refinements. A recent cladistic analysis carried out on a (Villeneuve, 1916), sexual patches (Curran 1927), hair fascicles large dataset of morphological characters supports the sub- (Crosskey 1973, 1976), patches of dense appressed hairs, sex family groupings Dexiinae + Phasiinae and Tachininae + Ex- patches (Wood 1985), Sturmia-Flecken (Tschorsnig and Hert- © 2014 The Royal Swedish Academy of Sciences 1 The tachinid sexual patches Cerretti et al. Acta Zoologica (Stockholm) 0: 1–15 (May 2014) ing 1994) and patches of appressed black hair (sex patches) TM1000 at CNBF (Centro Nazionale BiodiversitaFore- (Wood and Zumbado 2010). We give priority to Curran’s stale), Italian State Forestry Service, Verona, Italy. term, using ‘sexual patches’. Similar abdominal patches of Histological analyses were made on serial sections of the setae are found in the males of several species of Pterella Robi- abdomen. The abdomen, quickly removed from fresh speci- neau-Desvoidy (Sarcophagidae: Miltogramminae). For exam- mens and fixed with Bouin’s solution, was dehydrated in a ple, in P. melanura (Meigen), dense patches of short setae graded ethanol series and finally embedded in paraffin. Using extend from most of the lateroventral surface of tergite 4 to a rotary microtome (Zeiss HM 310, Oberkochen, Germany), almost the entire surface of tergite 5. Venturi (1957) remarked 7–10 lm thick serial sections were obtained and stained with upon the similarity of sexual patches in Pterella with those of Carazzi’s haematoxylin and eosin. Finally, sections were the tachinid Blepharipa pratensis (Meigen). Beyond the recog- observed using a light microscope Eclipse E400 (Nikon, nition of these structures in the taxonomic literature, there is Tokyo, Japan) and photographed with a 5 megapixel digital no conjecture in the literature about their role other than this camera Coolpix 5700 (Nikon, Tokyo, Japan) on multiple being of a sexual nature and their actual function is unknown. focal planes; digital images were then stacked using Combi- For this reason, we conducted the first comparative study on neZM (Hadley 2010). these abdominal sexual patches to explore their morphology For TEM investigations, three live individuals of field- in detail and infer their possible function. collected Blepharipa schineri (Mesnil) were anaesthetized with We provide a detailed characterization of the fine structure CO2 and immediately immersed in a solution of glutaralde- of the setae composing these sexual patches and of the associ- hyde and paraformaldehyde 2.5% in 0.1 M cacodylate ated glandular epithelium, using light microscopy and scan- buffer + 5% sucrose, pH 7.2–7.3. The abdomen was ning (SEM) and transmission (TEM) electron microscopy. removed from the thorax, and the ventrolateral part of the 4th We also discuss possible functional and phylogenetic interpre- abdominal tergite (T4) was isolated to aid fixative penetration, tations of these organs, and analyze their segmental patterning andleftat4°C for 2 h. The specimens were kept at 4 °C from an evo-devo perspective. overnight in 0.1 M cacodylate buffer + 5% sucrose, pH 7.2– 7.3, then postfixed in 1% OsO4 (osmium tetroxide) for 1 h at 4 °C and rinsed in the same buffer. Dehydration in a graded Materials and Methods ethanol series was followed by embedding in Epon–Araldite with propylene oxide as bridging solvent. Thin sections were Specimens taken with a diamond knife on an LKB ‘Nova’ ultramicro- The study was conducted on 130 specimens of more than 40 tome, and mounted on formvar coated 50 mesh grids. Finally, species belonging to 24 genera, representing the nine tribes the sections were investigated with a Philips EM 208 (FEIâ that are known to have sexual patches across three subfamilies Company, Eindhoven, the Netherlands), after staining with oftheTachinidae(Exoristinae,Phasiinae,Tachininae).The uranyl acetate (20 min, room temperature) and lead citrate species examined come from four biogeographical regions: (5 min, room temperature). Digital pictures (1376 9 1032 Afrotropical, Australasian, Nearctic and Palaearctic pixels, 8b, uncompressed greyscale TIFF files) were obtained (Table 1). using a high resolution digital camera MegaViewIII (SISâ, Morphological observations were performed with scan- Olympus, Tokyo, Japan) connected to the TEM. ning electron microscopy (SEM) for non-type material and environmental scanning electron microscopy (ESEM) for type Institutional abbreviations material. For the SEM analyses, abdomens from dry pinned museum specimens (Figs 1–5, 7A–B, 8A–Band9A–B) were CNC, Canadian National Collection of Insects, Agriculture removed from source specimens and mounted on stubs (by and Agri-Food Canada, Ottawa, Canada; MNHN, Museum using self-adhesive carbon discs). The abdomen of Sarromyia National d’Histoire Naturelle, Paris, France; MZUR, nubigena (Fig. 6) was further heated for 1 min in 10% KOH, Museum of Zoology, Sapienza Universita di Roma, Italy; rinsed in 70% ethanol and dissected in glycerol; the abdomen NMNW, National Museum of Namibia, Windhoek, Nami- wasplacedin70%aceticacidandthendehydratedina bia; RMCA, The Royal Museum for Central Africa, Tervu- graded ethanol
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