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Mecoptera: Panorpidae) with Phylogenetic Considerations 373-386 75 (3): 373 – 386 20.12.2017

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Mecoptera: Panorpidae) with Phylogenetic Considerations 373-386 75 (3): 373 – 386 20.12.2017 ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Arthropod Systematics and Phylogeny Jahr/Year: 2017 Band/Volume: 75 Autor(en)/Author(s): Zhang Bei-Bei, Hua Bao-Zhen Artikel/Article: Spermatogenesis and sperm structure of Neopanorpa lui and Neopanorpa lipingensis (Mecoptera: Panorpidae) with phylogenetic considerations 373-386 75 (3): 373 – 386 20.12.2017 © Senckenberg Gesellschaft für Naturforschung, 2017. Spermatogenesis and sperm structure of Neopanorpa lui and Neopanorpa lipingensis (Mecoptera: Panorpidae) with phylogenetic considerations Bei-Bei Zhang 1, 2 & Bao-Zhen Hua*, 1 1 State Key Laboratory of Crop Stress Biology for Arid Areas, Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, China — 2 Institute of Tropical Agriculture and Forestry, Hainan University, Danzhou, Hainan 571737, China; Bao-Zhen Hua* [[email protected]]; Bei-Bei Zhang [zhangbeibei@nwafu. edu.cn] — *Corresponding author. Accepted 21.vi.2017. Published online at www.senckenberg.de/arthropod-systematics on 11.xii.2017. Editors in charge: Ulrike Aspöck & Klaus-Dieter Klass Abstract Spermatogenesis and sperm ultrastructure were investigated in Neopanorpa lui Chou & Ran and Neopanorpa lipingensis Cai & Hua by light and transmission electron microscopy. Two lateral lamellae run along the lateral grooves of the spermatid nucleus during spermiogen- esis, but disappear in the mature spermatozoa. Sperm cells are very similar in ultrastructure between the two species. The spermatozoa are elongated cells, each comprising an apical bilayered acrosome inserted on the anterior nuclear region, an elongate nucleus that occupies the anterior sperm region, a neck region, and a posterior long flagellum. The nucleus has two prominent lateral grooves and assumes a helical appearance. The flagellum is helical and consists of a 9 + 2 axoneme, two mitochondrial derivatives of unequal size, one accessory body, and two extra-axonemal accessory structures. The uniqueness of spermatozoa of Neopanorpa lies in the specifically spoon-shaped larger mitochondrial derivative along most of the flagellum length. A tentative phylogenetic analysis based on sperm structure supports a possible monophyletic clade comprising Panorpidae, Panorpodidae, Bittacidae, and Boreidae of Mecoptera with two non-homoplasious characters: glycocalyx organised in longitudinal ridges and two extra-axonemal accessory structures/rods in flagellum. Closer affinities of Siphonaptera and the mecopteran clade are suggested by the characters of two asymmetric mitochondrial derivatives and the presence of mitochondrial derivative with crystalline structure. The sister group relationship of Panorpidae with Panorpodidae is supported by the presence of nuclear fiber and the irregular shape of the larger mitochondrial derivative. Key words Insecta, mitochondrial derivative, Neopanorpa, phylogeny, spermatozoa, spermiogenesis. 1. Introduction Mecoptera, a minor order in Antliophora of holometa- Diptera, however, has not been satisfactorily clarified in bolous insects, is unique in Holometabola because most Antliophora (WILLMANN 1987; WHITING 2002; BEUTEL & mecopteran groups (especially Panorpidae, Nannocho- BAUM 2008; WIEGMANN et al. 2009; BEUTEL et al. 2011; ri sti dae, Choristidae, and Bittacidae) possess a pair of FRIEDRICH et al. 2013; MISOF et al. 2014). WHITING (2002) prominent compound eyes in their larval stages (BYERS assumed that Mecoptera (Boreidae) is paraphyletic with & THORNHILL 1983; MELZER et al. 1994; KRISTENSEN 1999; respect to Siphonaptera based on molecular data. BEUTEL CHEN et al. 2012). Its relationship with Siphonaptera and & BAUM (2008) considered the peculiar family Nanno- ISSN 1863-7221 (print) | eISSN 1864-8312 (online) 373 Zhang & Hua: Sperm of Neopanorpa choristidae of Mecoptera as the sister group of Diptera 2. Material and methods supported by the mouthpart structure of adults. FRIEDRICH et al. (2013) also proposed that Mecoptera is a paraphy- letic group based on morphological characters of the 2.1. Insect collection adult head. However, some researchers (WILLMANN 1987; WIEGMANN et al. 2009; MISOF et al. 2014) argued that Adult males of Neopanorpa lui Chou & Ran, 1981 were Mecoptera is monophyletic as the sister group of Siphon- obtained from the Tiantaishan National Forest Park aptera. BEUTEL et al. (2011) even regarded Mecoptera (34°13′N 106°59′E, elev. 1500 – 1600 m) in the Qinling as the sister group of Diptera and Siphonaptera based Mountains, Shaanxi Province from late June to early on morphological data. Additional characters are obvi- July in 2014 and mid-July in 2015. Adult males of Neo­ ously needed to solve the phylogenetic position problem panorpa lipingensis Cai & Hua, 2009 were collected at of Mecoptera. The ultrastructure of spermatozoa might Huanglongtan (31°53′N 109°31′E, elev. 900 – 1000 m) in partly fulfill this requirement. the Hualong Mountains, Shaanxi Province in mid-July Spermatozoa are highly specialized cells, character- 2015. ized by patterns of rapid and divergent morphological evolution (BIRKHEAD et al. 2009; DALLAI et al. 2016; GOTTARDO et al. 2016). The variation in sperm morpho- 2.2. Light microscopy logy, especially the ultrastructure, can provide valuable characters for the assessment of evolution and the recon- Live adult males were anaesthetized with diethyl ether, struction of phylogeny in various groups (JAMIESON 1987; and their testes and epididymids were rapidly dissected JAMIESON et al. 1999; DALLAI 2009, 2014; DALLAI et al. in Ringer’s solution under a Nikon SMZ1500 stereo 2016; GOTTARDO et al. 2016). The ultrastructure of sper- microscope (Nikon, Tokyo, Japan). The testicular folli- matozoa has been extensively studied in the vast num- cles were opened at the basal part and the sperm bun- ber of species of insects (BAccETTI 1972; JAMIESON 1987; dles were spread onto clean microslides. Pictures were JAMIESON et al. 1999; DALLAI 2014; DALLAI et al. 2016). taken with a QImaging Retiga 2000R Fast 1394 Digital However, sperm structure is still poorly documented CCD equipped on the microscope. To determine the size in Mecoptera to date, and only four species have been of sperm nucleus, some slides were stained with 4,6-di- investigated in Panorpidae (GASSNER et al. 1972; JAMIE- amino-2-phenylindole (DAPI, Beyotime) for 5 min, and SON et al. 1999; DALLAI et al. 2003; ZHANG et al. 2016); washed in distilled water. Photographs were taken with a two species in Bittacidae (SHEPARDSON et al. 2014); two Nikon DS-Ril digital camera attached to a Nikon Eclipse species in Boreidae (DALLAI et al. 2003; RUSSELL et al. 80i epifluorescence microscope (Nikon, Tokyo, Japan). 2013); and one species in Panorpodidae (ZHANG & HUA For histological observation, the samples embedded 2014). in polymerized Epon 812 resin were cut into semi-thin Panorpidae, the largest family of Mecoptera, com- sections with a Leica EM UC7 ultramicrotome (Leica, prises approximately 400 extant species, which are dis- Nussloch, Germany), stained with 0.5% toluidine blue, tributed throughout Asia, North America, and Europe and examined under the microscope. (KALTENBACH 1978; PENNY & BYERS 1979; BYERS & THORNHILL 1983; HU et al. 2015). The species of Pan- orpidae are currently assigned to seven genera: Panorpa 2.3. Transmission electron microscopy Linnaeus, 1758; Leptopanorpa MacLachlan, 1875; Neo­ panorpa Weele, 1909; Sinopanorpa Cai & Hua, 2008; The testes and epididymides of live male adults were dis- Furcatopanorpa Ma & Hua, 2011; Dicerapanorpa Zhong sected rapidly in Ringer’s solution and fixed at 4°C over- & Hua, 2013; and Cerapanorpa Gao, Ma & Hua, 2016. night in a mixture of 2% paraformaldehyde and 2.5% Previous sperm structure studies of Panorpidae (GASSNER glutaraldehyde in 0.1 M phosphate buffer (PB, pH 7.2), et al. 1972; JAMIESON et al. 1999; DALLAI et al. 2003; in which 3% sucrose was added. ZHANG et al. 2016) only dealt with species of Panorpa The fixed samples were rinsed six times with PB, and and Furcatopanorpa, the sperm ultrastructures of which post-fixed in phosphate-buffered 1% osmium tetroxide are distinctly different in the mitochondrial derivative of (OSO4) for 1.5 h at 4°C. After rinsing six times with PB, flagellum, whereas the second largest genusNeopanorpa the testicular follicle and epididymis samples were dehy- has not been involved. drated in a graded series of acetone (30%, 50%, 70% for In this study, we investigated the spermatogenesis 10 min each, 80% for 15 min, 90% for 20 min, and 100% and sperm ultrastructure of Neopanorpa lui Chou & Ran, for 30 min twice), infiltrated successively with three mix- 1981 and Neopanorpa lipingensis Cai & Hua, 2009 by tures of acetone/Epon 812 resin (3:1 for 2 h, 1:1 for 4 h, light and transmission electron microscopy, in order to and 1:3 for 12 h) and pure Epon 812 resin for 24 h twice provide eventual additional characters for future phy- at room temperature, and were embedded in pure Epon logenetic analysis of Panorpidae, and in an attempt to 812 resin, polymerized at 30°C for 24 h and at 60°C 48 h. elucidate the phylogenetic relationships of Mecoptera in Ultra-thin sections were cut with a diamond knife on Antliophora. the ultramicrotome, double stained with uranyl acetate and lead citrate for 10 and 8 min, respectively, and ex- 374 ARTHROPOD SYSTEMATICS & PHYLOGENY — 75 (3) 2017 Fig. 1. Neopanorpa lui Chou
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