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Cephalic Anatomy of Zorotypus Weidneri New, 1978: New Evidence for a Placement of Zoraptera

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Cephalic Anatomy of Zorotypus Weidneri New, 1978: New Evidence for a Placement of Zoraptera 73 (1): 85 – 105 29.4.2015 © Senckenberg Gesellschaft für Naturforschung, 2015. Cephalic anatomy of Zorotypus weidneri New, 1978: new evidence for a placement of Zoraptera Yoko Matsumura 1, 2, †, Benjamin Wipfler 1, †, Hans Pohl 1, Romano Dallai 3, Ryuichiro Machida 4, Yuta Mashimo 4, Josenir T. Câmara 5, José A. Rafael 5 & Rolf G. Beutel *, 1 1 Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, Erbertstraße 1, 07743 Jena, Germany; Yoko Matsumura [[email protected]]; Benjamin Wipfler [[email protected]]; Hans Pohl [[email protected]]; Rolf G. Beutel [[email protected]] — 2 Department of Functional Morphology and Biomechanics, Institute of Zoology, Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1 – 9, 24118 Kiel, Germany — 3 Department of Life Sciences, Via A. Moro 2, University of Siena, I-53100 Siena, Italy; Romano Dallai [[email protected]] — 4 Sugadaira Montane Research Center, University of Tsukuba, Nagano, 386-2204 Japan; Ryuichiro Machida [[email protected]]; Yuta Mashimo [mashimo@suga- daira.tsukuba.ac.jp] — 5 Instituto Nacional de Pesquisas da Amazonia, Caixa Postal 478, 69011-970 Manaus, AM, Brazil; Josenir T. Câmera [[email protected]]; José A. Rafael [[email protected]] — † equally contributed — * Corresponding author Accepted 22.i.2015. Published online at www.senckenberg.de/arthropod-systematics on 17.iv.2015. Abstract External and internal head structures of Zorotypus weidneri were examined, documented with SEM images and photographs, and reconstructed 3-dimensionally. The results are compared with published results on Z. hubbardi and with conditions found in other hemimetabolan lineages, with a main focus on the polyneopteran orders and on Psocoptera and Thysanoptera representing Acercaria. Externally the head of both zorapteran species is very similar but they differ in some internal features such as the presence (Z. hubbardi) or absence (Z. weidneri) of an ampullo-aortic muscle of the antennal heart and a well-developed cervical gland. Cephalic characters are analysed phylogenetically addressing the controversial issue of the placement of Zoraptera. A position within monophyletic Polyneoptera is confirmed, but weakly supported. The analysis yielded a sister group relationship between Zoraptera and Plecoptera but also with a low support value. The placement of Zoraptera with morphological data is impeded by many preserved plesiomorphies such as the orthognathous head orientation, the complete tentorium, the free labrum or the largely unmodified orthopteroid mouthparts in the winged morphs, and also by modifications apparently caused by miniaturization. Similarly, anomalies in the genome cause problems in the assessment of the phylogenetic affinities of the group. Key words Zoraptera, groundlice, head, morphology, phylogeny, Polyneoptera, Acercaria. 1. Introduction Zoraptera or groundlice are a cryptic and controversial means „living in earth, small, apterous, agile and preda- group of small hemimetabolous insects (e.g., GRIMALDI cious insects”. With presently 39 extant and 9 extinct spe- & ENGEL 2005; MASHIMO et al. 2014c). The order was in- cies it belongs to the smallest groups of insects (ENGEL troduced by SILVESTRI (1913) who addressed them as „In- 2003; MASHIMO et al. 2013). The distribution is world- secta terrestria, parva, aptera, agila, praedantia“, which wide, with the exception of the Australian mainland and ISSN 1863-7221 (print) | eISSN 1864-8312 (online) 85 Matsumura et al.: Cephalic anatomy of Zoraptera Antarctica (MASHIMO et al. 2014c). The group is largely the groundplan of the order (e.g., blade-like lacinia). In restricted to tropical and subtropical regions. Zorotypus any case, considering the immense problems of placing hubbardi Caudell, 1918 has expanded its range as far Zoraptera and the unresolved intraordinal relationships north as Indiana, Iowa and Illinois (RIEGEL 1963; HUB- it appeared appropriate to examine other species with an BARD 1990), but this is likely due to transport with woods optimized spectrum of morphological techniques (e.g., (MASHIMO et al. 2014c). FRIEDRICH et al. 2014). The morphological results were in- Selected aspects of the morphology of Zoraptera tegrated in a large data matrix for cephalic characters of were treated in few earlier studies (e.g., CRAMPTON 1920, hemimetabolous insects and analyzed phylogenetically. 1921), but the investigation of the group was neglected for a long time (see e.g., MASHIMO et al. 2014c). Con- sequently, it was addressed as the least known insect order by KRISTENSEN (1995). In the last two decades the 2. Material and methods research on Zoraptera has gained remarkable momen- tum, with studies on the head morphology (BEUTEL & WEIDE 2005; WIPFLER & PASS 2014), thoracic skeleto- 2.1. Specimens muscular system (RASNITSYN 1998; FRIEDRICH & BEUTEL 2008), wing base (YOSHIZAWA 2007, 2011), genital struc- tures of different species (HÜNEFELD 2007; DALLAI et al. We used winged and wingless specimens of Zorotypus 2011, 2012a,b, 2014a,b, 2015; MATSUMURA et al. 2014), weidneri collected at Manaus (Brazil) in June 2002 pre- the egg structure (MASHIMO et al. 2011), the embryonic served in 70 % ethanol mainly for studying external struc- (MASHIMO et al. 2014a) and postembryonic development tures. Additional exemplars collected at the same locality (MASHIMO et al. 2014b), and the mating behavior (CHOE in 2014 were fixed in 2.5% glutaraldehyde in phosphate 1994, 1995, 1997; DALLAI et al. 2013). The controversial buffer to which 3% of sucrose was added. The specimens systematic placement of Zoraptera was addressed using were kept in this mixture in a refrigerator for one week. morphological characters (e.g., RASNITSYN 1998; BEUTEL After this they were gradually dehydrated and preserved & GORB 2001, 2006; BEUTEL & WEIDE 2005; YOSHIZAWA in 70% ethanol for detailed anatomical investigations. All 2007) and molecular data sets (YOSHIZAWA & JOHN- voucher specimens were deposited in the Phyletischem SON 2005: 18S rRNA; LETSCH & SIMON 2013; MISOF et Museum of the Friedrich-Schiller-Universität Jena. al. 2014: transcriptomes). Nevertheless, the “Zoraptera problem” (BEUTEL & WEIDE 2005) is far from being set- tled. The sister group relationship between Zoraptera and 2.2. Anatomy Acercaria (Paraneoptera concept) suggested by HENNIG (1969) and others (e.g., BEUTEL & WEIDE 2005; WILL- MANN 2005) has gained little support in recent studies, We used histological sectioning, scanning electron mi- which favor a placement among polyneopteran lineages croscopy (SEM) and confocal laser scanning microscopy (e.g., MINET & BOURGOIN 1986; ENGEL & GRIMALDI 2000; (CLSM). Transverse semithin sections were made of the GRIMALDI 2001; WHEELER et al. 2001; YOSHIZAWA 2007; anterior body region of winged and wingless exemplars. MASHIMO et al. 2014a; MISOF et al. 2014; WIPFLER & PASS The samples were embedded in araldite CY 212® (Agar 2014; see also TRAUTWEIN et al. 2012 and MASHIMO et al. ScientiWc, Stansted/Essex, England) and cut at 1 µm us- 2014c). However, the precise position within Polyneo- ing a microtome HM 360 (Microm, Walldorf, Germany) ptera, which may or may not be monophyletic (e.g., KRIS- equipped with a diamond knife. Sections were stained TENSEN, 1995; KLASS 2009; WIPFLER et al. 2011; LETSCH with toluidine blue and pyronin G (Waldeck GmbH and & SIMON 2013; BEUTEL et al. 2014b) (see MASHIMO et al. Co.KG/Division Chroma, Münster, Germany). Succes- 2014c), remains unclear. sive pictures were taken of every second section using The present study has its focus on cephalic structures, a light microscope (Zeiss Axioplan, Germany) equipped a complex character system which has turned out as phylo- with a camera (PixeLink Capture OEM) (wingless speci- genetically informative in many studies (e.g., BEUTEL et al. men: 360 pictures; winged specimen: 341 pictures). The 2011; WIPFLER et al. 2011). The skeletomuscular system of images were aligned using Amira 5.3.1 software (Visage the thorax of winged morphs is almost exclusively char- Imaging, Berlin, Germany). Based on the aligned image acterized by plesiomorphic features (FRIEDRICH & BEUTEL stacks we evaluated the arrangement of internal structures 2008) and the reproductive characters such as male geni- and manually traced each element to reconstruct three-di- talia, spermatogenesis, and spermatozoa are highly vari- mensional images for the winged specimen. For smooth- able among species even within the very small order (e.g., ing, coloring, illumination, and taking pictures we used GURNEY 1938; DALLAI et al. 2011, 2012a,b, 2014a,b). The MAYA 7 (Alias Wavefront, Toronto/Ontario, Canada). head morphology of Zorotypus hubbardi was already de- Scanning electron microscopy (SEM, Philips XL 30 scribed (BEUTEL & WEIDE 2005). However, it turned out ESEM) was used to observe cephalic surface structures. that some structures have been overlooked or misinter- We gradually dehydrated specimens preserved in 70% preted (e.g., WIPFLER & PASS 2014: antennal hearts) and ethanol with an ethanol-acetone series and dried them at that some features are apparently not conformed with the critical point (Emitech K850 critical point dryer). To 86 ARTHROPOD SYSTEMATICS & PHYLOGENY — 73 (1) 2015 Table 1. Taxon sampling for the cladistic analysis and source of the morphological information. Taxon Species Literature source Ephemeroptera Siphlonurus lacustris (Eaton, 1870) Blanke et al. 2012 Plecoptera
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