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Insecta: Neuropterida: Neuroptera) Based on X-Ray Microct Imaging

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Insecta: Neuropterida: Neuroptera) Based on X-Ray Microct Imaging Arthropod Structure & Development 57 (2020) 100951 Contents lists available at ScienceDirect Arthropod Structure & Development journal homepage: www.elsevier.com/locate/asd First description of male genital sclerites and associated musculature for two members of Coniopterygidae (Insecta: Neuropterida: Neuroptera) based on X-ray microCT imaging * Stephan Handschuh a, Ulrike Aspock€ b, c, a VetCore Facility for Research, Imaging Unit, University of Veterinary Medicine Vienna, Veterinaerplatz 1, A-1210, Vienna, Austria b Natural History Museum, 2nd Zoological Department, Burgring 7, A-1010, Vienna, Austria c Department of Evolutionary Biology, University of Vienna, Althanstraße 14, A-1090, Vienna, Austria article info abstract Article history: Coniopterygidae are the dwarfs among the Neuroptera. Despite their miniaturisation, the males are Received 12 September 2019 equipped with genital sclerites that are excessively heterogeneous. They function in copulation and Received in revised form sperm transfer and have been widely utilized for species identification, as well being considered of high 24 April 2020 phylogenetic relevance. The present study is the first to describe the musculature associated with the Accepted 24 April 2020 genital sclerites of two species of Coniopterygidae, Helicoconis lutea (Wallengren, 1871) (Aleuropter- Available online xxx yginae), and Coniopteryx pygmaea (Enderlein, 1906) (Coniopteryginae) based on X-ray microCT imaging. We found six pairs of muscles associated with the genital sclerites in H. lutea and seven in C. pygmaea. Keywords: Gonocoxite hypothesis The images depict other internal organs of the posterior abdominal segments, such as gonads and Terminalia alimentary canal. In both investigated species, the internal sclerites support the ductus ejaculatorius, Homologisation which e surprisingly e turned out to be a landmark for the identification of closely adjacent internal Copulation sclerites and associated musculature. The interpretation of these sclerites as gonocoxites and gona- Helicoconis pophyses of the tenth segment (traditionally denoted as parameres and penis) could be corroborated. Coniopteryx Thus it is no longer tenable to assert that possession of a “penis” is exclusive to Coniopterygidae, since this sclerite is part of the ground pattern in Neuroptera. Interactions of genital sclerites and corre- sponding musculature during copulation are discussed. © 2020 Elsevier Ltd. All rights reserved. 1. Introduction forewing length between 1.2 and 6 mm and by being equipped with diverse morphological characters that are not yet functionally un- The Coniopterygidae Burmeister, 1839, (Insecta: Neuropterida: derstood. Secondly, due to several disagreements between Neuroptera) include approximately 580 known species assigned to morphological and molecular analyses, their systematic position three subfamilies: Brucheiserinae Navas, 1927, with only four within Neuroptera is still unresolved. known species restricted to South America, and the species-rich Coniopterygidae are equipped with excessively heterogeneous subfamilies Coniopteryginae Burmeister, 1839, with 201 known male genital sclerites which function during copulation and sperm species and Aleuropteryginae Enderlein, 1905, with 370 known transfer. They have been widely utilized for species identification species, which are distributed worldwide (Meinander, 1972, 1990; (Tjeder, 1957; Meinander, 1972; Sziraki, 2011; Martins and Sziraki, 2007, 2011; Martins and Amorim, 2016; Oswald, 2017; Amorim, 2016) and are of high phylogenetic relevance Oswald and Machado, 2018). Coniopterygidae have been a matter (Meinander, 1972, U. Aspock€ and H. Aspock,€ 2008). The first of permanent interest for two reasons: Firstly, as the dwarfs among “portraits” of genital sclerites of Coniopterygidae were published Neuroptera and Neuropterida they remain enigmatic with a in the early twentieth century by Enderlein (1906).Almostfifty years later, Tjeder (1954) created a general terminology for genital sclerites of Neuropterida, which still serves as a reference for many * Corresponding author. Natural History Museum, 2nd Zoological Department, neuropterologists (Meinander, 1972; Sziraki, 2011; Martins and Burgring 7, A-1010, Vienna, Austria. Amorim, 2016). Tjeders terminology for Coniopterygidae E-mail addresses: [email protected] (S. Handschuh), ulrike. included, among other characters, a pair of external sclerites [email protected], [email protected] (U. Aspock).€ https://doi.org/10.1016/j.asd.2020.100951 1467-8039/© 2020 Elsevier Ltd. All rights reserved. 2 S. Handschuh, U. Aspock€ / Arthropod Structure & Development 57 (2020) 100951 (gonarcus), two pairs of internal sclerites (penis, parameres) and a segmental muscles, the alimentary canal, and the reproductive prominent external hypandrium. organs), may provide new insights in order to either corroborate or More recently, male genital sclerites in Neuropterida have been falsify current homology assumptions with respect to genital studied and interpreted in the context of an extended gonocoxite sclerites. Specific questions include: (i) Does musculature support hypothesis (U. Aspock€ and H. Aspock,€ 2008, Liu et al., 2016,U. the interpretation of the external genital sclerites as appendages of Aspock,€ 2019). Although not the first to do so, Matsuda (1957) segment nine? Furthermore, can the musculature of the external argued that abdominal segments eight, nine, and ten of female sclerites be homologised with muscles of other Hexapoda? (ii) Can Archaeognathan Machilidae are equipped with serially homolo- the musculature of the two pairs of internal sclerites be homolo- gous gonocoxites, gonostyli and gonapophyses. Lawrence et al. gised with muscles of other Hexapoda? If yes, does musculature (1991) extended the gonocoxite hypothesis of Matsuda to the corroborate interpretation of these sclerites as tenth segmental genital appendages of female Holometabola. U. Aspock€ and H. appendages, and does the muscle homologisation allow a homo- Aspock€ (2008) adopted the gonocoxite hypothesis to Neuro- logisation of the internal genital sclerites of Coniopterygidae to pterida, involving also male genital appendages by using the male sclerites of other Hexapoda? (iii) Do the presented data allow for a terminalia of Raphidioptera as key link. In this extended gonocoxite sound interpretation of the identity of the external hypandrium of hypothesis, they included also sclerites of abdominal segment 11. Coniopterygidae? (iv) Do the presented data allow for any new clue The extended gonocoxite hypothesis assumes that each of the male on specific and unique configurations and modifications of the genital sclerites of Coniopterygidae can be homologized with either genital sclerites found in the two investigated genera? (3) To gonocoxites, gonostyli or gonapophyses of the abdominal segments explore the informational value of genital sclerite associated mus- nine, ten or eleven. Within the extended gonocoxite hypothesis, cles for phylogenetic evidence. sclerites of Neuroptera have been homologised according to their position and structure. In the Coniopterygidae, several sclerites 2. Material and methods show large positional and structural similarities with other neu- ropterans providing reasonable support for homology assumptions 2.1. Animals (U. Aspock€ and H. Aspock,€ 2008). These include a prominent pair of external sclerites (gonarcus sensu Tjeder (1957)), which has been For this study we used one male specimen of H. lutea interpreted as derived appendages of the ninth abdominal segment (Wallengren, 1871) (Aleuropteryginae Enderlein, 1905) from sam- (gonocoxites, or potentially fused gonocoxites þ gonostyli). Also, pling locality Allershausen, Bavaria, Germany, N48,42541 two pairs of internal sclerites are present in Coniopterygidae E11,61307, July 2017, leg. Axel Gruppe, and one male specimen of (parameres and penis sensu Tjeder (1957)), which have been C. pygmaea Enderlein (1906) (Coniopteryginae Burmeister, 1839), interpreted as genital sclerites of abdominal segment ten (U. from sampling locality Windischhütte near Klosterneuburg, Lower Aspock€ and H. Aspock,€ 2008). The wealth of data on con- Austria, N48,1719,9 E16,1620,5, May 2013, leg. Ulrike Aspock.€ iopterygid genitalia (Meinander, 1972, 1990) provides good support for homology assumptions for these three pairs of sclerites. 2.2. Sample preparation and microCT imaging Furthermore, their descent from segment nine and ten appendages receives reasonable support from comparison to other Neuro- One male of H. lutea and one male of C. pygmaea were fixed and pterida, and Hexapoda/Endopterygota in general (U. Aspock€ and H. stored in 70% ethanol. Prior to microCT imaging, they were dehy- Aspock,€ 2008). However, the exact identity of single sclerites drated with absolute ethanol and stained for 24h in 1% (w/v) (referring to the interpretation as gonocoxites, gonostyli, gona- elemental iodine in absolute ethanol (Metscher, 2009). After pophyses), the potential presence of amalgamated composite staining, specimens were washed in absolute ethanol and vertically sclerites (e.g., gonocoxite þ gonostylus), the identity of the external mounted in polypropylene pipette tips in absolute ethanol. hypandrium, as well as the presence of genital sclerites of segment Specimens were scanned using an XRadia MicroXCT-400 (Carl 11 are so far still largely subject to interpretation and hypothetical, Zeiss X-ray Microscopy, Pleasanton, CA, USA). Overview scans
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