ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Arthropod Systematics and Phylogeny Jahr/Year: 2018 Band/Volume: 76 Autor(en)/Author(s): Klass Klaus-Dieter, Matushkina Natalia A. Artikel/Article: The exoskeleton of the male genitalic region in Archaeognatha, with hypotheses on the early evolution and the morphological interpretation of genitalia in insects 235-294 76 (2): 235 – 294 18.7.2018 © Senckenberg Gesellschaft für Naturforschung, 2018. The exoskeleton of the male genitalic region in Archaeo- gnatha, with hypotheses on the early evolution and the morphological interpretation of genitalia in insects Klaus-Dieter Klass 1 & Natalia A. Matushkina 2 1 Senckenberg Natural History Collections Dresden, Museum of Zoology, Königsbrücker Landstrasse 159, 01109 Dresden, Germany; Klaus- Dieter Klass [[email protected]] — 2 Department of Ecology and Zoology, Institute of Biology and Medicine, Taras Shevchenko National University of Kyiv, Ukraine; Natalia A. Matushkina [[email protected]] Accepted 16.iii.2018. Published online at www.senckenberg.de/arthropod-systematics on 29.vi.2018. Editor in charge: Frank Wieland Abstract. The ventral exoskeleton of abdominal segments 7 – 9, including the phallic organs (belonging to segment 9 or 10), is described for five archaeognathan species: Machilis hrabei and Lepismachilis notata (Machilidae-Machilinae), Pedetontus unimaculatus (Machili- dae-Petrobiinae), Petrobiellus takunagae (Machilidae-Petrobiellinae), and Machilinus sp. (Meinertellidae). In the focus are the segmental patterns of sclerites and formative elements, and fine structures of the cuticular surface. The results are compared with earlier descriptions of these body parts in Archaeognatha. Hypotheses of homonomy (transsegmental and male-female) and homology at the level of Ectogna- tha (= Insecta) are proposed and insect-wide terminologies applied. Morphological interpretations are revised, if required, with a focus on the segmental assignment and other aspects of the male genital opening and phallic organs. A data matrix of 39 male genitalic characters is composed as a source of information for subsequent phylogenetic and taxonomic work on Archaeognatha. Some discussions on character evolution are given; few apomorphies agree with previous molecular results of a clade Petrobiellinae + Meinertellidae, but phylogenetic conclusions remain limited due to poor data for outgroup comparison (mainly for Zygentoma). We compare and discuss the occurrence of genitalic specialities (= structural differences compared to pregenital segments) on segments 7 – 9 in both sexes. The new data shows that male Archaeognatha exhibit many genitalic specialities on segment 9 and few on segment 8, whereas females show many on segments 9 and 8 and on the posterior part of segment 7; the male specialities are largely a subset of the female ones, except for structures categorised as phallic in the male being largely absent in the female (with possible exceptions). Based mainly on the genitalic specialities common to both sexes, we discuss two discrete scenarios for the early sex-shared evolution of the genitalic region in stem-Insecta: (1) The ‘aquaeductal hypothesis’ proposes that water-uptake from crevices was the initial driving force of structural specialities that today mainly serve for genitalic functions. (2) The ‘sensorial hypothesis’ proposes that improving the sensorial exploration of the substrate was the driving force. Key words. Genitalia, penis, phallic organs, gonapophysis, paramere, morphology, homology, evolution, taxonomy, SEM. 1. Introduction In Insecta (= Archaeognatha + Zygentoma + Pterygota) BIRKET-SMITH 1974; ROHDENDORF & RASNITSYN 1980: the males bear external genitalia, i.e. the phallic organs, p. 22; see Appendix chapter 8 for a preliminary discus- on the ventral side of the posterior part of the abdomen. sion). The phallic organs range from being very simple Together with the genital opening upon or close to them, (e.g. Embio ptera: ROSS 2000) to highly complicated (e.g. the genitalia either belong to abdominal segment 9 or Dictyo ptera: KLASS 1997) in their structure. Complicat- 10, being either derivatives of (parts of) the 9th- or 10th- ed structuring includes the presence of many sclerites, segmental limbs or formations independent of limbs. Hy- many formative elements (such as processes, apodemes, potheses on the morphological interpretation of the phal- and ridges), and a rich musculature. The symmetry of lic organs are highly diverse, with many questionable the phallic organs ranges from fully bilateral (e.g. many arguments but also conflicting evidence (e.g. SNODGRASS Ortho ptera: SNODGRASS 1937) to asymmetrical in a way 1936, 1957; BECKER 1966: p. 264; BITSCH 1974b: p. 218; that the homonomy of elements of the two sides has re- ISSN 1863-7221 (print) | eISSN 1864-8312 (online) 235 Klass & Matushkina: Male genitalia of Archaeognatha mained obscure (e.g. Dictyo ptera: KLASS 1997; Phasmat- dition of the coxal lobes on venter 9 and the presence on odea: HELM et al. 2011). The ontogenetic development of venters 8 and 9 of long, sclerotised gonapophyses (often the phallic organs (e.g. SNODGRASS 1936, 1957; MATSUDA called ‘parameres’ in the males) instead of coxal vesicles 1976 and references therein) starts with a pair of primary (BITSCH 1994). In the males, both pairs of gonapophyses phallic lobes. These either fuse medially to form an un- can be present or absent; those of venter 9 are, if present, paired penis (Archaeognatha, Zygentoma); or each forms intimately associated with the penis. one penis of a pair (Ephemero ptera); or each lobe divides Archaeognatha is most likely the sister group of the (ty pial for Neo ptera), usually in a mesal mesomere and remaining Insecta, the Dicondylia, which comprise Zyg- a lateral paramere, and the two mesomeres often fuse to entoma and Pterygota (e.g. BEUTEL & GORB 2006; KJER form a median aedeagus. The phallic organs as such are et al. 2006; KLASS 2009; MISOF et al. 2014). Therefore, likely – though not with certainty – homologous across the morphology of the male genitalic region in Archaeo- the Insecta, but their morphology is so diverse that the gnatha is important for conclusions on the early evolu- homology of their elements in different order-level taxa tion of this body part in Insecta and for the use of it as is widely unknown (see SNODGRASS 1957). This is espe- a character system for phylogenetic work. In addition, cially evident when comparing taxa with highly compli- among the insects with well differentiated male and fe- cated phallic organs, such as Dictyo ptera and Phasmato- male genitalic regions, the archaeognathans are the ones dea (see KLASS 1997 and HELM et al. 2011, respectively). where male and female genitalic morphologies as well as Homologies may even partly not exist, as both the struc- the morphologies of genitalic and pregenitalic abdomi- tural complexity and the asymmetry could well have nal segments are most similar, with the homonomies be- been acquired independently in different major lineages. tween sexes and among segments being largely resolved The starting point of phallic evolution in insects may (BITSCH 1974a,b). The abdominal morphology of Ar- have resembled the simple, more or less cylindrical me- chaeognatha is thus also of great significance in tracing dian penes of Archaeognatha (BITSCH 1974b) and Zyg- the origin of insect genitalia under consideration of both entoma (BIRKET-SMITH 1974), but there are competing sexes. This matter was never analysed in detail. hypotheses of paired penes like those of Ephemero ptera The numerous illustrations of archaeognathan male being ancestral (e.g. SNODGRASS 1936). The females seem genitalia in taxonomic contributions are mostly sketches to consistently lack projections potentially homonomous focused on the shape and surface structures (e.g. seta- with the phallic organs (e.g. BITSCH 1974a,b for Archaeo- tion) of the projecting parts: coxal lobes, penis, and gon- gnatha). However, whether females possess projecting apophyses (e.g. STURM & MACHIDA 2001: figs. 4.3., 8.26, or non-projecting elements isosegmentally homonomous 8.27; BACH DE ROCA et al. 2013). Contributions consider- with particular phallic elements depends strongly on the ing the other exoskeletal parts of the male genitalic region morphological interpretation of the male phallic organs are scarce. Most of them only treat selected parts (SMITH and other postabdominal structures of both sexes, which 1969, 1970) or are very sketchy (SNODGRASS 1935, 1936). is widely unclarified. GUSTAFSON (1950) studied several archaeognathan spe- Many of the non-phallic parts of the posterior abdo- cies in order to conclude on the origin of insect genitalia, men of male insects can show differentiations more or but his work lacks detailed descriptions and illustrations. less strongly involved in genitalic functions. Most usu- MATSUDA’s (1957) investigation of the archaeognathan ally the ventral side of abdominal segment 9 (= venter Neomachilis halophila Silvestri, 1911 is focused on the 9) shows differentiations correlated with the placement abdominal musculature; he only provides a brief textual of the phallic organs on or immediately behind it. This description and diagrammatic drawings of the male geni- mainly concerns an elongation of its limb vestiges (coxal talic exoskeleton. BECKER (1966) conducted comparative lobes) and often their median fusion