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Functional Morphology of the Male Genitalia and Copulation in Lower

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Functional Morphology of the Male Genitalia and Copulation in Lower AZO094.fm Page 331 Wednesday, September 5, 2001 10:03 AM Acta Zoologica (Stockholm) 82: 331–349 (October 2001) FunctionalBlackwell Science Ltd morphology of the male genitalia and copulation in lower Hymenoptera, with special emphasis on the Tenthredinoidea s. str. (Insecta, Hymenoptera, ‘Symphyta’) Susanne Schulmeister Abstract Institut für Zoologie und Anthropologie, Schulmeister, S. 2001. Functional morphology of the male genitalia and Abteilung Systematik, Morphologie und copulation in lower Hymenoptera, with special emphasis on the Tenthredinoidea Evolutionsbiologie, Berliner Str. 28, s. str. (Insecta, Hymenoptera, ‘Symphyta’). — Acta Zoologica (Stockholm) 82: D–37073 Göttingen, Germany 331–349 Keywords: A general description of the male reproductive organs of lower Hymenoptera Hymenoptera, Tenthredinoidea, is given. The terminology of the male genitalia is revised. The male external morphology, male genitalia, copulation genitalia of Tenthredo campestris are treated in detail as a specific example of the morphology. The interaction of the male and female parts during copula- Accepted for publication: tion is described for Aglaostigma lichtwardti. The possible function of sclerites 5 April 2001 and muscles of the male copulatory organ of Tenthredinoidea s. str. is dis- cussed. Additional observations on morphology and function made in non- tenthredinoid lower Hymenoptera are included. The assumption that the gonomaculae act as suction cups is confirmed for the first time. The evolution of obligate and facultative strophandry is discussed. The stem species of all Hymenoptera was probably orthandrous and facultatively strophandrous. Susanne Schulmeister. Institute of Zoology, Berliner Str. 28, D–37073 Göttingen, Germany. E-mail: [email protected] tionships among Hymenoptera. This scarcity of male genital Introduction characters is due to the fact that a comparative analysis in a The lower Hymenoptera known as ‘Symphyta’ or sawflies phylogenetic context does not exist. The detailed investiga- are a paraphyletic grouping lacking the wasp-waist of the tion of the morphology and function of the male copulatory Apocrita. Among them, the Tenthredinoidea s. str. [Argidae, organ of the Tenthredinoidea s. str. presented here was Cimbicidae, Diprionidae, Pergidae (= Pterygophoridae) and undertaken to serve as the basis for such an analysis. Tenthredinidae] are probably monophyletic (Vilhelmsen To date, the most extensive publication on the male exter- 1997, 2001). With about 7400 described species, the nal genitalia of ‘Symphyta’, especially their musculature, is Tenthredinoidea s. str. comprise the majority of the approx- that of Boulangé (1924). Other noteworthy papers on this imately 8000 described sawfly species (Goulet and Huber topic are those of Birket-Smith (1981), Crampton (1919), 1993). Peck (1937), Ross (1945), Michener (1956), E. L. Smith Since the ‘Symphyta’ are the basal groups of Hymeno- (1969, 1970a, 1970b, 1972), and Snodgrass (1941). The ptera, they play an important role in the elucidation of the copulation of sawflies is discussed in Boulangé (1924), relationships between holometabolous insect groups. Many Rohwer (1915), d’Rozario (1940), and E. L. Smith (1970a). morphological features of lower Hymenoptera have already The function of the genital muscles of a male braconid been studied intensively and used for phylogenetic analysis (Apocrita) was studied by Alam (1952). However, the present (Königsmann 1976, 1977; Vilhelmsen 1997, 2000; refer- paper treats the morphology and especially the function in ences therein), but very few characters of the male external much more detail. genitalia were employed in these studies. Of the five male There has been a lot of confusion about the terminology genital characters included in Vilhelmsen (2001), two were of the parts of the male genital organ in Hymenoptera. A coded as invariant in the Hymenoptera, and therefore only main source for this confusion is the fact that early authors three were potentially informative for the phylogenetic rela- studied mainly Apoidea, in which the male copulatory organ © 2001 The Royal Swedish Academy of Sciences AZO094.fm Page 332 Wednesday, September 5, 2001 10:03 AM Male genitalia and copulation in Hymenoptera • Schulmeister Acta Zoologica (Stockholm) 82: 331–349 (October 2001) is highly derived, and later on their terms were often applied exemplars from each species were examined. The male to non-homologous parts in other Hymenoptera. A treatment genitalia were dissected under a Zeiss stereomicroscope of all terms that have been applied to the male external geni- Stemi SV 6 (maximum magnification 50). Viewing the talia of Hymenoptera is beyond the scope of this paper, but objects under light coming from the side (obtained by point- is in preparation. However, the usage of the most important ing the tip of a goose-necked lamp at the side of the prepara- of the many existing terms is discussed in the present paper. tion dish) proved sufficient for a discrimination of the parts, An interesting feature of the male genital organ of Xyelinae so that staining was not necessary. Drawings were made with and Tenthredinoidea s. str. is that it is revolved as a whole by the aid of a camera lucida. 180° on its median axis (Crampton 1919). The normal con- Sclerites and membranes of the male genitalia can be hard dition is called orthandrous (orthandrious), the rotated con- to distinguish at the beginning. It proved useful to dry a gen- dition strophandr(i)ous (Crampton 1919). In strophandrous ital organ in a critical point dryer, apply a gold-coating (as for sawflies, the true ventral side becomes the apparent dorsal electron microscopy), and examine it under a stereomicro- side of the genital organ, which Boulangé (1924) termed ex- scope. Sclerites treated in this manner appear smooth and ventral. In this paper, the terms ventral and dorsal always shining, whereas membranes appear rough and dull. refer to the original (i.e. orthandrous) condition, i.e. ‘ventral’ Copulations were either observed (rather coincidentally) always means ‘anatomically ventral’. Strophandry probably in the field (in C. pygmeus, E. koehleri and T. temula) or initi- evolved independently in Xyelinae and Tenthredinoidea ated by putting a female and a male together in a vial (in s. str. (Vilhelmsen 1997, 2001). According to Rasnitsyn (1969; C. pygmeus, A. lichtwardti and M. ferruginea). Pairs fixed in in Ronquist et al. 1999), the torsion is already present in the copula were obtained by drowning them in alcohol (70–95%) pupa in Tenthredinoidea s. str., while in Xyelinae it appears during copulation. The pairs stayed coupled in about 30– during eclosion. No anatomical differences in the torsion of 50% of the attempts. Four pairs in copula of A. lichtwardti the male genitalia could be observed in these two taxa. were dissected. However, in the copulation of orthandrous as well as Aglaostigma lichtwardti was chosen for a detailed study of strophandrous Hymenoptera the ventral side of the male copulation because it was the only tenthredinoid species of genitalia is always facing up, whereas the dorsal side is always which several pairs in copula could be obtained. However, facing down, towards the substrate. In orthandrous species the drawings in the morphological part of this paper show this is achieved, for example, by curving the abdomen so that mainly Tenthredo campestris, because its male copulatory the tip of the abdomen comes to lie upside down. In organ is less derived than that of Aglaostigma and therefore strophandrous species such a measure is unnecessary facilitates comparison with other species. However, the dif- because the male genitalia already are upside down. ferences are not substantial, so that the general conclu- sions drawn about the functional morphology in the present paper should apply to both these species and most other Material and Methods Tenthredinoidea s. str. as well. (The differences between The species studied are shown in Table 1. these two species can be deduced to some extent from All specimens were fixed in Bouin’s fluid and kept in Fig. 2A,B vs. 4B,C; Fig. 8A vs. 8D; Fig. 7F vs. 9 A, and from ethanol (70%) until the preparation. If possible, two or more Fig. 6) Table 1 Species studied in this paper Xyeloidea: Xyelidae: Macroxyela ferruginea (Say, 1824) Tenthredinoidea: Blasticotomidae Runaria reducta (Malaise, 1931) Tenthredinidae: Nematus abbotii (Kirby, 1882) Tenthredo campestris (Linnaeus, 1758) Tenthredo temula (Scopoli, 1763) Macrophya annulata (Geoffroy, 1785) Aglaostigma lichtwardti (Konow, 1892) Elinora koehleri (Klug, 1817) Argidae: Arge rosae (Linnaeus, 1758) Arge rustica (Linnaeus, 1758) Pergidae: Lophyrotoma analis (Costa, 1864) Diprionidae: Macrodiprion nemoralis (Enslin, 1917) Pamphilioidea: Megalodontesidae: Megalodontes cephalotes (Fabricius, 1781) = klugi (Leach, 1817) = spissicornis (Klug, 1824) Pamphiliidae: Cephalcia sp. Cephoidea: Cephidae: Cephus pygmeus (Linnaeus, 1767) Siricoidea: Siricidae: Xeris spectrum (Linnaeus, 1758) Anaxyelidae: Syntexis libocedrii Rohwer, 1915 © 2001 The Royal Swedish Academy of Sciences AZO094.fm Page 333 Wednesday, September 5, 2001 10:03 AM Acta Zoologica (Stockholm) 82: 331–349 (October 2001) Schulmeister • Male genitalia and copulation in Hymenoptera Fig. 1—Male reproductive organs. —A. Schematic drawing to show the relations of the membranous parts of the integument, the sclerites and the inner reproductive organs. —B. One half of the male genitalia of Tenthredo campestris, looking onto the medio-sagittal
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