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An Instance of Intergeneric Copulation in the Family Rhopalidae

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An Instance of Intergeneric Copulation in the Family Rhopalidae ZOOSYSTEMATICA ROSSICA ISSN 2410-0226 Zoological Institute, Russian Academy of Sciences, St Petersburg ▪ https://www.zin.ru/journals/zsr/ [ onl ine] 0320-9180 Vol. 28(1): 3–18 ▪ Published online 7 March 2019 ▪ DOI 10.31610/zsr/2019.28.1.3 [ print] RESEARCH ARTICLE An instance of intergeneric copulation in the family Rhopalidae (Heteroptera): structure, functioning and congruence of the genitalia in two different species from the standpoint of the lock-and-key hypothesis Случай межродового спаривания в семействе Rhopalidae (Heteroptera): структура, функционирование и конгруэнтность гениталий двух разных видов с точки зрения гипотезы «ключ-замок» D.A. Gapon Д.А. Гапон Dmitry A. Gapon, Zoological Institute, Russian Academy of Sciences, 1 Universitetskaya Emb., St Petersburg 199034, Russia. E-mail: [email protected] Abstract. An event of mating between specimens of Corizus hyoscyami and Rhopalus parumpunctatus, registered in the Novgorod Province of Russia is considered. The structure of the aedeagi in their completely inflated state and the female genitalia, as well as the functioning of the genitalia, are described and illustrated. The process of unfolding and swelling of the aedeagi is traced using the method of hydraulic inflation of the membranous parts with glass microcapillaries. The congruence of the genitalia is discussed for each species, and also for the interspecific crosses in both combinations of sexes and species. Structures of insect terminalia are divided into three groups according to their functions: 1) auxiliary structures; 2) structures providing the mutual fixation of the genitalia; and 3) structures directly performing the function of transferring seminal fluid. It is shown that in the considered variants of interspecific crosses, the parts of the genitalia belonging to the second group have almost the same structure and functioning, and most likely cannot perform the function of structural isolation. The structures of the third group have taxon-specific morphological and functioning traits and a high degree of congruence within each species. Schemes of the functioning of the genitalia in interspecific crosses, speculatively showing the impossibility of normal insemination, are proposed. Резюме. Рассмотрен случай спаривания между Corizus hyoscyami и Rhopalus parumpunctatus, зарегистрированный в Новгородской области России. Описано и проиллюстрировано строение эдеагусов в полностью раздутом состоянии и гениталий самок, а также их функционирование. Прослежен процесс расправления и раздувания эдеагусов при помощи метода гидравлического их раздувания с использованием стеклянных микрокапилляров. Рассмотрена конгруэнтность гениталий для каждого вида, а также в межвидовых скрещиваниях в обеих комбинациях полов и видов. Структуры терминалий разделены на три группы по их функциям: 1) вспомогательные структуры; 2) структуры, обеспечивающие взаимную фиксацию гениталий; и 3) структуры, выполняющие функцию передачи семенной жидкости. Показано, что структуры второй группы в рассматриваемых вариантах межвидового спаривания имеют почти одинаковое строение и, скорее всего не могут выполнять функцию структурной изоляции. Структуры третьей группы имеют специфическое для каждого таксона строение и особенности функционирования, обладая высокой степенью конгруэнтности внутри каждого вида. Предложены схемы функциони- рования гениталий в межвидовых спариваниях, умозрительно показывающие невозмож ность нормального осеменения. © 2018 Zoological Institute RAS and the Author(s) D.A. Gapon. An instance of intergeneric copulation in the family Rhopalidae Key words: genitalia, aedeagus, gynatrium, functioning, congruence, structural reproductive isolation, lock-and-key hypothesis, insects, Heteroptera, Rhopalidae Ключевые слова: гениталии, эдеагус, гинатриум, функционирование, конгруэнтность, структурная репродуктивная изоляция, гипотеза «ключ-замок», насекомые, полужестко- крылые, Rhopalidae ZooBank Article LSID: urn:lsid:zoobank.org:pub:6C796633-E732-4F3C-8114-D123D5073588 Introduction 1829. According to the author of the photos, E.Yu. Kirtsideli, the mating was lasting during The lock-and-key hypothesis has been proposed about 20 minutes while photographing and by Dufour in 1844 in an extravagant statement, was continued thereafter, although no further ‘L’armure copulatrice est un organe ou mieux un observations were carried out and the material instrument ingénieusement compliqué, destiné was not collected. This event of intergeneric à s’adapter aux parties sexuelles externes de la copulation is curious per se and interesting femelle pour l’accomplissement de l’acte copulatif; from the standpoint of the lock-and-key rule. elle est la garantie de la conservation des types, Obviously, the reproductive isolation mechanism la sauvegarde de la légitimité de l’espèce’. Since of genitalia did not operate in this case, since the then, quite a lot of data has been accumulated for copulation began and lasted for rather a long time different groups of animals, both confirming and (unfortunately, it is not known how long it lasted disproving this hypothesis; review of these data as a whole and how long the normal copulation is given, for example, by Mayr, 1963; Shapiro & continues for each of these species). Therefore, it Porter, 1989; and Masly, 2012 (I deliberately seems to me interesting to consider the structure shy away from the consideration of particular of the genitalia in these species for understanding examples and theoretical considerations proposed why copulation between these rather strongly in the literature, since otherwise the volume of the diverged species from the group having a complex article would have increased by several times). It structured aedeagus turned out to be possible; seems more correct to designate this concept not and whether the mechanism of structural isolation as a hypothesis, but as the lock-and-key rule or which is supposed to prevent insemination was Dufour’s rule, which can be formulated as follows: implemented. complex structured genitalia of various animal Thus, the purpose of this work was to exa- species are congruent in the sexes inside the mine the structure of male and female internal species and operate like a key and lock, preventing ectodermal genitalia in C. hyoscyami and hybridisation between individuals of different Rh. parumpunctatus, the functional morphology species. The challenge for researchers is to test of these structures and to evaluate a degree of the applicability of this rule to as many taxonomic their morphological and functional congruence in groups as possible, taking into account past the interspecific cross, both direct and reciprocal. methodological errors, when only the external and auxiliary, not participating in closest contact parts Material and methods of genitalia were involved in the analysis (for more on this, see below in the Preliminary reasoning The photographs of mating true bugs were section). One of model objects convenient for taken on 29 May 2013 in a meadow near particular testing of the lock-and-key rule is Terekhovo Village, Novgorod Province, Russia. considered in this article. The genitalia of dry specimens of C. hyoscyami and Some time ago I have received photos of Rh. parumpunctatus were examined basing on the copulating true bugs (Fig. 1; Figs 13–15 as material from collection of the Zoological Institute, electronic supplementary material) which were Russian Academy of Sciences. The structure and identified by me asCorizus hyoscyami (Linnaeus, functional morphology of the aedeagi was studied 1758) and Rhopalus parumpunctatus Schilling, by the method of hydraulic inflation using glass 4 ( Zoosystematica Rossica, Vol. 28, No. 1, pp. 3–18 D.A. Gapon. An instance of intergeneric copulation in the family Rhopalidae Fig. 1. Copulation of Corizus hyoscyami (male) and Rhopalus parumpunctatus (female), Novgorod Province. Photograph by E.Yu. Kirtsideli. microcapillaries (Gapon, 2001). Female terminalia 1 female. Russia: Ryazan’ Rrov., Miloslavskiy were anatomised by the standard method after Distr., Gremyachka Settlm., 13, 27.V.1908 (A. & Z. boiling for 2–3 minutes in 15–20% KOH solution; Semenov), 1 male, 1 female; Nizhniy Novgorod Prov., when necessary, gynatrial membranes were Arzamas Distr., Staraya Pustyn’, 12,16,22.VIII.1939 stained with methylene blue. In all cases, including (Kiritshenko), 2 males, 3 females; Samara Rrov., Kinel’ Distr., Kinel’, 23–24,26.VII.1927 (Lubischew), 1 consideration of the functional morphology, the male, 1 female; Volgograd Prov., Sarepta [Volgograd], aedeagi are described according to their position in 30.V.1926 (Obolenskiy), 1 male; Irkutsk Rrov., Tayshet an inverted pygophore, i.e. in copula. Thus, the right Distr., Yurty Settlm., 23.V1912 (Mishin & Verkhovsk. side of the aedeagus in the descriptions corresponds [iy]), 1 male. Kyrgyzstan, 1928, 1 male (collector to the left side of the gynatrium. Terminology for unknown). parts of the endosoma is based on the topographic principle and follows Konstantinov & Gapon Rhopalus parumpunctatus Schilling, 1829 (2005) and Gapon (2007); terminology for parts of (Figs 1, 7–9, 12; Figs 13–16 as electronic the internal ectodermal genitalia of females follows supplementary material) Štys (1961) and Gapon (2007). Material examined. Russia: Tver’ Prov.[?], Mele- Structure of the genitalia dikha Settlm., 16.VII.1912 (S. Rodionoff), 1 female; Moscow Prov., Zaraysk Distr., Gremyachevo Settlm. Corizus hyoscyami (Linnaeus, 1758) (L. Bianki), 1 female; Ryazan’ Prov., Ryazan’ Distr.,
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