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

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 функционирования гениталий в межвидовых спариваниях, умозрительно показывающие невозмож ность нормального осеменения. D.A. Gapon. An instance of intergeneric copulation in the family Rhopalidae ( Zoosystematica Rossica, Vol. 28, No. 1, pp. 3–18 4 Introduction The lock-and-key hypothesis has been proposed by Dufour in 1844 in an extravagant statement, ‘L’armure copulatrice est un organe ou mieux un instrument ingénieusement compliqué, destiné à s’adapter aux parties sexuelles externes de la femelle pour l’accomplissement de l’acte copulatif; elle est la garantie de la conservation des types, la sauvegarde de la légitimité de l’espèce’. Since then, quite a lot of data has been accumulated for different groups of animals, both confirming and disproving this hypothesis; review of these data is given, for example, by Mayr, 1963; Shapiro & Porter, 1989; and Masly, 2012 (I deliberately shy away from the consideration of particular examples and theoretical considerations proposed in the literature, since otherwise the volume of the article would have increased by several times). It seems more correct to designate this concept not as a hypothesis, but as the lock-and-key rule or Dufour’s rule, which can be formulated as follows: complex structured genitalia of various animal species are congruent in the sexes inside the species and operate like a key and lock, preventing hybridisation between individuals of different species. The challenge for researchers is to test the applicability of this rule to as many taxonomic groups as possible, taking into account past methodological errors, when only the external and auxiliary, not participating in closest contact parts of genitalia were involved in the analysis (for more on this, see below in the Preliminary reasoning section). One of model objects convenient for particular testing of the lock-and-key rule is considered in this article. Some time ago I have received photos of copulating true bugs (Fig. 1; Figs 13–15 as electronic supplementary material) which were identified by me as Corizus hyoscyami (Linnaeus, 1758) and Rhopalus parumpunctatus Schilling, 1829. According to the author of the photos, E.Yu. Kirtsideli, the mating was lasting during about 20 minutes while photographing and was continued thereafter, although no further observations were carried out and the material was not collected. This event of intergeneric copulation is curious per se and interesting from the standpoint of the lock-and-key rule. Obviously, the reproductive isolation mechanism of genitalia did not operate in this case, since the copulation began and lasted for rather a long time (unfortunately, it is not known how long it lasted as a whole and how long the normal copulation continues for each of these species). Therefore, it seems to me interesting to consider the structure of the genitalia in these species for understanding why copulation between these rather strongly diverged species from the group having a complex structured aedeagus turned out to be possible; and whether the mechanism of structural isolation which is supposed to prevent insemination was implemented. Thus, the purpose of this work was to examine the structure of male and female internal ectodermal genitalia in C. hyoscyami and Rh. parumpunctatus, the functional morphology of these structures and to evaluate a degree of their morphological and functional congruence in the interspecific cross, both direct and reciprocal. Material and methods The photographs of mating true bugs were taken on 29 May 2013 in a meadow near Terekhovo Village, Novgorod Province, Russia. The genitalia of dry specimens of C. hyoscyami and Rh. parumpunctatus were examined basing on the material from collection of the Zoological Institute, Russian Academy of Sciences. The structure and functional morphology of the aedeagi was studied by the method of hydraulic inflation using glass