The Lock-And-Key Mechanisms of the Internal Genitalia of the Noctuidae (Lepidoptera): How Are They Selected For?
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POINT OF VIEW Eur. J. Entomol. 105: 13–25, 2008 http://www.eje.cz/scripts/viewabstract.php?abstract=1296 ISSN 1210-5759 (print), 1802-8829 (online) The lock-and-key mechanisms of the internal genitalia of the Noctuidae (Lepidoptera): How are they selected for? KAURI MIKKOLA Finnish Museum of Natural History, P.O. Box 17, FI-00014 University of Helsinki, Finland; e-mail: [email protected] Key words. Apamea, functional anatomy, species-specific, male vesica, female bursa, monandry, polyandry, evolution, genetic drift, sexual selection, zoogeography, Holarctic sister species Abstract. In the Noctuidae, the owlet moths, the internal genitalia, i.e. the aedeagus and vesica (penis) in the males, and the bursa copulatrix in the females, together form a lock-and-key mechanism (LKM). The species-specific structures have their counterparts in the opposite sex. The internal LKM constitutes a specific reproductive isolation mechanism (lock-and-key hypothesis), which seem to be the rule in the ditrysian Lepidoptera, and also occurs in the Carabidae (Coleoptera) and some other insects. In contrast, the external genitalia rarely have species-specific counterparts in the sexes. Several results indicate the presence of LKMs: In the Noc- tuidae, (1) heterospecific differences in the male vesica may prevent sperm transfer or lead to mechanical failure during copulation, (2) the more complicated the specific genitalia structures, the more aberrations may occur even in conspecific copulations, and (3) in many species pairs and groups, and in one large genus, Apamea, the structures in the opposite sexes show a strictly specific corre- spondence, but, (4) when there is precopulatory isolation due to differences in pheromone production or perception, the internal genitalia may be identical. Conversely, in the Colias butterflies (Pieridae), (5) frequent heterospecific hybridization is associated with the similarity of the internal genitalia. The LKMs seem to protect genomes against alien genes, supposedly selected for because of the lower fitness of specimens with an imprecise LKM and/or inferiority of hybrids. In the literature, the diversity of the noctuid genitalia has been ascribed to sexual selection, because the females were classified as polyandrous. Most species produce the main part of their eggs monandrously, and remate, if at all, in their old age, and are thus successively monandrous and polyandrous. The allopatric divergence in the structure of the internal genitalia of 39 Holarctic pairs of sister species of Noctuidae is suggested to be due to genetic drift. The insecure function of the female pheromones and external genitalia of males are illustrated with the aid of original photographs. 1. Introduction 2. Proof of the lock-and-key mechanisms in the internal genitalia 2.1. Anatomical and physiological evidence 2.2. Morphological evidence 2.3. Evidence from other Lepidoptera and other insects 3. Precopulatory mechanical isolation mechanisms 4. Remating in the Noctuidae and other Lepidoptera 5. Divergence among the Holarctic pairs of sister species of Noctuidae 6. Discussion 6.1. General aspects 6.2. Zoogeographical aspects 6.3. Speciation and the species concept 7. References 1. INTRODUCTION early stage of the coupling process, and the internal geni- The lock-and-key hypothesis (LKH) was defined by talia subsequently lock the sexes together rendering the Eberhard (1985) and by Shapiro & Porter (1989) who sperm transfer possible. The LKMs occur in the internal briefly wrote that it purports “to explain species-specific genitalia. Compared to the long tradition of using charac- genital morphology in terms of mechanical reproductive ters of the external genitalia in lepidopteran species tax- isolation”. Eberhard (1985) considers that the lock-and- onomy, the taxonomic use of internal genitalia is a keys (LKMs) are just “backup or fail-safe devices” and relatively recent and rapidly developing aspect of Shapiro & Porter (1989) think that “the hypothesis has research (cf. Mikkola, 2007), which has resulted in the not yet been supported convincingly”. evolutionary study of the LKMs. These authors do not specify whether they refer to the Most of the authors that discuss insect lock-and-key external genitalia, the male uncus and valvae, as they are mechanisms fail to distinguish between the functions of called in Lepidoptera, or to the internal genitalia, the male the external and internal genitalia (e.g. Thornhill & aedeagus and vesica and female bursa copulatrix, or both Alcock, 1983; Eberhard, 1985, 1996; Shapiro & Porter, (cf. Figs 1–2). The external genitalia are important at an 1989; Arnqvist, 1998; Arnqvist & Green, 2002). It is puz- zling why these authors do not refer to the pioneering 13 Fig. 1. The male abdominal skin and male and female genitalia of the noctuid moth Apamea maillardi (Geyer, 1834) mounted on microscope slides. From the left: 1 – male skin with hair brushes; 2 – male external genitalia, caudal aspect, opened by pressing, without aedeagus; 3 – male internal genitalia, ventral aspect with posterior upwards; 4 – female genitalia in similar position. The fit of the male internal genitalia into that of the female should be checked by turning them around, cf. Fig. 2. The overall fit is not self- evident because the receiving parts of the female are often flexible; the correspondence of the shapes of the “shoulders” is easily seen, however. This female has copulated twice as there are two spermatophores in the bursa copulatrix. work on the functional anatomy of the internal genitalia the aedeagus and the corresponding fold in the female of Noctuidae (Lepidoptera) by Callahan & Chapin indicate that during copulation the aedeagus penetrates (1960). However, Eberhard (1985) does cite the number the entire length of the ductus bursae (cf. Mikkola, 1992: of spermatophores. Similarly, Arnold & Fischer (1977), Figs 1 and 3). Only thereafter does the vesica have the publishing in the same journal as Callahan & Chapin, do space to expand and produce the spermatophore. Note: not mention their work, nor do Scoble (1995) and the short aedeagus of Cyanotricha (Dioptidae) does not Arnqvist & Nilsson (2000) include it in their reviews. enter the female (Miller, 1988). Kristensen (2003) presents illustrations from Callahan & In describing copulation in Lepidoptera the following Chapin (1960), but without mentioning their conclusion nomenclature is followed (cf. Figs 1–2): about a “definite ‘lock-and-key’ barrier”. (1) External genitalia, the male valvae (referred to as Many examples indicate that LKMs are at present an gonopods in many other insect groups) and uncus, grip unpopular topic in discussions of the evolution of genita- the female’s abdomen at three points at the onset of cou- lia. Some of the traits that were earlier predicted by the pling. LKH, such as negative allometry and little variation in the (2) External coupling involves the use of the external structure of genitalia (Arnqvist, 1997), were soon, by genitalia. It is mostly a transient fixing phase before weak and seemingly ad hoc arguments, attributed to copulation proper, but may have an extended sensory sexual selection (Eberhard et al., 1998, cf. Green, 1999). function (see below). It does not have any direct bearing As regards Lepidoptera, the statement of Hosken & upon reproduction. Stockley (2004) that the LKH is not consistent with the (3) Internal genitalia, the male aedeagus and vesica, “evidence based on the morphology of the female repro- and female bursa copulatrix from ostium bursae to the ductive tract” and “genital associations during copula”, is opening of the ductus seminalis, show anatomical corre- surprisingly erroneous (see Chapter 2). spondences (the LKMs). Such a correspondence is often Mutanen et al. (2006) and Mutanen & Kaitala (2006) seen also between the male juxta (ventral sclerotization of have unfortunately misunderstood the function of the fultura inferior, the diaphragma) and female lamina ante- sclerotized aedeagus (= penis, phallus). The latter authors vaginalis of the ductus bursae, as well as between the (2006: 299) exclude it from the internal genitalia by citing male spermatophore and female corpus bursae (Lafon- Callahan & Chapin (1960) and claiming that it “is posi- taine & Mikkola, 1987; Mikkola, 1992, see below). tioned on the female ostium bursae but is not placed in (4) Internal coupling involves the internal genitalia. the female ductus bursae”, and explaining that the internal The LKM lock the sexes together for copulation proper genitalia should be soft. However, Callahan & Chapin (cf. Callahan, 1958b: Fig. 1), during which the male (1960: 778) report that in both Peridroma and Pseu- inserts a spermatophore into the female bursa and sperm daletia the aedeagus is short and “fits only a short dis- transfer may or may not occur. tance up the female ductus bursae”. For Helicoverpa zea (5) Postlocking isolation denotes isolation caused by an (Boddie), Callahan (1958b: Fig. 6) shows that the unsuccessful transfer of sperm into the female ductus aedeagus penetrates the whole length of the ductus seminalis. bursae. The aedeagus is certainly rigid, because of the (6) Postcopulatory isolation, mainly genetic, occurs requirements of intromission and protection of the mem- after sperm transfer. branous vesica (= endophallus). The carina near the tip of 14 Fig. 2. The lock-and-key mechanism of the palaearctic noctuid species Apamea crenata (Hufnagel, 1766) and its nearctic sister species Apamea vultuosa (Grote, 1875). In both,