Article

Possible Removal of Rival Sperm by the Elongated Genitalia of the Earwig, Euborellia plebeja

Authors:
To read the full-text of this research, you can request a copy directly from the author.

Abstract

Sperm displacement is a sperm competition avoidance mechanism that reduces the paternity of males that have already mated with the female. Direct anatomical sperm removal or sperm flushing is known to occur in four insect orders: Odonata, Orthoptera, Coleoptera and Hymenoptera. In a fifth order, Dermaptera (earwigs), I found that the virga (the elongated rod of the male genitalia) of Euborellia plebeja seems to be used to remove rival sperm from the spermatheca (a fine-tubed female sperm storage organ). In this species, copulation lasted on average 4.6 minutes, during which time the male inserted the virga deep into the spermatheca, and then extracted it ejaculating semen from the opening of the virgal tip. The extraction of virgae (with its brim-like tip) appeared to cause removal of stored sperm in the spermatheca. The virga was as long as the body length of males, and the spermatheca was twice the female body length. The long length of the spermatheca and the possible removal function of the virga may select for virgal elongation.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the author.

... The entire length of the spermatheca was measured using a curvi-meter (COMCURVE-8, KOI-ZUMI, Tokyo, Japan; to the nearest 3.57-7.69 lm, depending on the magnification: see Kamimura, 2000 for details) for the samples that had been sufficiently spread on a slide (N = 17 out of 30 prepared). ...
... Because the mating duration of this species is relatively short (Kamimura, 2000(Kamimura, , 2013, matings were interrupted 1.5 min after initiation, at which time the virgae were inserted deeply into the spermatheca (Kamimura, 2000(Kamimura, , 2003. The treated males were kept for at least 3 days to allow for the development of detectable melanized patches, which are indicative of wound repair (Kamimura & Matsuo, 2001). ...
... Because the mating duration of this species is relatively short (Kamimura, 2000(Kamimura, , 2013, matings were interrupted 1.5 min after initiation, at which time the virgae were inserted deeply into the spermatheca (Kamimura, 2000(Kamimura, , 2003. The treated males were kept for at least 3 days to allow for the development of detectable melanized patches, which are indicative of wound repair (Kamimura & Matsuo, 2001). ...
Article
Full-text available
Ovoviviparity or viviparity has evolved independently in animals and involves adaptations in females to accommodate developing embryos for a prolonged duration in their bodies, a condition which has likely to have influenced the evolution of the male genitalia. We aimed to ascertain whether the elongated male genitalia of the ovoviviparous free-living earwig species Marava arachidis (Dermaptera: Spongiphoridae) delivers sperm directly to the female ovaries where fertilization occurs. Males mated coercively with females by grabbing the female antenna with their mouth parts. Although females resisted the mating attempts, pairs mated 3.3 times on average over 15 h. The elongated intromittent organ, known as a virga, was inserted into the long-tubed spermatheca during insemination. Surgical ectomy of the spermatheca confirmed that sperm migrated from here to the ovaries with a variable delay. A pair of sclerites in the male genitalia frequently inflicted wounds near the spermathecal opening, while the single, thin virga sometimes broke off during mating. However, unlike earwigs bearing a 'spare' virga, damage was restricted to the tip of the virga, without which the males could still inseminate the females. We discuss the evolution of the genitalia in this insect in the light of sexual selection and sexual conflict over mating and fertilization.
... Haas 1995;Haas & Kukalová-Peck 2001) treated Anisolabididae as a taxa lacking basal vesicles, this structure has also been found in several anisolabidids (e.g. Hudson 1973;Sakai 1987a;Kamimura 2000)). The most caudal part (or entire length) of each virga is surrounded by a membranous penis lobe (here I define a penis as a virga and its penis lobe). ...
... Both of these questions have being explored in relation to postcopulatory sexual selection. In anisolabidids such as A. maritima and Euborellia plebeja (Dohrn), males have two functionally competent elongated virgae, although they use only one of them during a single genital coupling (Kamimura 2000;Kamimura & Matsuo 2001). Since the virgae are fragile, they sometimes break off during mating; therefore, the remaining counterpart in paired virgae functions as a spare (Kamimura & Matsuo 2001). ...
... The resulting allometric relationship was negative with a slope of 0.653 (major axis regression; 95% confidence interval of the slope 0.567-0.755). For the same species, a previous study with a much smaller sample size (n = 43) did not detect a significant correlation between the two traits, apparently because of the low allometric slope (Kamimura 2000). Similarly, in another anisolabidid, M. brunneri, male genital length showed only a weak, positive correlation with body size (measured as pronotum width; n = 15-92; van Lieshout 2011;van Lieshout & Elgar 2011a). ...
Article
Dermaptera (earwigs) is a relatively small polyneopteran order with approximately 2200 described species. They are characterized by a pair of forceps, which are hardened, unsegmented cerci at the caudal end of the abdomen. In most species, males have more exaggerated forceps than females, indicating an effect of sexual selection on them. Earwigs also exhibit astonishing diversity in the number, laterality and size of both male and female genital components. This characteristic has promoted the study of postcopulatory sexual selection in several representative species. Here, previous studies of earwigs that examined pre- and postcopulatory sexual selection are reviewed in detail. Related topics included here are sexually antagonistic coevolution, evolution of laterally asymmetrical morphologies, and developmental aspects of intra-sexually dimorphic traits. A new terminology system for male genitalia is also proposed.
... For E. brunneri, van Lieshout & Elgar (2011a) also showed that males with longer genitalia enjoy defensive sperm competitive benefits. Although the detailed sperm displacement mechanism may differ between Euborellia species (note that the newest taxonomic system places brunneri in another genus Mongolabis; Srivastava 1999 ), the elongated virgae of male E. plebeja can also be considered an adaptation for sperm competition (see Introduction; Kamimura 2000 Kamimura , 2005). Thus, females seem to beat males by having a longer spermatheca that allows for only incomplete sperm manipulation. ...
... Thus, it is necessary to examine the costs and benefits of mating to determine whether the highly frequent matings of female E. plebeja can be considered a CFC adaptation. In E. plebeja, males do not donate detectable nutrients during mating or provide care of offspring (Baijal & Srivastava 1974; Kamimura 2000). Males cannot accomplish forced matings and no harassment behaviour to unreceptive females has been reported (Baijal & Srivastava 1974; Kamimura 2000 Kamimura , 2003b Kamimura , 2005). ...
... In E. plebeja, males do not donate detectable nutrients during mating or provide care of offspring (Baijal & Srivastava 1974; Kamimura 2000). Males cannot accomplish forced matings and no harassment behaviour to unreceptive females has been reported (Baijal & Srivastava 1974; Kamimura 2000 Kamimura , 2003b Kamimura , 2005). Therefore, females are not likely to mate frequently for material benefits or to avoid the costs of sexual harassment. ...
Article
Female genitalia often show complex morphologies that cannot be explained by sperm reception and storage functions. However, our understanding of the forces underlying genital exaggeration in females is limited. Female earwigs, Euborellia plebeja, are promiscuous and their highly elongated sperm storage organs allow only partial removal and displacement of stored sperm by shorter male genitalia, resulting in only a 20% gain in paternity per copulation with a sperm-saturated female. This study examined the significance and optimality of restricted sperm displacement for females. A staged mating experiment with a paternity success analysis revealed that large males dominated male-male competition for burrows housing females, resulting in repeated copulations with the same female. Despite the low paternity gain per copulation, such repeated copulations resulted in a significant increase in paternity for larger males with higher resource-holding potential. A numerical simulation based on the relationship between male body size and copulation frequency showed that restricted sperm displacement (about 20% per copulation) is optimal for promiscuous females to accumulate sperm effectively from larger males. Because male body size is heritable in this species, females were estimated to benefit from a 1.4% increase in their sons' mating success. This genetic benefit disappeared when only a single copulation per male-female encounter was assumed. Since no measurable costs of mating for females have been detected in this species, the combination of promiscuity and restricted sperm displacement is best explained by the cryptic female choice hypothesis.
... Females of the earwig Euborellia plebeja mate frequently with multiple males and lay egg batches of mixed paternity, indicating severe sperm competition (Baijal and Srivastava 1974;Kamimura 2003a, b). During mating, males use one of the pair of male intromittent organs (virgae), each of which is as long as the body, to remove rival sperm from the spermatheca, the fine-tubed female sperm-storage organ (Kamimura 2000(Kamimura , 2003a. The mechanism of sperm removal is as follows. ...
... First, a male inserts the virga deeply into the spermatheca without ejaculation. He then extracts the virga while ejecting semen from its tip and simultaneously removing rival sperm using a fringe-like projection on the virgal tip (Kamimura 2000). Because spermathecae are twice the virgal length, and the basal part of the virga lies in the common oviduct posterior to the spermatheca during mating (Kamimura 2000), one can predict that only a portion (less than 50%) of rival sperm is removed by a single mating. ...
... He then extracts the virga while ejecting semen from its tip and simultaneously removing rival sperm using a fringe-like projection on the virgal tip (Kamimura 2000). Because spermathecae are twice the virgal length, and the basal part of the virga lies in the common oviduct posterior to the spermatheca during mating (Kamimura 2000), one can predict that only a portion (less than 50%) of rival sperm is removed by a single mating. Therefore, we can predict that males gain only a minor share of the paternity per single mating when the female has a saturated sperm store. ...
Article
Both sexes of the earwig Euborellia plebeja (Dermaptera: Anisolabididae) mate frequently. The elongated intromittent organs of males are as long as their bodies. Previous studies have revealed that this organ is used to remove rival sperm from the female sperm-storage organ (spermatheca), the length of which is twice that of the female body. The fitness benefit of sperm removal was quantified using two mating experiments with paternity analysis. As expected, given that the sperm-removal organ is shorter than the sperm-storage organ, males gained only about 20% of paternity per single mating with sperm-saturated females. The significance of frequent repeated matings with the same female by males is discussed.
... Furthermore, male and female reproductive morphologies correspond closely in shape, suggesting a co-evolutionary process. The spermatheca comprises a single thin convoluted blind duct of a fractionally greater diameter than the virga (Kamimura 2000(Kamimura , 2005 personal observation). Electron-microscopic examination in Euborellia plebeja, which has a similar reproductive morphology, revealed that virgae have an apical projection that displaces sperm stored in the spermatheca (Kamimura 2000). ...
... The spermatheca comprises a single thin convoluted blind duct of a fractionally greater diameter than the virga (Kamimura 2000(Kamimura , 2005 personal observation). Electron-microscopic examination in Euborellia plebeja, which has a similar reproductive morphology, revealed that virgae have an apical projection that displaces sperm stored in the spermatheca (Kamimura 2000). Consistent with this finding, longer virgae in E. brunneri offer defensive benefits in sperm competition, apparently by depositing ejaculate deeper in the spermatheca, out of range from removal by rivals (van Lieshout and Elgar, unpublished). ...
... The altered mating behaviour of mated females in this study is consistent with such strategic male investment in mating. As predicted, males appear to recognise mated females and respond by protracting individual copulations to include a sperm removal stage previously demonstrated for E. plebeja (Kamimura 2000). Longer copulations are associated with a greater degree of rival sperm removal and increased male fertilisation success in many species (e.g. ...
Article
Full-text available
Phenotypic variation in male genitalia may affect copulation behaviour, which can have important fitness consequences for males. Male genitalia commonly possess traits that increase male control over copulation, but in species where females control mating, a poor functional understanding often prevents insight into the processes responsible for such effects. Here, I investigate the effect of male genital length on copulation behaviour in the earwig Euborellia brunneri, where both sexes exhibit extremely elongated genitalia that correspond in shape. This model system is particularly suitable because pairs mate repeatedly and females can limit both the number and duration of copulations. I used both virgin and mated males and females in a double-mating design because longer male genitalia confer benefits in sperm competition. Consistent with a greater predicted male mating effort in mated females, the duration of individual copulations increased, but this traded off against mating frequency as cumulative mating duration remained unchanged. In contrast, male genital length increased both individual and cumulative mating duration, regardless of mating status. This difference suggests that, while males may modify copulation duration in response to mating status, females facultatively adjust mating frequency to prevent mating excessively or express preferences for increased male genital length. Notably, this study demonstrates that male genital phenotypes that are successful in sperm competition also enjoy female-mediated mating benefits. Keywords Euborellia brunneri –Mating status–Genitalia–Spermatheca–Copulation duration–Copulation frequency–Sperm competition–Female mate choice
... These barb-like structures may be for the removal of rival sperm from female sperm storage organ(s), as known in several insect groups (Waage 1979). Males of the anisolabidid, Euborellia plebeja (Dohrn, 1863) also use their highly elongate virga, which is usually longer than the entire body, for removing rival sperm from the tubular spermatheca of mates (Kamimura 2000). However, in this species, a recurved flange at the virgal tip is considered responsible for sperm removal (Kamimura 2000). ...
... Males of the anisolabidid, Euborellia plebeja (Dohrn, 1863) also use their highly elongate virga, which is usually longer than the entire body, for removing rival sperm from the tubular spermatheca of mates (Kamimura 2000). However, in this species, a recurved flange at the virgal tip is considered responsible for sperm removal (Kamimura 2000). Although males of most earwig species directly insert a virga into the female spermatheca for transferring sperm during copulation (Kamimura 2014;Kamimura et al. 2019), D. flavicollis is an exception: the virgal tips are much wider than the spermathecal openings and ducts, indicating that physical removal of stored sperm by a virga is not feasible (Kamimura 2004). ...
Article
Full-text available
To explore diversity of earwigs (Dermaptera) in different agricultural ecosystems of South India, an extensive taxonomic survey was conducted in 2020 during which an undescribed species of Diplatys was collected. Twenty-one species of the genus Diplatys (Diplatyidae, Diplatyinae) have been reported to date from India, of which six species are known from Karnataka, South India. Based on a male specimen collected from a sugarcane field in Karnataka, a new species, Diplatys sahyadriensis sp. nov. , is described as the twenty-second species of this genus from India. A revised key to the males of Diplatys species from India and Sri Lanka is provided. This new record adds to the known species diversity in the Sahyadri Ranges of the Western Ghats in Shivamogga District, Karnataka, part of the Southern Plateau and Hills agro-climatic region of India.
... It appears to be a challenge for males to insert and withdraw the extremely slender virga (aspect ratio, 1:2117) into the spermatheca since the high aspect ratio can easily cause buckling of the structure. Although it is known that indeed such long virgae in other earwigs penetrate the spermatheca 34,35 , the insertion and withdrawal mechanisms remain unclear. The geometry and bending stiffness reported here on E. horridum suggest the following penetration mechanism (Fig. 9). ...
... Earwigs would be a great candidate group to unveil the penetration mechanics from a comparative perspective due to their remarkable diversity of the virga and spermatheca morphology and function 25 . In Dermaptera, for example, it is known that the virga of Euborellia plebeja (Dohrn, 1863) (Anisolabididae) is used for sperm removal and that its tip is specialised to rake sperm 34 , whereas the virga tip of Marava arachidis (Yersin, 1860) (Spongiphoridae) is curved and slightly swollen in shape, and the virga may not be used for physical removal of rival sperm 35 . In future studies, they may be candidate species for comparison to Echinosoma species. ...
Article
Full-text available
We unveiled the penile penetration mechanics of two earwig species, Echinosoma horridum, whose intromittent organ, termed virga, is extraordinarily long, and E. denticulatum, whose virga is conversely short. We characterised configuration, geometry, material and bending stiffness for both virga and spermatheca. The short virga of E. denticulatum has a material gradient with the stiffer base, whereas the long virga of E. horridum and the spermathecae of both species are homogeneously sclerotised. The long virga of E. horridum has a lower bending stiffness than the spermatheca. The virga of E. denticulatum is overall less flexible than the spermatheca. We compared our results to a previous study on the penetration mechanics of elongated beetle genitalia. Based on the comparison, we hypothesised that the lower stiffness of the male intromittent organ comparing to the corresponding female structure is a universal prerequisite for the penetration mechanics of the elongated intromittent organ in insects.
... Males of Euborellia spp. directly insert the elongated virga into the female spermatheca during copulation (Kamimura 2000;Lieshout and Elgar 2011). Elongation of the virga (and the genitalia as a whole, which functions as the virgal sheath when in repose) is considered an adaptation for removal of rival sperm from the female spermatheca, which is usually longer than the virga (Kamimura 2000(Kamimura , 2005(Kamimura , 2013(Kamimura , 2015 Lieshout and Elgar 2011). ...
... directly insert the elongated virga into the female spermatheca during copulation (Kamimura 2000;Lieshout and Elgar 2011). Elongation of the virga (and the genitalia as a whole, which functions as the virgal sheath when in repose) is considered an adaptation for removal of rival sperm from the female spermatheca, which is usually longer than the virga (Kamimura 2000(Kamimura , 2005(Kamimura , 2013(Kamimura , 2015 Lieshout and Elgar 2011). Thus, genital elongation in E. janeirensis suggests intensive sperm competition in this species. ...
Article
Full-text available
Based on samples collected during surveys of Brazilian cave fauna, seven earwig species are reported: Cylindrogaster cavernicola Kamimura, sp. n., Cylindrogaster sp. 1, Cylindrogaster sp. 2, Euborellia janeirensis, Euborellia brasiliensis, Paralabellula dorsalis, and Doru luteipes, as well as four species identified to the (sub)family level. To date, C. cavernicola Kamimura, sp. n. has been recorded only from cave habitats (but near entrances), whereas the other four organisms identified at the species level have also been recorded from non-cave habitats. Wings and female genital structures of Cylindrogaster spp. (Cylindrogastrinae) are examined for the first time. The genital traits, including the gonapophyses of the 8th abdominal segment shorter than those of the 9th segement, and venation of the hind wings of Cylindrogastrinae correspond to those of the members of Diplatyidae and not to Pygidicranidae. This is the first synopsis of cave-dwelling earwigs of Brazil, one of the most species-rich areas of Dermaptera in the world.
... Snodgrass, 1935;Tuxen, 1970;Matsuda, 1976). The elongated parts of male genitalia are also quite variable among different groups, but in general their function is to be efficiently inserted into the spermatheca or spermathecal duct of the female and to act as a sperm/spermatophore-transporting organ (Gack and Peschke, 1994;Gschwentner and Tadler, 2000;Kamimura, 2000;Freitag et al., 2001;Matsumura and Yoshizawa, 2010; for exceptions see, e.g., Matsumura et al., 2014;Jałoszyński et al., 2015). Even though in many cases the anatomy has not yet been described in detail, several distinctly different categories of intromittent organs can be distinguished (Matsumura et al., 2014). ...
... In both of the Cassida species studied, the male flagellum is much longer than the female spermathecal duct (Table 1; Filippov et al., 2015). While this phenomenon is common in cassidine species (Rodriguez et al., 2004), in the majority of other beetle taxa with elongated intromittent organs the flagellum lengths are comparable to, or even shorter than, those of the spermathecal duct (Gschwentner and Tadler, 2000;Ilango and Lane, 2000;Kamimura, 2000;Gack and Peschke, 2005;Matsumura and Suzuki, 2008;Matsumura et al., 2014). In C. rubiginosa, whose males have a longer flagellum than those of C. vibex, with more than 70% of the flagellum length remaining outside of the spermathecal duct, such a 'waste of material' is difficult to understand. ...
Article
The peculiar phenomenon of hyper-elongation of intromittent organs is well known in a number of insect groups. However, the unresolved questions of how and why such a phenomenon originated independently many times continue to attract biologists’ attention. To be able to detect the evolutionary driving mechanisms that enabled insects to repeatedly acquire such a peculiarity, first of all the structural key features and the mechanics of these organs have to be determined. In the present study, the morphology of the reproductive organs of two species of the beetle genus Cassida, with a special focus on the male structures, was scrutinised in detail during copulation and at rest using different microscopy techniques. We found that the hyper-elongated structure of the intromittent organ, called flagellum, is part of the male ejaculatory duct. When the flagellum is inserted into the female spermathecal duct, longitudinal muscles of the ejaculatory duct, but not the flagellum, are shortened. These results strongly suggest that the contraction of the longitudinal muscles of the ejaculatory duct causes propulsion of the flagellum into the highly spiralled spermathecal duct of the female. The tip of the cuticular flagellum is curled up, which can suggest that its physical properties differ from those of the rest of the flagellum. Considering the preceding modelling studies, this property aids the flagellum in penetrating within the highly spiralled and very variable female duct. Based on our morphological results and in comparison with the morphology of intromittent organs of other beetles, we discuss the evolutionary origin of the hyper-elongation in the Cassida species and propose a hypothesis that explains the independent origin of the hyper-elongation of intromittent organs.
... The identification of the samples is only tentative, because of the many similar species in the genus that are inadequately described. As in other examined Euborella spp, (Hudson 1973;Kamimura 2000), the spermatheca is a very long, thin, blind duct without a capsule at the distal end (Fig. 68A). In one laboratory-raised male the tegmina were well-developed but hindwings were totally lacking. ...
... The fully winged form of our specimens cannot be distinguished from those of Euborellia plebeja (Dohrn, 1863) (Dohrn 1863b;Srivastava 2003a), warranting further studies of this group. Similar to its close relatives (Hudson 1973;Kamimura 2000), the spermatheca is a very long, thin, blind duct without a capsule at the distal end (Fig. 68B). ...
Article
Full-text available
The earwig (Dermaptera) fauna of Penang Island, Malaysia, was evaluated by means of an extensive field survey together with revision of the few published data. Based on the results of the field survey, 31 species are recognized (2 Diplatyidae, 3 Pygidicranidae, 5 Anisolabididae, 2 Labiduridae, 14 Spongiphoridae, 4 Chelisochidae, 1 Forficulidae). Fifteen of these taxa are new to Peninsular Malaysia (=West Malaysia): Diplatys annandalei Burr, 1911, Diplatys mutiara n. sp., Euborellia philippinensis Srivastava, 1979, Metisolabis punctata (Dubrony, 1879), Pseudovostox brindlei Srivastava, 2003, Chaetospania anderssoni Brindle, 1971, Chaetospania javana Borelli, 1926, Chaetospania huisiangi n. sp., Paralabellula boettcheri (Borelli, 1923), Paralabellula rotundifrons (Hincks, 1954), Nesogaster amoenus (Stål, 1855), Hamaxas crassus Borelli, 1926, Proreus coalescens (Borelli, 1927), Hypurgus humeralis (Kirby, 1891), and an unidentified Echinosoma sp. Species composition of the island are compared with the dermapteran fauna of Thailand. Descriptions of females (or female genitalia) are given for some species for the first time.
... The insect order Dermaptera (earwigs) shows much diversity in the genital structures, including size, number and laterality of both male and female genital components, and the degree of differentiation of female com-ponents, making them valuable study models of genital evolution (e.g., PoPham 1965;Steinmann 1986Steinmann , 1989Steinmann , 1990Steinmann , 1993Kamimura 2000Kamimura , 2004aKamimura ,b, 2006Kamimura , 2007bKamimura , 2013Kamimura , 2014Kamimura & matSuo 2001;KlaSS 2001KlaSS , 2003Kamimura & iwaSe 2010;Schneider & KlaSS 2013). The presence of either a single or a pair of male intromittent organs (penes) is an especially striking feature of earwigs. ...
... Irrespective of the importance for inferring the phylogeny of Dermaptera and its placement in the polyneopteran insect orders, the evolutionary reason how the ancestor of earwigs acquired paired penes has remained unexplained. In anisolabidids such as Anisolabis mar itima (Bonelli, 1832) and Euborellia plebeja (Dohrn, 1863), males have two functionally competent penes although they use only one of them during a single genital coupling (Kamimura 2000;Kamimura & matSuo 2001). Each penis bears an elongated virga, which is a heavily sclerotized process which contains the terminal part of the ejaculatory duct and has the gonopore on its tip. ...
Article
Full-text available
Dermaptera (earwigs) shows much diversity in the genital structures, the presence of either one or two male intromittent organs (penes) being one striking aspect. The members of several groups (Karschiellidae, Eudermaptera, Arixeniina, and Hemimerina) possess a single functional penis, while others have a pair of penes. The latter condition is considered to be plesiomorphic in Dermaptera. Despite its importance for inferring the phylogeny of Dermaptera, it is presently unclear how the ancestor of earwigs acquired paired penes. To estimate the mode of mating and sperm transfer in the common ancestor of extant earwigs, this study examines the mating behavior and genital coupling of the primitive earwig species Echinosoma denticulatum Hincks, 1959 as a representative of Pygidicranidae, one of the basal-most assemblages of earwigs. Staged mating experiments, including surgical manipulation of male penes revealed the following characteristics for this species: (1) males use only one of the paired penes for a single genital coupling; (2) both penes are likely functional; (3) there are no consistent biases in usage of the penes; (4) laterality of the penis-use pattern is not related to the direction of rotation of the male abdomen to establish genital coupling; (5) sperm are transferred directly into the spermatheca, a female sperm storage organ; (6) the spined area of the penis inflicts wounds on the vagina around the spermathecal opening, which bears many setae, during copulation. Characteristics (1)-(4) are considered to be plesiomorphic and may represent the condition of the common ancestor. Traumatic penetration during copulation is reported for earwigs for the first time. Together with intermittent acceptance of courting males by females only after a certain interval, these results suggest sexual conflict over mating in this species.
... The phenomenon of the 'hyper elongation' of insect genitalia is usually discussed in the context of specific intromittent structures of the male reproductive system, e.g., the flagellum in various beetle families (e.g., Gack and Peschke, 2005;Matsumura et al., 2013), the distiphallus in tephritid flies (Eberhard, 2005), the processus gonopori in lygaeid bugs (Gschwentner and Tadler, 2000), the virga of earwigs (Kamimura, 2000(Kamimura, , 2005, the 'flagellum' or 'elongated tube' of Zoraptera (Mashimo et al., 2013;Matsumura et al., 2014), and others (summarized by Matsumura and Yoshizawa, 2012). Such elongated sclerotized structures have various functions, from sperm transfer to removal of a rival sperm from the female reproductive tract, and may play a role in cryptic female choice (e.g., Rodriguez, 1995;Gschwentner and Tadler, 2000;Kamimura, 2000;S. ...
... The phenomenon of the 'hyper elongation' of insect genitalia is usually discussed in the context of specific intromittent structures of the male reproductive system, e.g., the flagellum in various beetle families (e.g., Gack and Peschke, 2005;Matsumura et al., 2013), the distiphallus in tephritid flies (Eberhard, 2005), the processus gonopori in lygaeid bugs (Gschwentner and Tadler, 2000), the virga of earwigs (Kamimura, 2000(Kamimura, , 2005, the 'flagellum' or 'elongated tube' of Zoraptera (Mashimo et al., 2013;Matsumura et al., 2014), and others (summarized by Matsumura and Yoshizawa, 2012). Such elongated sclerotized structures have various functions, from sperm transfer to removal of a rival sperm from the female reproductive tract, and may play a role in cryptic female choice (e.g., Rodriguez, 1995;Gschwentner and Tadler, 2000;Kamimura, 2000;S. Naomi, pers. ...
Article
We compared the postabdominal architecture of Mastigini with extremely long (Stenomastigus) or short (Palaeostigus) aedeagus. A novel mode of copulation was discovered: males of Stenomastigus insert a paramere between the female's abdomen and elytra, and the intromission is stabilized by several structures in both sexes. The intrinsic aedeagal mechanism is indicated as responsible for inflating the endophallus, and the long flagellum does not penetrate the ductus spermathecae during copulation. The structure of the flagellum suggests that it is primarily responsible for the sperm transfer. Asymmetrical postabdominal rotators of the aedeagus were only found in Stenomastigus; they presumably facilitate the withdrawal of the genitalia. Their origin as bunches separated from larger muscles is postulated. We discuss a scenario in which the evolution of elongated genitalia was facilitated by the lack of structural constraints and existing preadaptations. Benefits of stabilizing the copulation and intromission are indicated as the driving force for the evolution of extremely long aedeagi, while the short aedeagi might have the advantage of freedom of movements facilitating the initiation of copulation by males. Disruptive selection is suggested as a working hypothesis to further investigate mechanisms that have played a role in the evolution of genital structures of Mastigini.
... For example, male M. arachidis possess a pair of sclerites in the penis lobe, which forcibly pinch the genital region of the female mates during copulation, resulting in copulatory wounds (Kamimura, et al., 2016). Male Euborellia spp., are known to use the elongated genitalia to remove rival sperm from the tubular spermatheca of the mates (Kamimura, 2000;van Lieshout and Elgar, 2011). Accordingly, the identification of closely related species often requires an examination of the genital morphology by specialist taxonomists. ...
Article
The Dermaptera is a polyneopteran order with > 2,000 described species from mainly tropical, subtropical, and warm temperate regions. More than 310 species of the Dermaptera belonging to nine families have been reported from the Indian subcontinent (India, Pakistan, Nepal, Bhutan, Bangladesh and Sri Lanka) as a result of the extensive work of Gyanendra Kumar Srivastava. Embracing environmental and climatic heterogeneity, the Indian subcontinent is an intersection of multiple faunal regions and includes several dermapteran groups of special interest. To restart the studies on the Dermaptera of this region, which has been stagnant for a decade, this paper includes a beginner’s guide for collecting and identifying Dermaptera, together with a brief summary of recent advances in their classification and phylogeny.
... It occurs in the oldest extant damselfly, Hemiphlebia mirabilis, suggesting that was acquired early in odonate evolution (Cordero-Rivera 2016). Sperm removal has been also demonstrated in Orthoptera (Ono et al., 1989;Helversen & Helversen 2004), Dermaptera (Kamimura 2000) and Coleoptera (Yokoi 1990) and has been suggested in a millipede (Barnett et al., 1993). The function of apyrene/eupyrene sperm is still unclear but is highly likely an adaptation to sperm competition (Watanabe 2016). ...
... The elongated intromittent organs in insects are diversified not only in shape but also in the functional repertoire. They are used, for instance, for penetration + insemination in some beetles, hangingflies and a seed bug [23,26,[55][56][57][58][59][60], for penetration + sperm removal + insemination in the earwig Euborellia plebeja [61], for insemination but not penetration in the beetle Stenomastigus longicornis [62], and for penetration + sperm removal but not insemination in the angel insect Zorotypus caudalli [13]. The functional repertoire may also affect the morphology of male and female copulation organs and the penetration mechanics. ...
Article
Coevolution of male and female genitalia is widespread in animals. Nevertheless, few studies have examined the mechanics of genital interactions during mating. We characterized the mechanical properties of the elongated female genitalia, the spermathecal duct, of the small cassidine beetle, Cassida rubiginosa. The data were compared with the mechanical properties of the elongated male genitalia, the flagellum. We analysed the material distributions of the spermathecal duct using a microscopy technique, established a tensile test setup under a light microscope and conducted tensile tests. Diameter and tensile stiffness gradients were present along the spermathecal duct, but its Young's modulus and material distribution were more or less homogeneous. The results confirmed the hypothesis based on numerical simulations that the spermathecal duct is more rigid than the flagellum. In the study species, the penile penetration force is simply applied to the base of the hyper-elongated flagellum and conveyed along the flagellum to its tip. Considering this simple penetration mechanism, the relatively low flexibility of the spermathecal duct, compared to the flagellum, is likely to be essential for effective penetration of the flagellum.
... By contrast, offensive pre-emption mechanisms to maximise fertilization success focus either on the mechanical displacement of previously deposited sperm from rival males or other means to ensure either the numerical or qualitative precedence of one's own sperm. Examples of mechanical displacement can be found in male crickets, damselflies and dragonflies [13][14][15], who use their genitalia to physically remove or compact the sperm of the female's prior mates before they inseminate her with their own sperm, with similar methods found also in longicorn beetles Psacothea hilaris [16] and the earwig Euborellia plebeja [17]. By contrast, in other insect groups sperm predominance can be achieved by the production of longer sperm [18], more sperm [19] or a higher sperm viability [20]. ...
Article
Full-text available
Background: Studying reproductive trait allometries can help to understand optimal male investment strategies under sexual selection. In promiscuous mating systems, studies across several taxa suggest that testes allometry is usually positive, presumably due to strong selection on sperm numbers through intense sperm competition. Here, we investigated testes allometry in a bush-cricket species, Metaplastes ornatus, in which females mate promiscuously, but where sperm removal behaviour by males likely drastically reduces realised sperm competition level. Results: As hypothesised, we found evidence for negative testes allometry and hence a fundamentally different male investment strategy compared to species under intense sperm competition. In addition, the mean relative testes size of M. ornatus was small compared to other species of bush-crickets. Surprisingly, the spermatophore gland, a potential alternative trait that males could invest in instead of testes, also did not show positive allometry, but was approximately isometric. We further observed the expected pattern of negative allometry for the male morphological structure responsible for sperm removal in this species, the subgenital plate, supporting the one-size-fits-all hypothesis for intromittent genitalia. Conclusion: Our findings suggest that the evolution of sperm removal behaviour in M. ornatus was a key adaptation for avoiding sperm competition, with important consequences for reproductive trait allometries. Nevertheless, they also imply that it does not pay for larger males to invest disproportionately in nuptial gift production in this species.
... In the extreme case of the leaf beetle species Lema coronata, the intromittent organ reaches a length of approximately 10 mm with a diameter of only 2 µm 17 . Nevertheless, these structures are solely used as sperm transferring organs [18][19][20][21][22][23] , with one exception of a zorapteran species, whose elongated intromittent organ is plausibly used only for sperm displacement 15 . However, the mechanisms of sperm transfer through such structures remain unexplored. ...
Article
Full-text available
Many insects possess a hyper-elongated intromittent organ with a diameter of only a few micrometers. Using morphological and theoretical approaches, we investigated the biomechanics of sperm transfer through such organs by calculating (1) how far and how fast sperm could fill in the penis by capillary action, (2) how much capillary pressure is generated in the penis, and (3) how much pressure is needed to pump sperm out of the penis. The results enabled us to propose the following hypotheses: (1) penile filling basically occurs by capillary action, and (2) sperm transport to females occurs by contracting the sperm pump muscles or by active propulsion of spermatozoa. Potential experimental approaches to test these hypotheses are discussed.
... In some cases, the evolution of genitalia may be influenced by the elaborate genital morphologies that are favoured in males for the removal of sperm stored by females from previous matings (Gage, 1992;Kamimura, 2000;Robinson & Novak, 1997;Sekizawa, Goto, & Nakashima, 2019;Waage, 1979). In removing rival sperm, males can avoid sperm competition, which occurs when the sperm from more than one male overlap temporally in the reproductive tract of a female and compete to fertilize her ova (Parker, 1998;Simmons, 2001). ...
Article
Female genitalia have been largely neglected in studies of genital evolution, perhaps due to the long standing belief that they are relatively invariable and therefore taxonomically and evolutionarily uninformative in comparison to male genitalia. Contemporary studies of genital evolution have begun to dispute this view, and to demonstrate that female genitalia can be highly diverse and covary with the genitalia of males. Here we examine evidence for three mechanisms of genital evolution in females: species isolating “lock‐and‐key” evolution, cryptic female choice and sexual conflict. Lock‐and‐key genital evolution has been thought to be relatively unimportant, however we present cases that show how species isolation may well play a role in the evolution of female genitalia. Much support for female genital evolution via sexual conflict comes from studies of both invertebrate and vertebrate species, however the effects of sexual conflict can be difficult to distinguish from models of cryptic female choice that focus on putative benefits of choice for females. We offer potential solutions to alleviate this issue. Finally, we offer directions for future studies in order to expand and refine our knowledge surrounding female genital evolution. This article is protected by copyright. All rights reserved.
... Alternatively, the asymmetrically arranged sensilla might function to sense proper genital coupling with a right-side penis. In E. plebeja, the spermatheca is also elongated to twice the body length (Kamimura, 2000). This structure is considered an adaptation to selectively accumulate sperm from large-sized males, which are capable of repeating partial displacement of the stored sperm using their elongated virgae (Kamimura, 2015). ...
Article
The evolution of laterality, i.e., the biased use of laterally paired, morphologically symmetrical organs, has attracted the interest of researchers from a variety of disciplines. It is, however, difficult to quantify the fitness benefits of laterality because many organs, such as human hands, possess multimodal functions. Males of the earwig Labidura riparia (Insecta: Dermaptera: Labiduridae) have morphologically similar laterally paired penises, only one of which is used for inseminating the female during a single copulation bout, and thus provide a rare opportunity to address how selection pressure may shape the evolution of population‐level laterality. Our population studies revealed that in 10 populations, located at 2.23–43.3° north, the right penis is predominantly used for copulating (88.6%). A damaged penis was found in 23% of rare left‐handers, suggesting that the left penis can function as a spare when the right one is damaged. By pairing L. riparia females with surgically manipulated males, we found that males forced to use the right penis outperformed left‐handed males in copulation (the probability of establishing genital coupling during the 1‐hr observation period: odds ratio of 3.50) and insemination (probability of transferring a detectable amount of sperm: odds ratio of 2.94). This right‐handed advantage may be due to the coiled morphology of the sperm storage organ with a right‐facing opening. Thus, female genital morphology may play a significant role in the evolution of handedness and may have acted as a driving force to reduce penis number in related taxa. This article is protected by copyright. All rights reserved.
... The phylogenetic signal of insect genitalia has been subject to some debate. Polyandry has been found in confamilial species Euborellia plebeja (Dohrn) [114][115][116][117] and Euborellia brunneri (Dohrn) [118], so it is likely that genital morphology is subject to sexual selection. However, the precise function of the parameres is unknown [41] so it is difficult to make definitive statements about the effect of sexual selection on their morphology. ...
Article
Full-text available
Dermaptera (earwigs) from the Anisolabididae family may be important for pest control but their taxonomy and status in Australia is poorly studied. Here we used taxonomic information to assess the diversity of southern Australian Anisolabididae and then applied cox1 barcodes as well as additional gene fragments (mitochondrial and nuclear) to corroborate classification and assess the monophyly of the putative genera. Anisolabididae morphospecies fell into two genera, Anisolabis Fieber and Gonolabis Burr, based on paramere morphology. Combinations of paramere and forceps morphology distinguished seven morphospecies, which were further supported by morphometric analyses. The morphospecies were corroborated by barcode data; all showed within-species genetic distance < 4% and between-species genetic distance > 10%. Molecular phylogenies did not support monophyly of putative genera nor clades based on paramere shape, instead pointing to regional clades distinguishable by forceps morphology. This apparent endemism needs to be further tested by sampling of earwig diversity outside of agricultural production regions but points to a unique regional insect fauna potentially important in pest control.
... The genetic diversity of stored sperm in female sperm storage organs (Siva-Jothy and Hooper 1995), multiple paternity of a clutch of offspring, and last male precedence in reproductive success (Cooper et al. 1996) have been studied in insects using DNA analysis. These results suggest many insects perform sperm displacement by sperm removal (Córdoba-Aguilar et al. 2003;Kamimura 2000Kamimura , 2003. Furthermore, Takami (2007) showed that spermatophore displacement was highly probable by DNA analysis of a spermatophore placed in the female genitalia of a ground beetle. ...
Article
Simultaneous hermaphroditism is, at least initially, favoured by selection under low density — and therefore it can be assumed that sperm competition has little importance in this sexual system. However, many simultaneously hermaphroditic nudibranchs have both an allo-sperm storage organ (the seminal receptacle) and an allo-sperm digesting organ (the copulatory bursa), suggesting the possibility of the occurrence of sperm competition. A nudibranch, Chromodoris reticulata, autotomizes its penis after every copulation and replenishes it within about 24 h to perform another copulation. We observed that the surface of the autotomized penis was covered with many backward-pointing spines and that a sperm mass was often entangled on the spines. This suggests that the nudibranch removes sperm that is already stored in a mating partner’s sperm storage organ(s) with its thorny penis. Using six microsatellite markers, we determined that the sperm mass attached to the penis were allo-sperm originating from individual(s) that had participated in prior copulations. We revealed that C. reticulata performed sperm removal using the thorny penis. These results suggest that competition in fertilization is quite intense and mating frequency in the wild is relatively high in this species.
... In some millipedes, the volume of the second male ejaculate significantly increased within 24 hours after copulation (Cooper, 2015), or the volume of the first male ejaculate significantly decreased during the same period (Barnett et al., 1995). Sperm competition may act as an agent in the shaping of genital structure(s) involved in sperm removal (Kamimura, 2000) and sperm mixing (Barnett et al., 1995;Simmons, 2001). In millipedes, the flagellum can have such a role (Tadler, 1996;Minelli and Michalik, 2015). ...
Article
Full-text available
Sexual selection can be a major driving force that favours morphological evolution at the intraspecific level. According to the sexual selection theory, morphological variation may accompany non-random mating or fertilization. Here both variation of linear measurements and variation in the shape of certain structures can significantly influence mate choice in different organisms. In the present work, we quantified sexual behaviour of the millipede Megaphyllum bosniense (Verhoeff, 1897) as characterized by several sequences. These are: mating latency, duration of copulation, contact to copulation time, duration of contact without copulation, time from entrance (time-point when individuals were placed in boxes in which tests occurred) to contact with copulation, and time from entrance to contact without copulation. Further, we analysed the influence of morphological variation (both variation of linear measurements and variation in the shape of several structures) on mating success. Variation of body length, antennal length, length of the walking legs, trunk width, and trunk height was analysed by traditional morphometrics, while variation in size and shape of the antennae, walking legs, head, and gonopods (promeres, opisthomeres) was analysed using geometric morphometrics. More than half of all physical contacts detected among the millipedes resulted in copulation. Based on the value of sexual selection coefficients, preferences toward the previous partner were found to be prevalent in both female and male choice tests. Individuals with different mating status significantly differed in some morphological traits (body mass, head centroid size, head shape, and promere shape). Our study yielded new information about the sexual behaviour of millipedes and variation of morphological traits as a potential basis for mate preferences.
... In some millipedes, the volume of the second male ejaculate significantly increased within 24 hours after copulation (Cooper, 2015), or the volume of the first male ejaculate significantly decreased during the same period (Barnett et al., 1995). Sperm competition may act as an agent in the shaping of genital structure(s) involved in sperm removal (Kamimura, 2000) and sperm mixing (Barnett et al., 1995;Simmons, 2001). In millipedes, the flagellum can have such a role (Tadler, 1996;Minelli and Michalik, 2015). ...
Article
Full-text available
Sexual selection can be a major driving force that favours morphological evolution at the intraspecific level. According to the sexual selection theory, morphological variation may accompany non-random mating or fertilization. Here both variation of linear measurements and variation in the shape of certain structures can significantly influence mate choice in different organisms. In the present work, we quantified sexual behaviour of the millipede Megaphyllum bosniense (Verhoeff, 1897) as characterized by several sequences. These are: mating latency, duration of copulation, contact to copulation time, duration of contact without copulation, time from entrance (time-point when individuals were placed in boxes in which tests occurred) to contact with copulation, and time from entrance to contact without copulation. Further, we analysed the influence of morphological variation (both variation of linear measurements and variation in the shape of several structures) on mating success. Variation of body length, antennal length, length of the walking legs, trunk width, and trunk height was analysed by traditional morphometrics, while variation in size and shape of the antennae, walking legs, head, and gonopods (promeres, opisthomeres) was analysed using geometric morphometrics. More than half of all physical contacts detected among the millipedes resulted in copulation. Based on the value of sexual selection coefficients, preferences toward the previous partner were found to be prevalent in both female and male choice tests. Individuals with different mating status significantly differed in some morphological traits (body mass, head centroid size, head shape, and promere shape). Our study yielded new information about the sexual behaviour of millipedes and variation of morphological traits as a potential basis for mate preferences.
... Finally, some male strategies do not moderate female behaviour but simply remove the sperm from previous males. For example, male earwig Euborellia plebeja insert their elongated genitalia into the female reproductive tract and remove the stored sperm from the spermatheca (Kamimura 2000). Even though cryptic female choice is difficult to distinguish from other internal mechanisms such as sperm competition, there are some studies that cleverly demonstrate that females select the sperm of preferred males when they mate with multiple males (see Elgar et al. 2000;Schneider et al. 2015). ...
Article
Multiple mating by females is a common phenomenon in nature. Polyandrous females may benefit from genetically diverse progeny that may survive better in a changing environment. Males in polyandrous systems, however, may not achieve their maximum paternity. Therefore, males are predicted to carry traits that prevent or reduce female polyandry. Praying mantids are predatory insects in which females can mate multiple times, predicting the evolution of male counter‐strategies. However, the rate of polyandry and male strategies against polyandry are rarely studied in these insects. In the current study, we used false garden mantids Pseudomantis albofimbriata to quantify the rate of multiple mating when several males are present within close visual range of an unmated female. We further determined how long mated females stay unattractive after mating. We found that in a scramble scenario, the subsequent males stay with a copulating pair and attempt mating once the first male has completed copulation. These second copulation attempts are often successful. If only one male is attracted as a result of the initial pheromone plume, then polyandry is unlikely because the female will remain chemically unattractive for 8 days on average (thus preventing subsequent male attractions), which is longer than the usual latency to lay the first egg sac. From previous studies, we know that single male attraction is the most common scenario in this system in both natural and semi‐natural contexts. Therefore, polyandry depends on the number of males attracted to the initial pheromone plume of the female and is likely to be a relatively uncommon phenomenon in this system.
... Therefore, males have to move the elongated structure for rather long distances to insert the elongated structure from their abdomen into a female duct, which is usually called spermatheca (or spermathecal duct). Although a tunnel-like structure, into which the elongated structure penetrates, is situated in the female, the correspondingly long female structures are convoluted and/or highly coiled (10,(22)(23)(24)(25) and penetration does not appear to be a very simple task for males. In addition, the elongated part of the intromittent organ seems to be very fragile [in an extreme case, its diameter is less than 2 mm (24)]. ...
Article
Full-text available
Hyper-elongated structures and their penetration are widespread among insects, for example, intromittent organs, ovipositors, and piercing-sucking mouthparts. The penetration of thin structures with high aspect ratio without buckling and rupturing is mechanically very challenging. However, this problem is economically solved in nature, and the solutions might be helpful for, for example, in the development of harmless catheters. We focus on the penetration process of a hyper-elongated structure of a cassidine beetle intromittent organ, termed a flagellum. We applied a three-point bending test for the flagellum to measure its bending stiffness along the entire flagellum. We demonstrated the bending stiffness gradient, in which the basal half is relatively stiff and the apical half is softer, whose good performance during copulation had been previously numerically demonstrated. The stiffness gradient is the result of the flagellum shape, which is cylindrical and tapered toward the tip. Moreover, the curved tip comprises a harder outer curve and a softer inner curve. Considering the findings of preceding studies, the flagellum works in the following way: (i) the bending stiffness gradient supports the flagellum, easily fitting to a shape of a highly coiled spermathecal duct, (ii) the stiffness property of the very tip may make the tip tougher, and (iii) the curled tip and homogeneously cylindrical shape of the organ help the very tip to fit the shape of the spermathecal duct of the female. Our study shows that the apparently simple flagellum penetration is achieved with numerous elaborate mechanical adaptations.
... However, some of the materials of A. mordax and A. cerrobarjai studied by Steinmann (1978Steinmann ( , 1979 correspond to immature male specimens. Immature and recently metamorphosed males in the family Anisolabididae show external secondary sexual characters and genital structures characteristically developed, but with a large variability (Jamet & Caussanel 1995, Kamimura 2000, 2007, Kamimura & Iwase 2010, probably a consequence of poor sclerotization. Coloration of tibiae is highly variable in northern African Aborolabis, from solid black to light cream and varies in immature and recently metamorphosed individuals. ...
Article
An update on the taxonomy and geographic distribution of Iberian Anisolabididae (Dermaptera) is provided. Former catalogues reported in the Iberian Peninsula three genera of Anisolabididae: Aborolabis, Anisolabis, and Euborellia. A revision of 487 specimens of Iberian and North African Anisolabidoidea permit to exclude the genus Aborolabis from the Iberian fauna, the re-assignation of inland Euborellia annulipes Iberian records to Euborellia moesta, and the exclusion of Aborolabis angulifera from Northwestern Africa. Examination of type materials of Aborolabis mordax and Aborolabis cerrobarjai allows to propose the treatment of A. cerrobarjai as a junior synonym of A. mordax. The diagnostic characters of Euborellia hispanica are included within the local variability found in E. moesta. I propose that E. hispanica should be treated as a junior synonym of E. moesta.
... In addition to these nomenclatural problems, recent studies have shown that the morphology of earwig virgae, particularly the length, evolves rapidly due to sperm competition, resulting in considerable variation even among very closely related congeners (Kamimura 2000, 2014, Lieshout and Elgar 2011. Therefore, although useful for species diagnosis, generic classification systems based primarily on virgal characteristics (e.g., length, convolution) likely do not reflect accurately the phylogenetic relationships. ...
Article
Full-text available
The pygidicranid earwigs (Dermaptera) of Penang Island, Peninsular Malaysia were re-examined based on material collected in extensive field surveys in 2012–2013 and 2015. Echinosomaroseiventre Kamimura & Nishikawa, sp. n. is described and illustrated, and Cranopygiapallidipennis (de Haan, 1842) is reported from the island for the first time. The taxonomic and nomenclatural problems of the genus CranopygiasensuHincks (1959) [A Systematic Monograph of the Dermaptera of the World. Part II. Pygidicranidae excluding Diplatyinae. British Museum (Natural History)] are also discussed. For the members of the subfamily Pygidicraninae from Indo-Austral and Oriental regions, the system, definitions of genera, and key of Hincks (1959) are followed. The genus Mucrocranopygia Steinmann, 1986 is synonymized with Cranopygia Burr, 1908. A key to the males of small Echinosoma from the Oriental region is provided.
... Because the male genitalia of Spo. semiflavus are extremely long (see Results), a curvimeter (COMCURVE-8, KOIZUMI, Tokyo, Japan) was used to measure the entire length from an enlarged copy of photographs taken under the DIC microscope (to the nearest 8.7-11.1 lm, depending on the magnification: see Kamimura 2000 for details). ...
Article
Full-text available
Ovoviviparity and viviparity have evolved independently multiple times in animals. Although females exhibit extensive parental care of their eggs, (ovo)viviparity has only been reported in a few species of free-living, nonepizoic earwigs. In contrast, to date, all the studied members of families Arixeniidae and Hemimeridae, which live on mammals, are viviparous. We herein report ovoviviparity in the tropical earwig species, Spongovostox semiflavus (Bormans, 1894) (Forficuloidea: Spongiphoridae: Spongiphorinae). We observed that females of this species retain well-developed embryos within the ovaries and then lay them with complete egg envelopes just before hatching. An average of 9.4 embryos concurrently developed in a female’s body. A similar condition has been reported for only one other species Marava arachidis (Yarsin, 1860), in the subfamily Spongiphorinae. Without additional mating, Spo. semiflavus females produced at least three clutches, consisting of an average of nine offspring within a period of 14–27 d. Both Spo. semiflavus and M. arachidis males are characterized by elongated male genitalia that are more than twice as long as their body lengths. Interestingly, elongated male genitalia are also present in the two other spongiphorids for which (ovo)viviparity has been reported. We discuss the causes of the potential convergence of the evolution of the male genital structure and the development of (ovo)viviparity in females.
... Rodriguez 1994Rodriguez , 1995Rodriguez et al. 2004), or males can replace rival sperm using the elongated organ (e.g. Kamimura 2000). However, it is still unclear why such a conspicuous variation of the length evolved. ...
Article
Phylogenetic relationships among major groups of Criocerinae were reconstructed using molecular data (mitochondrial cytochrome oxidase I and 12S rDNA, and nuclear histone 3). The monophyly of Criocerinae was consistently and robustly supported. The Lema group including Lema, Oulema and Neolema was recovered as a clade, with the latter two genera imbedded within Lema. The Lilioceris group was placed as the sister taxon of the Lema group, and the genus Crioceris was identified as the sister taxon of the Lilioceris + Lema groups. The monophyly and/or validity of Mecoprosopus Chûjô, 1951 and the subgenera Lema, Petauristes Latreille, 1829, Quasilema Monrós, 1960, Microlema Pic, 1932, and Bradyceris Chûjô, 1951 were not confirmed. The monophyly of the subgenus Lema except for the type species L. cyanea was supported by molecular and morphological data, and we termed it the cyanella clade. The present molecular phylogeny was compared with previous concepts with respect to the validity of each genus/subgenus. A revision of several genera is necessary. Based on the phylogenic result, the character evolution of the reproductive organs was analyzed. The ancestral states of this character system were parsimoniously reconstructed. Various shapes of the spermatheca were observed in the subfamily. A convoluted spermatheca evolved once, and reversals to the ancestral state took place several times independently. An elongation of a part of the intromittent organ also occurred several times independently. The length of the male and female reproductive ducts, which are in physical contact during copulation, showed a tight positive correlation even after removing phylogenetic effects. This strongly suggests coevolution between the male and female genital length.
... In some families, such as Escadabiidae, the sclerotized base of the pars distalis is wider than the ovipositor, thus making the penetration below the penis tip impossible, in which case sperm deposition would be restricted to the apical section of the ovipositor. This may have resulted in male genitalic structures capable of removing sperm, as has been described in many other arthropod groups with intromittent genitalia (see references in Kamimura 2000). A handful of species in six distantly related subfamilies of Gonyleptidae have evolved a structure that could serve that function, the ventral process (fi gure 13.9). ...
... Priority advantage may arise through numerous mechanisms, including preferential sperm use by the female, stratification of the sperm within the sperm storage, site of the female, or displacement of sperm by a later male. In certain insects, the male genitalia are even specialized to remove active sperm from the female's sperm storage organs, as earwig Euborellia plebeja (Kamimura 2000(Kamimura , 2005 or in several odonates (Córdoba-Aguilar 1999;Córdoba-Aguilar et al. 2003;Eberhard 1996;González-Soriano and Córdoba-Aguilar 2003;Waage 1979). ...
Chapter
Cryptic female choice (CFC) in spiders may involve several mechanisms to bias paternity including early termination of copulation, remating likelihood, and sperm dumping . In Pholcidae , these mechanisms seem to be very common and will be examined in the present chapter. In the Pholcidae Physocyclus globosus , sperm dumping involves an active role of the female. In contrast, in the Pholcidae Holocnemus pluchei , sperm mass ejection during copulation is mainly under male control. In another haplogyne spider, the Oonopidae Opopaea fosuma , females are able to influence male’s chances of rearing their offspring by also exerting CFC by sperm dumping. Among pholcids, rhythmic genitalic movements of the pedipalps (squeezes ) during copulation have been interpreted as genitalic copulatory courtship . Additionally, recent studies have evaluated the possibility that the outcome of male–female copulatory communication affects paternity. Future attention to the behavior of both female and male, and to the possible dialogues during copulation, promises to be a valuable tool in understanding sexual interactions in these spiders.
... The mechanism of sperm removal and the significance of such behaviour had been studied in E. plebeja (Dohrn, 1863) and Mongolabis brunneri (Dohrn, 1864). The males of these species insert the virga into the spermatheca without ejaculating and then extract the rival sperm using a fringe-like projection on the virgal tip while simultaneously ejaculating semen (Kamimura 2000, 2014). Both species studied are highly promiscuous, and, due to multiple matings, their offspring show mixed paternity (Kamimura 2005, van Lieshout & Elgar 2011). ...
Article
Full-text available
Greenhouses in botanical or zoological gardens are home to dozens of species of invertebrates that were introduced alongside plants or potting soil. Our study presents the description of an alien species of earwig, Euborellia arcanum sp. nov., found in tropical greenhouses in Leipzig and Potsdam (Germany) and in Vienna (Austria), including information about its biology in breeding culture. The species was most likely introduced into Europe by way of plants or plant matter from Florida, but the region of its natural habitat is unknown. The sequence of the mitochondrial gene cytochrome c oxidase subunit I (COI) was also evaluated and added to GenBank as a DNA barcode for further identification.
... Furthermore, this rate does not differ between the morphs. The slow transfer rate may be due to the mechanical limitations of extreme genital morphology driven by sexual selection: Extremely long virgae / aedeagi (the male phallus) have been documented in dermapterans (Kamimura 2000;Kamimura 2004). The rate of sperm transfer is likely to be physically limited where this organ is longer and more narrow. ...
... The description of this fact by Waage (1979) opened a new era in sexual selection studies, clearly under the infl uence of the seminal work on sperm competition by Parker (1970). Removing or repositioning rivals' sperm is obviously advantageous for males, and there is no doubt that selective forces (sperm competition, see below) have contributed to the evolution of sperm removal behavior, not only in odonates but other insects as well (Haubruge et al. 1999;Kamimura 2000;Ono et al. 1989;Yokoi 1990; reviewed by Simmons 2001). However, research on genitalic evolution and sexual biology in general (see for example explanations for male postcopulatory behavior by Waage 1984) has been biased or shaped by sperm competition theories, and sexual selection in general , and tests for other selective forces have been rare. ...
... Rodriguez 1994Rodriguez , 1995Rodriguez et al. 2004), or males can replace rival sperm using the elongated organ (e.g. Kamimura 2000). However, it is still unclear why such a conspicuous variation of the length evolved. ...
Article
Full-text available
Phylogenetic relationships among major groups of Criocerinae were reconstructed using molecular data (mitochondrial cytochrome oxi-dase I and 12S rDNA, and nuclear histone 3). The monophyly of Criocerinae was consistently and robustly supported. The Lema group including Lema, Oulema and Neolema was recovered as a clade, with the latter two genera imbedded within Lema. The Lilioceris group was placed as the sister taxon of the Lema group, and the genus Crioceris was identified as the sister taxon of the Lilioceris + Lema groups. The monophyly and/or validity of Mecoprosopus Chûjô, 1951 and the subgenera Lema, Petauristes Latreille, 1829, Quasilema Monrós, 1960, Microlema Pic, 1932, and Bradyceris Chûjô, 1951 were not confirmed. The monophyly of the subgenus Lema except for the type species L. cyanea was supported by molecular and morphological data, and we termed it the cyanella clade. The present molecular phylog-eny was compared with previous concepts with respect to the validity of each genus/subgenus. A revision of several genera is necessary. Based on the phylogenic result, the character evolution of the reproductive organs was analyzed. The ancestral states of this character system were parsimoniously reconstructed. Various shapes of the spermatheca were observed in the subfamily. A convoluted spermatheca evolved once, and reversals to the ancestral state took place several times independently. An elongation of a part of the intromittent organ also occurred several times independently. The length of the male and female reproductive ducts, which are in physical contact during copulation, showed a tight positive correlation even after removing phylogenetic effects. This strongly suggests coevolution between the male and female genital length.
... , and it is used to remove rival sperm in an anisolabidid earwig (Kamimura, 2000). In a chrysomelid beetle, it was identified as an indicator of cryptic female choice (Rodriguez, 1995;Rodriguez et al., 2004), which comprises a part of female choice occurring after the initiation of the copulation (Thornhill, 1983;Eberhard, 1996). ...
Article
A very unusual genital apparatus of a species of the enigmatic insect order Zoraptera is described. It contains a unique configuration of two different intromittent organs, one of them coiled, very narrow, and strongly elongated. Hyper elongated genitalia are known in different groups of insects. Males have to accommodate these unwieldy structures in the limited spaces of the abdomen and manipulate them acutely during copulation. A crucial question is how species with elongated genitalia cope with these requirements? To elucidate this, we investigated key features enabling storage, insertion and withdrawal of the elongated genitalia in Zorotypus caudelli. The genital anatomy and fitting during copulation of the tiny insects (ca. 2 mm) was reconstructed. The co-existence of an elongated very narrow tube and a bulky spermatophore is a highly unusual and apparently paradox condition. However, we demonstrate that the tube is not involved in sperm transmission, but that the large spermatophore is transferred to females by a membranous fold of the genitalia. The movement of the spermatophore is caused by hemolymph pressure, which likely also promotes the insertion of both intromittent organs. A comparison with the genital anatomy and reproductive mode in related groups suggests that the elongated tube and its accommodating pouch is a de novo structure of some zorapteran species, and that the ancestral sperm transport via spermatophore is a preadaptive condition for the acquisition of this unusual structure.
... Direct removal of sperm from the female reproductive tract by means of male specialized genital structures is a widespread mechanism in Odonata (Córdoba-Aguilar & Cordero-Rivera, 2008;Córdoba-Aguilar et al., 2003), although it has been observed in several other orders of insects, such as the Dermaptera, Orthoptera and Coleoptera (Haubruge et al., 1999;Helversen & Helversen, 1991;Kamimura, 2000;Ono et al., 1989;Yokoi, 1990), and even in a cuttlefish (Wada et al., 2005), which suggests this might be a widespread phenomenon. Before sperm transference is achieved, male odonates remove rival ejaculates stored by the female from previous matings (Cordero & Miller, 1992;Waage, 1979). ...
Article
Full-text available
It has been hypothesized that sperm removal ability in male Odonata (damselflies and dragonflies) has promoted sexual conflict over the sperm stored in the reproductive tract of the female. Although there is evidence supporting this hypothesis, most studies have been conducted in a small number of species from specific families. We explored sperm removal ability in the Antillean Megapodagrionidae, Hypolestes trinitatis through examination of specialized structures on the genital ligula (“penis”) and through measurement of sperm volumes stored in the sperm storage organs (bursa copulatrix and spermathecae) at different stages of the copula. Males removed sperm from the bursa, but not from the spermathecae. The penis has four finger-like terminal processes covered by spines which could contribute to sperm removal. Given the width of the penile processes, males could introduce them into the spermathecae to remove sperm; however this does not seem to occur. A possible explanation for the sperm removal pattern of H. trinitatis could be that the penile processes are prevented to reach the sperm stored due to their position in relation to the spermathecae during the copulation.
... The morphology of male genitalia is important to understanding the proximal factors in the displacement of sperm and spermatophores. In earwig Euborellia plebeja (Dohrn, 1863) (Dermaptera: Anisolabididae), the extension of male genitalia plays a crucial role in sperm replacement (Kamimura 2000). In S. perforata, the apical part of the male genitalia is usually hidden inside the basal part. ...
Article
Silphinae (Coleoptera: Silphidae) is an abundant decomposer that plays important roles in the ecosystem. However, there is little information about the life history of this taxon. We found sperm displacement behavior in carrion beetle Silpha perforata. Copulating males bit the female's antenna strongly and inserted the penis into the partner's genital organ more than once. We found a white substance on the tip of penis during copulation. We examined whether this white substance is a previous male's spermatophore, which was removed from the mating partner. When females were dissected just after mating, the same substance that often presents on the penis of mating males was found in the bursa copulatrix of females, although the bursa copulatrix of virgin females was empty. Male behavior during copulation with females of different mating history was also observed to confirm that the removal of spermatophores was observed only in copulation with females that have the spermatophores of previous males. Consequently, we estimated that S. perforata males removed spermatophores of previous males from mating partners. In addition, we dissected the males frozen during copulation, and inspected the penis morphology. This observation revealed that the apical part of the penis was usually hidden in the basal part of penis, but expanded and appeared during insertion. This apical part had many spines, which play an important role in sperm displacement and sexual conflict in some species. These results indicate that there is the sperm competition in S. perforata. This is the first report on sperm competition in Silphinae.
... While copulations terminated through harassment lasted longer than self-terminated copulations, both were dramatically reduced compared to situations without harassment ( van Lieshout 2010), suggesting many self-terminated copulations were instead failed attempts. In turn, the reduction in mating duration caused by harassment may prevent the transfer of ejaculate altogether since sperm transfer may be preceded by a sperm removal phase which, in a congener, lasts more than 1 min (Kamimura 2000). Since this pattern of mating is likely to be suboptimal for both contestants, this raises the question which of the contestants will persist longer. ...
Article
The act of mating may render individuals vulnerable by inhibiting mobility and defence. While the consequences of this vulnerability for predation risk are well known, the implications for male-male contests over mating have been largely ignored. We examined the influence of vulnerability during mating by assessing the effectiveness of asymmetries in resource-holding potential (RHP) and subjective resource value (female mating status) in determining access to females in a resident-intruder scenario. In the earwig Euborellia brunneri, mating males are vulnerable to attack because they cannot use their armaments, and may risk breakage of their extremely elongated intromittent organs. We expected agonistic outcomes and 'ownership' of females to be decided entirely according to imposed asymmetries, since defeat normally induces a strong loser effect and flight responses in losers. Using behavioural assays of dyads of males contesting one female we show that, although small differences in RHP strongly affected agonistic outcomes, dominant males could not monopolize females. Through recurrent harassment, subordinate males exploited the vulnerability of mating opponents to break up copulations and generate mating opportunities. Dominant males also employed this tactic and were more effective at it. While female mating status affected resident mating duration and investment in conflict, only asymmetry in RHP affected fighting and mating outcomes. Resource owners in E. brunneri hence experience a positional disadvantage specific to a mating context. This previously unrecognized phenomenon may provide a proximate explanation for the taxonomically widespread occurrence of attacks during copulation and the avoidance thereof. (C) 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
... Next, we questioned whether the spinula had the potential to manipulate a rival spermatophore during copulation or to prevent female remating. The use of elaborate genital parts for sperm displacement is known in several insect taxa (Waage, 1979;von Helversen and von Helversen, 1991;Yokoi, 1992;Haubruge et al., 1999;Shigemura and Naito, 1999;Kamimura, 2000;Tsuchiya and Hayashi, 2008;Sumitomo et al., 2011). The spinula of C. clathratus was positioned at the base of the intromittent organ, and was attached near the opening of the vagina throughout copulation. ...
Article
The morphologies of male genitalia often appear harmful or aggressive, as if they may inflict physical damage upon females during copulation. Such male genitalia are often thought to function in intra- and intersexual interactions during mating. In the carabid genus Carabus, division Spinulati, males possess a spine (spinula) on the intromittent organ, of which function is unknown. To reveal the function of the spinula, we studied the mating behavior and genital coupling of a Spinulati species, Carabus (Limnocarabus) clathratus. The males positioned the spinula along the inner wall of the vaginal opening throughout copulation. This placement created a small dent and subsequently a melanized patch (wound) on the vaginal wall, but the spinula rarely penetrated the vaginal wall. The spinula did not reach the innermost part of the vagina where the spermatophore is deposited. These results suggest that the spinula is not used for inflicting damage on female genitalia or manipulating spermatophores of rival males. During spermatophore formation, the male partially withdrew the aedeagus, and only the aedeagal tip and endophallus remained within the female. By placing the spinula against the vaginal wall, the male could hold the endophallus within the vaginal chamber in the unstable copulatory posture. Thus, our observations suggest that the spinula primarily functions as an "anchor" to maintain the coupling of the male and female genitalia and thereby ensure insemination.
Article
Females of social Hymenoptera mate only at the beginning of their adult lives and produce offspring until their death without additional mating. In most ant species, queens live for over a decade, indicating that ant queens can store large numbers of spermatozoa throughout their long lives. Because morphology of the spermatheca (sperm storage organ) in ant queens is very unique among social Hymenoptera, this organ should be important for long-term sperm storage mechanisms in ants. Sperm cells are immotile in the spermatheca of queens at 5 years after mating. This may be effective to maintain a low metabolic activity of spermatozoa that prevents cellular damage and inhibits reactive oxygen species production. The immotile spermatozoa begin to swim when they are exposed to PBS buffer. This indicates that spermatozoa do not lack flagellum functions and continue to survive even after storage for 5 years. Sperm morphology of ants is similar to that of other hymenopteran species, however differences of the cellular characterization is still unknown (e.g. tolerance to oxidative stress) . Highly expressed genes in the ant spermatheca relative to those in body samples have been identified. The genes identified include those encoding antioxidant enzymes, chaperones, and energy metabolism enzymes as well as novel genes that have no similar sequences in the public databases. In future study, it should be necessary to identify the genes responsible for the sperm longevity in ant queens and shed light on molecular and cellular mechanisms of the long-term sperm storage.
Article
Cryptic female choice (CFC) does not necessarily involve discriminative responses in the female nervous system to sperm from multiple mates. Even without any active sperm-choice mechanisms, polyandrous females can gain genetic benefits by having an arena in which genetically superior sperm are “automatically” sorted. In this chapter, possible mechanisms in this CFC category, termed “indirect CFC ,” are reviewed. A simple theoretical model is developed to examine the hypothesis that females obtain genetic benefits by allowing only partial displacement of stored sperm by subsequent mates. The model predicts that such restricted sperm displacement automatically grants genetic benefits when genetically superior males copulate more times per encounter with the female than less fit males. The promiscuous earwig species, Euborellia plebeja , provides an empirical example of this type of indirect CFC. The elongated female sperm-storage organs allow only partial removal and displacement of stored sperm by shorter male genitalia, resulting in a 20 % gain in paternity per mating. In staged mating trials, large males dominated male–male competition for burrows housing females, resulting in a significant increase in paternity by repeated matings with the same female. A numerical simulation based on this mating pattern showed that restricted sperm displacement (~20 % per mating) is optimal for females to accumulate sperm from larger males. Given that male body size is heritable, females were estimated to gain a 1.4 % increase in their sons’ mating success as a genetic benefit. Advantages and disadvantages of indirect CFC are discussed and compared with precopulatory mate choice and direct CFC.
Article
Females of the swallowtail butterfly Papilio xuthus L. (Lepidoptera: Papilionidae) mate multiply during their life span and use the spermatophores transferred to increase their longevity as well as fecundity. Sperm from different males may be stored in the sperm storage organs (bursa copulatrix and spermatheca). To clarify the pattern of sperm storage and migration in the reproductive tract, mated females are dissected after various intervals subsequent to the first mating, and the type and activity of sperm in the spermatheca are observed. When virgin females are mated with virgin males, the females store sperm in the spermatheca for more than 10 days. Sperm displacement is found in females that are remated 7 days after the first mating. Immediately after remating, these females flush out the sperm of the first male from the spermatheca before sperm migration of the second male has started. However, females receiving a small spermatophore at the second mating show little sperm displacement, and the sperm derived from the small spermatophore might not be able to enter the spermatheca. Females appear to use spermatophore size to monitor male quality.
Thesis
Full-text available
In most animals, males are assumed to have access to an unlimited supply of sperm, while females produce few eggs that are large and costly to produce. In parasitoids, there is a paradigm to the effect that males are polyandrous, inseminate as many females as possible and express no optimization in their behaviours. In reality, sperm production incurs non-trivial costs. Because sperm are transferred in ejaculates and that their cost is greater than that of individual sperm, males can gain by carefully allocating their ejaculates. In this thesis I have investigated different aspects of males’ reproductive strategies, mainly sperm and time allocation, in the egg parasitoid Trichogramma turkestanica Meyer (Hymenoptera: Trichogrammatidae). In T. turkestanica, mating mainly occur on the emergence patch. However, results show that mating opportunities are not distributed equally among males and 2.9% of successful males are sperm-depleted when they disperse from the emergence patch. Nevertheless, 97.1% of males disperse non sperm-depleted, suggesting off-patch mating potential. Male T. turkestanica have thus an insemination capacity higher than necessary to inseminate the females present on the emergence patch, a pattern that seems to be common among parasitic wasps. On the emergence patch, both virgin and mated females can be encountered. Males are able to discriminate between those mates and prefer virgin ones. This preference is stronger for energy- and time-limited males. Sperm competition risks and/or intensity are important for males that decrease their sperm investment when the number of rivals increases. Such response is optimal when the benefits from investing more sperm become lower than the costs of a low paternity assurance under intense sperm competition. Finally, male T. turkestanica express behaviours enabling them to optimize their patch time exploitation. Depending on their evaluation of the patch quality, males modify their patch residence time. This thesis shows that time- and sperm-limited male T. turkestanica are not simply maximizing the number of females inseminated, but rather maximize their lifetime fitness by optimizing sperm and patch time allocation.
Article
The hypothesis that the elaborated genitalia of male insects serve to improve insemination success were tested using the ground beetle Carabus insulicola. To enhance variation in genital size, the genital hooks of experimental males were cut, and these males were then mated with virgin females. Logistic regression showed that the length of the male genital hook affected insemination success. Males with a shorter genital hook tended not to deposit spermatophores at the proper site, and failed to transfer sperm into the spermatheca. Therefore, the male genital hook serves to increase insemination success by depositing a spermatophore at the site where sperm are likely to be transferred. The duration of copulation and post-copulatory guarding may also be explained by these determinants. Stepwise regressions indicated that the occurrence of ejaculation, and the location of the spermatophore determined the duration of copulation and post-copulatory guarding, respectively.
Article
Forficulina, the largest suborder of Dermaptera (earwigs), has eight families. In five families (Pygidicranidae, Diplatyidae, Anisolabididae, Apachyidae, and Labiduridae), the males have two penises, whereas the males of the other three families (Spongiphoridae, Chelisochidae, and Forficulidae) have a single penis. Several cladograms have been proposed for Forficulina. However, those systems are constructed mainly from observations of male genital morphology and outstandingly inconsistent. This study reconstructed an earwig phylogeny with representatives of seven families (excluding Apachyidae) by using partial sequences of the mitochondrial 16S and nuclear 28S rRNA genes, sequences that are independent of genital evolution. To avoid difficulties caused by outgroup-rooting for a deep phylogeny, ingroup relationships were first established as unrooted trees based on the 16S, 28S, and combined data sets. The resulting affinities of the earwig families supported several superfamilies, such as Forficuloidea (single-penis families) and Pygidicranoidea (Pygidicranidae + Diplatyidae). Inclusion of the outgroup (Glylloblattodea and Blattodea) did not distort the established ingroup relationships. However, the root position varied according to the genes and outgroup taxa used. Kishino–Hasegawa tests based on the maximum likelihood criterion suggested that the common ancestor of contemporary Forficulina had twin penises, each with one gonopore.
Article
Earwigs (Insecta, Dermaptera) show astonishing diversity in penis morphology. In several families, males have a single penis (termed virga), whereas males of other families possess two functional virgae. Taxonomists have assumed that the two-virgae state is ancestral; however, ecological reasons why the ancestor acquired two virgae have not been explored. This study investigated in detail male and female genital structures, mating behaviour and insemination processes in the earwig Diplatys flavicollis (Diplatyidae). Diplatyidae are considered to be the most primitive family of earwigs. SEM and light-microscopy revealed that males of this species have two gonopores on each of two virgae, similar to those reported in other diplatyids (i.e. two double-barrelled penises), while females have four to six independent sperm-storage organs (spermathecae). Rapid fixation of mating pairs and insemination success of males from which one virga had been removed clearly revealed that only one virga was used for mating and was usually sufficient for inseminating multiple spermathecae. This finding rejects the one-to-one correspondence between male gonopores and female spermathecae. Based on allometric analysis of spermathecal variation, the possible significance of multiple spermathecae in relation to sperm-storage strategies of females is discussed. Compared to studies of male genital morphology, few studies have described spermathecal morphology. Based on compiled data of spermathecal and virgal morphology among earwigs, a parallel evolutionary trend between spermathecae and virgae from complicated (multiple) to simple (single) ones is suggested, and further investigation of the phylogeny, female genital morphology and insemination processes among earwigs is encouraged.
Article
Male genitalia show several evolutionary characteristics, including rapid morphological divergence between closely related species and low within-species phenotypic variability. In addition, genital asymmetry is widespread despite the essentially bilaterally symmetric external morphology of insects. Several hypotheses, such as sexual selection and lock-and-key hypotheses, have been proposed to explain these characteristics of genital evolution. Although these hypotheses provide different predictions about the genetic basis of variation in genitalia, detailed quantitative genetic studies have been conducted in only three insect taxa: heteropterans, dung beetles (Scarabaeidae), and drosophilid flies. For an anisolabidid earwig, Euborellia plebeja, characterized by paired elongated intromittent organs, we estimated the heritabilities and genetic correlations of genital laterality, size of genitalia, and body size. No statistically significant additive genetic, dominance, maternal, or common environmental effects were detected for genital laterality (readiness to use either the left or the right intromittent organ). This result lends further support to the general rule that the direction of antisymmetric variations is randomly determined by non-genetic factors. Irrespective of the restricted phenotypic variation in genitalia compared with body size (allometric slope < 1), as observed in previous studies for other insects, these two traits showed a similar level of genetic variation, measured as the narrow sense heritability (h2) and the coefficient of additive genetic variation (CVA). Comparison suggests the causes of interspecific differences in genetic variability/correlation structures were developmental processes (holo- or hemimetabolous) and/or mode of sexual selection. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 103–112.
Article
The present study shows that females of Silhouettella loricatula (Arachnida: Araneae: Oonopidae) manage to process sperm in an unusual and previously unknown way. The male ejaculate consisting of spermatozoa and globular secretion is enclosed in a secretory sac. This may avoid the mixing of sperm from different males and at least severely limit sperm competition. The process of sperm enclosure occurs within the female's sperm storage site (receptaculum) as the ejaculate is not surrounded by a sac inside the male's sperm-transferring organs (palpal bulbs). The secretion forming the sac is produced by glands adjoining the receptaculum. The possibility that globular secretions in the male palpal bulbs partly contribute to the sac cannot be ruled out completely. It is suggested that in S. loricatula, the main function of sperm enclosure in a sac is enabling females to dump the ejaculate of a male. The present study represents the first report on sperm dumping in the family Oonopidae. During five first and three second copulations in the laboratory, the dumping of a sac was observed. One dumped sac was sectioned and contained spermatozoa. Two couples were flash-fixed with liquid nitrogen early during copulation, which revealed the mechanism of the sac dumping. By muscle contractions, the receptaculum is bent backwards and the sac moved into the genital opening. The actual sac dumping occurs most probably in cooperation with the male, which moves his pedipalps rhythmically during the entire copulation. Extensions and furrows on the emboli suggest that they may additionally be used as copulatory courtship devices. The enclosure of sperm from the current male in secretion takes place during or immediately following copulation as all mated females sacrificed after copulation had a new sac containing spermatozoa in the receptaculum. Dumping sperm of a previous male during the next copulation may allow females to bias sperm precedence.
Article
Full-text available
Based on breeding cultures various behaviours, reproductive biology including maternal brood care, and nymphal development were studied in the basal dermapteran Tagalina papua de Bormans, 1903 (Pygidicranidae s.str.). Supplementary observations were made on T. burri Hincks, 1955, Paracranopygia siamensis (Dohrn, 1863) (Pygidicranidae s.str.), and an unidentified species of Diplatyidae. T. papua specimens did not display any courtship behaviour. In egg deposition gonapophyses VIII are used as a guiding device for the proper placement and upright positioning of the eggs. Eggs are fixed to the substrate in Tagalina, Paracranopygia, and the diplatyid, probably using secretions from the true accessory (colleterial) glands, which have been retained in most basal Dermaptera. Consequently, eggs cannot be transported and piled up, which in other Dermaptera is an important component of brood care. Brood care in T. papua consists in the association with and defense of eggs and 1st instar nymphs and the occasional control of the eggs by the mouth parts, but no egg cleaning was observed. Brood care is thus less ela-borate than in all examined higher Forficulina. Arguments are provided why this simple pattern is plesiomorphic for Dermaptera. Due to the low complexity of behavioural patterns shared between Embioptera and the basal dermapteran T. papua, homology of brood care in Dermaptera and Embioptera is only weakly supported. T. papua almost consistently has six nymphal instars, which are here described. This is in contrast to conditions in higher Forficulina, where Anisolabididae and Labiduridae usually have five nymphal instars and Eudermaptera usually have four. However, due to occasional exceptions and intraspecific variation the number of nymphal instars does not yield autapomorphies in support of monophyletic higher Forficulina or Eudermaptera. Problems in the counting of nymphal instars in Dermaptera are discussed, with particular reference to the embryonic cuticle and its egg tooth, but a solution of this issue requires further data.
Article
Full-text available
The genitalia of 30 females and 30 males in Paralabella dorsal is were dissected and drawn using a camera lucid. Between 10 and 20 min from the initiation of copulation 20 pairs were frozen with ethylchloride, and the females were then dissected immediately to determine the location of male genitalic parts. The male genitalia consist of a subcylindrical penis with a single medial distal lobe, ornamented areas with sclerotized spines in the mid section. The cloacal opening of the female is simple with spines surrounding the gonopore. The spermatheca is a thin coiled tube. During copulation part of the male genitalic teeth reach the sclerotized female spines. The tip of the virga reaches the opening of the spermatheca, were sperm deposition occurs.
Article
Full-text available
Competition between different males' sperm for the fertilization of ova has led to the evolution of a diversity of characters in male reproductive behaviour, physiology and morphology. Males may increase sperm competition success either by enhancing the success of their own sperm or by negating or eliminating the success of rival sperm. Here, we find that in the flour beetle Tribolium castaneum, the second male to mate gains fertilization precedence over previous males' sperm and fertilizes approximately two-thirds of the eggs. It is not known what mechanism underlies this pattern of last-male sperm precedence; however, the elongate tubules of the female sperm storage organ may encourage a 'last-in, first-out' sperm use sequence. Here we present an additional or alternative mechanism of sperm precedence whereby previously deposited sperm are removed from the female tract by the mating male's genitalia. In addition to providing evidence for sperm removal in T. castaneum, we also show that removed, non-self sperm may be translocated back into the reproductive tracts of new, previously unmated females, where the translocated sperm go on to gain significant fertilization success. We found that, in 45 out of 204 crosses, sperm translocation occurred and in these 45 crosses over half of the offspring were sired by spermatozoa which had been translocated between females on the male genitalia. In the natural environment of stored food, reproductively active T. castaneum adults aggregate in dense mating populations where copulation is frequent (we show in three naturally occurring population densities that copula duration and intermating intervals across three subsequent matings average 1 to 2 min). Selection upon males to remove rival sperm may have resulted in counter-selection upon spermatozoa to survive removal and be translocated into new females where they go on to fertilize in significant numbers.
Article
Full-text available
The male of Calopteryx maculata (Beauvois) (Odonata) uses its penis not only to transfer sperm to the female but also to remove sperm deposited in the female's sperm storage organs from previous matings. Apparently, no such sperm removal function has previously been attributed to the intromittent organ of any animal.
Article
The copulation process of a longicorn beetle, Psacothea hilaris consists of two successive events; frequent, short-time penis insertion (first stage) and a single long-time insertion (second stage). It was found that number of sperm stored in the Spermatheca decreased to about 2% of that of control females (which had mated only once), when the second males did first stage copulation without ejaculation. Second males discharged their rivals' sperm during first stage copulation. Scanning microscopic observations showed that the distal portion of the penis had a triangular process and pointed micro-bristles. Sperm displacement in this species is suggested by our observation of the removal of rival sperm by these characteristic structures on the penis. © 1990, JAPANESE SOCIETY OF APPLIED ENTOMOLOGY AND ZOOLOGY. All rights reserved.
Article
The functional morphology of the male and female organs of reproduction of the Common earwig (Forficula auricularia L.) are described together with typical examples of the external male genitalia of most sub-families of the order. Evolutionary trends involve a gradual reduction in the number of penis lobes from two to one; a process which seems to have taken place several times within the Dermaptera. A natural classification of the Dermaptera is suggested in the light of these data.
Article
Sperm removal in Tenebrio molitor L. (Coleoptera: Tenebrionidae) has been proposed as an adaptation to sperm competition and has been documented when the remating interval between successive copulations is short, but not when it is long (Gage, 1992). If sperm removal is adaptive, it follows that there should be different fertilization outcomes from double matings with different remating intervals. Sperm precedence patterns were assessed using reciprocal double matings of normal and γ-irradiated (sterile) virgin males of controlled size and age with virgin females of controlled size and age. Immediate last male sperm precedence was high whether the remating interval was short (<10 min) (P2,= 0.89) or long (24h) (P2= 0.92). Sperm precedence in eggs laid in a 16-day period after the last copulation showed no difference in the pattern of change between females with short and long remating intervals. By examining the aedeagus of males we show that sperm are removed at the end of copulation by the first and the second male to mate with a virgin female regardless of whether the remating interval is short or long. We conclude that sperm removal is unlikely to be the primary mechanism by which males gain such high levels of last male sperm precedence.
Article
A novel combination of adaptations resulting from sperm competition is demonstrated for the tree cricket Truljalia hibinonis (Matsumura) (Podoscirtinae: Gryllidae: Orthoptera). 87.5% of the semen of previous males is displaced onto the penis of the copulating male and is removed at the end of copulation. Semen thus removed is ingested during post-copulatory oro-genital grooming. No overt morphological adaptations for sperm removal were observed and, on the basis of anatomical evidence, it is suggested that rivals' semen is flushed out of the female?s sperm storage organ by the semen of the last male.
Article
The mechanism by which sperm are transferred from the male's spermatophore to the female's storing cage is described for the rove beetle Aleochara curtula, emphasizing a novel mechanism of sperm displacement by competing males. The cuticular, U-shaped spermatheca is equipped with a valve structure and two sclerotized teeth. The tube of the spermatophore extends into the spermathecal duct through the guidance of the flagellum of the male endophallus. Further elongation of the spermatophore tube, however, occurs only after separation of the pair. A primary tube bursts at its tip after passing through the valve. Within the lumen of the primary tube, a second tube passes through the valve and continues to extend up to the apical bulb of the spermatheca, doubles back on itself and swells to form a balloon filling most of the spermatheca. The balloon of the spermatophore is pierced within the spermatheca by tooth-like structures pressed against the spermatophore through contraction of the spermathecal muscle. The same process of spermatophore growing and swelling is also observed in mated females. Sperm from previous copulations are backflushed through the valve and the spermathecal duct, indicative of last-male sperm predominance.
Article
Mating in the bushcricket Metaplastes ornatus Ramme 1931 entails a number of peculiar genital couplings that precede the transfer of the large spermatophore. During these phase-I couplings, the male introduces his specially structured subgenital plate into the female's genital chamber, performs back-and-forth movements, and turns her genital chamber inside out when he withdraws, whereupon the female carefully cleans her everted genital chamber with her mouthparts. During the last coupling (phase II) the male's subgenital plate is not introduced but the large spermatophore, which averages 22% of a male's body weight, is transferred. Counts of sperm in the spermathecae of females suggested that the phase-I couplings, which occur prior to spermatophore transfer, function to remove, or at least to reduce, the sperm of a female's previous mates. The form of the keel of the male's subgenital plate, its position within the female's genital tract during phase-I couplings, and the back-and-forth movements suggest that the male may stimulate release of sperm from the female's spermatheca by a mechanism similar to fertilization as eggs pass through the genital chamber during oviposition.
Article
Positive intraspecific allometry, the tendency for large individuals to have relatively larger morphological traits, is thought to be more likely for secondary sexual traits than naturally selected traits. This is because secondary sexual traits are often used to signal individual quality and positive allometry should arise where the costs and/or benefits of signalling are size dependent. Here we examine the allometric relationships between forceps length, a sexually selected trait and elytra length, a naturally selected trait, in 42 species of earwig. Both forceps and elytra showed positive allometry. However, the degree of allometry was greater for forceps as predicted. If allometry arises due to sexual selection we would predict a greater degree of allometry in species with more exaggerated secondary sexual traits. Across species, the degree of forcep allometry did increase with forcep exaggeration. The relevance of positive allometry to reliable signalling is discussed.
Article
Demonstrations of the mechanism of sperm displacement as a means of sperm competition have been restricted to the order Odonata. From those studies it appears that male and female genital structure plays an important part in sperm competition.A survey is presented here of the female genitalia of several species of libellulid dragonfly. Histology, fine structure and anatomy are described; there is considerable intergeneric variation in the morphology of the organs of sperm storage, but uniformity in the histology, musculature and sensory structures which have been examined. Possible reasons for the variation are discussed.
Chapter
The chapter focuses on the understanding of the mechanisms of sperm competition, which are essential for interpreting nonrandom patterns of paternity and for predicting the types of adaptations that sperm competition can generate. P2 values are often used to infer the mechanism of underlying patterns of sperm utilization: intermediate values are taken as indicative of sperm mixing while higher values of P2 are taken as evidence for sperm precedence or sperm displacement. The bimodal distribution of P2 values seen in Lepidoptera is an excellent example of how little the mean value of P2 can tell us about the patterns of sperm competition. Patterns of sperm competition can change markedly with changes in the intervals between copulations. It is clear that males can adjust the numbers of sperm ejaculated into females, depending on female quality and/or the risks of sperm competition. Thus, patterns of sperm utilization depend on the behavior of males. Alternatively, they also depend on the responses of females to males that vary in their quality as mates. Variation in the numbers of sperm inseminated into the female prior to the final mating can have marked effects on the patterns of sperm utilization.
On the male genital armature of the Dermaptera Part 1: Protodermaptera (except Psalidae)
  • M Burr
Burr, M. 1915a. On the male genital armature of the Dermaptera Part 1: Protodermaptera (except Psalidae). J R mics Soc 1915: 413-447.
On the male genital armature of the Dermaptera Part 3: Eudermaptera
  • M Burr
Burr, M. 1916. On the male genital armature of the Dermaptera Part 3: Eudermaptera. J R mics Soc 1916: 1-18.
Rates of evolution in the Dermaptera
  • E J Popham
Popham, E. J. 1969. Rates of evolution in the Dermaptera. Entomologist 102: 75-79.
The mechanism of sperm displacement in the turnip sawfly, Athalia rosae (Hymenoptera: Tenthredinidae)
  • T Shigemura
  • T Naito
Shigemura, T. and T. Naito. 1999. The mechanism of sperm displacement in the turnip sawfly, Athalia rosae (Hymenoptera: Tenthredinidae). Entomological Science 2: 61-65.