Functional morphology of the copulatory system of box crabs with long second gonopods (Calappidae,Eubrachyura, Decapoda,Crustacea)

Male True Crabs use two pairs of gonopods to deliver mating products during copulation. Commonly, the second pair is shorter than the first pair, and most research to date has focused on species with short second gonopods. We investigated male and female copulatory organs in Calappula saussurei and Calappa pelii, two species of box crabs (Calappidae) with second gonopods which are longer than the first pair. Scanning electron microscopy and histological cross sectioning show that the female copulatory system is unique in several aspects: the genital duct is part concave and part simple type. The seminal receptacle is divided into two chambers, a ventral chamber of ectodermal and mesodermal origin, and a dorsal chamber of ectodermal origin. This dorsal chamber is the location of spermatophore reception during copulation. A sperm plug closes the dorsal chamber off. We propose that long second gonopods deliver male mating products directly into the dorsal chamber. To date, spermatophore reception has been associated with the mesodermal tissue of the seminal receptacle. The copulatory system of box crabs with long second gonopods shows novel deviations from this general pattern. J. Morphol. 276:77–89, 2015. © 2014 Wiley Periodicals, Inc.     

The morphology of the reproductive system in the crab Percnon gibbesi (Decapoda: Brachyura: Grapsoidea) reveals a new combination of characters in Thoracotremata

Recent studies revealed a high diversity of reproductive structures in heterotreme brachyurans, while those of Thoracotremata seem rather uniform. Yet, there still is a huge lack of data in this group as only few species have been studied with respect to their reproductive system. The phylogenetic position of Percnidae is ambiguous. Recent molecular studies place it within polyphyletic grapsoids. We herein study the reproductive morphology of Percnon gibbesi using histology, scanning electron microscopy, micro‐computed tomography and 3D‐reconstructions to test whether this species shows the characteristic thoracotreme pattern. Our results reveal that the male copulatory system conforms to other thoracotremes. It is composed of two pairs of pleopods (gonopods) and likewise paired penes. The first gonopod is relatively long. It possesses a bent terminal process with a distal opening of the ejaculatory canal, a character also present in other grapsoids. The second gonopod is short and terminates in an apical girdle. The female reproductive system reveals a combination of characters, so far unknown for thoracotremes. The paired oviducts do not lead into the seminal receptacles, but run into separate cuticular ducts joined with the vaginae. Accessory sperm storage organs, the bursae, are also connected to the vaginae. Bursae have previously only been described in heterotreme crabs. The data presented in this study reveals a higher diversity of thoracotreme reproductive systems than anticipated.     

Sperm displacement in a millipede? An investigation into the genital morphology of the southern African spirostreptid millipede Orthoporus pyrhocephalus

Male and female genital morphology of the spirostreptid millipede Orthoporus pyrhocephalus was examined by conventional and scanning electron microscopy techniques. The relative syncopulatory positions of the genitalia were established through dissections of pairs in copula. Male gonopods bear scoops and regions of pitted spines. both of which are similar in form to morphological structures implicated in insect sperm displacement. Consideration of the position of the oviduct-spermathecal junction in females predicts that displacement is restricted to a sperm removal mechanism. The importance of spermathecal shape in determining sperm precedence patterns is discussed. The orientation of the genitalia during copulation indicates that sperm displacement is plausible and a mechanism of gonopod action is suggested.     

Genitalia Fitting,Mating Behaviour and Possible Hybridization in Millipedes of the Genus Craspedosoma (Diplopoda,Chordeumatida, Craspedosomatidae)

Abstract The functional anatomy of the extremely complex copulatory organs of the millipede Craspedosoma transsilvanicum Verhoeff, 1897, was investigated by scanning electron microscopy and serial semi-thin sectioning after fixation of the animals by freezing in copula. There is no male organ for sperm transfer which inserts into the receptacula seminis. Sperm secretion is only brushed over the openings of the receptacula by cuticular projections of the anterior gonopods (‘brush’). Other parts of the gonopods (projections of the cheirites, podosternite) bring the brush and the openings of the receptacula in the proper position. Examination of the gonopods from series of Craspedosoma from locations near Vienna showed that there are intermediary specimens between the nominal species C. transsilvanicum and C. alemannicum Verhoeff, 1910. Obviously, a mechanical isolation mechanism, as supposed by Verhoeff, does not exist between these nominal species. At the beginning of a copulation, the male forces the female into the mating position. When touched by males, the females try to evade them by rolling up. The possibilities are discussed that females thereby test the actual fitness of males, and that males use their clasper-like copulatory organs to prevent females from escaping.     

Morphology and function of the copulatory system in freshwater crabs of the genus Potamon

To understand the reproductive processes of freshwater crabs of the genus Potamon, we examined the first and second gonopod and the gonoducts of the female by histological methods. The gonopods are highly modified compared to those of other brachyuran crabs. In particular, the second gonopod is unusually long and has a special morphology, ending in a long sclerotized tube. Suggestions for the function of both gonopods and their different parts are presented. Tubulation of the first and second gonopod is observed. Rosette glands, which are abundant in the subterminal joint of the first gonopod, are connected to the sperm channel by cuticular pores. In females, the chitinous parts of the inner vulva may prove to have a more constant morphology than the external flexible structures. J. Morphol. 239:157–166, 1999. © 1999 Wiley‐Liss, Inc.     

Developmental sequence for the copulatory organs of Kontikia mexicana with remarks on taxonomic significance (Turbellaria: Tricladida: Geoplanidae)

Five specimens, presumably representing different developmental stages of the land planarian Kontikia mexicana (Hyman, 1939), were used to reconstruct the development of the copulatory apparatus in this species. The results support the notion that Kontikia differs from the closely related Caenoplana in its possession of a penis papilla. In the earliest stage available, a penis papilla was absent and other components were not differentiated. In a late-juvenile condition, the gonopore, seminal vesicle, and ejaculatory duct were present. The short penis papilla appeared to arise in this stage by elongation of the terminal tissue around the ejaculatory duct and its separation from the antral wall. The female canal was guarded by an epithelial fold and the glandular duct was present. In the mature condition, the penis papilla was more elongate, and the secretory (prostatic) region of the ejaculatory duct was functional. The female canal, guarded by an epithelial fold, was well-developed with enlarged glandular duct but lacking the posterior diverticulum and the sperm storage system associated with the ovovitelline ducts known in Kontikia orana Froehlich, 1955.     

The reproductive system of Limnopilos naiyanetri indicates a thoracotreme affiliation of Hymenosomatidae (Decapoda,Eubrachyura)

The eubrachyuran Hymenosomatoidea is widely distributed in tropical and subtropical regions ranging from marine to freshwater habitats. Even though the biology of this taxon has been studied to some extent, its phylogenetic relationships are not resolved. Based on different morphological characters, some authors suggested a close affinity of hymenosomatid crabs to heterotremes. However, many of these characters are ambiguous, and the few molecular studies did not provide convincing solutions either. To address this issue, we studied the reproductive system of the hymenosomatid freshwater species Limnopilos naiyanetri Chuang and Ng, 1991 using histology and scanning electron microscopy. The females show the characteristic organization of the paired eubrachyuran reproductive system. Additionally, a bursa (an accessory sperm storing cuticle cavity) is present. The male copulatory system is characterized by paired long first and short second gonopods, and a pair of sternal gonopores equipped with a penis. Both, the female and male reproductive organs reveal a number of similarities to thoracotreme crabs. The seminal receptacle is lined by a very thin cuticle and by a mono-layered glandular epithelium. The male gonopods and the sternal genital opening also resemble the thoracotreme condition. Thus, our results indicate that Hymenosomatidae are most likely part of the Thoracotremata.     

A histochemical study of the reproductive structures in the flatworm Dugesia leporii (Platyhelminthes, Tricladida)

Abstract. The functional morphology and the topographic distribution of tissues in the reproductive system of specimens of Dugesia leporii , an endemic Sardinian free-living planarian, are investigated. Data are provided on the nature of epithelial and glandular secretions, spermatophores, and cocoons by histochemistry, light microscopy, and scanning electron microscopy. All secreting epithelial cells produce strongly acidic sulfated glycoproteins. Glandular cells secrete strongly acidic sulfated glycoproteins or keratohyalin-like material in the penis bulb, and prekeratin-like material in atrial glands. Secretions of the bursa copulatrix may be involved in the activation of sperm while material produced by the bursa canal and oviducts probably serves to propel spermatophores or sperm and eggs. Mucous secretion of the seminal vesicle may serve to dilute and activate sperm before copulation. The viscous secrete of the ejaculatory duct and vasa deferentia may play a protective role to maintain sperm viability. Materials produced by the penis papilla and atrium probably lubricate the epithelial surface. The bilayered wall of spermatophore made of keratohyalin-like material and strongly acidic sulfated glycoproteins is produced by two gland types of the penis bulb. The bilayered shell of cocoon made of prekeratin-like and keratohyalin-like materials is secreted by both atrial glands and vitelline cells. The cocoon stalk is made of keratohyalin-like material produced by cement glands. Shell glands, producing GAG, are not involved in cocoon formation, but they may be implicated in the dilution and activation of seminal material to favor sperm movement toward the oviducts.     

The effect of size,age, and recent egg laying on copulatory choice of the hermaphroditic mollusc Aplysia juliana

Summary

Aplysia juliana is a cross-fertilizing, simultaneous hermaphrodite. During copulation, an individual may act as either a sperm donor or a sperm recipient, or both, when a pair copulates reciprocally. Experiments were conducted with A. juliana to determine if an animal's size, age, or recent egg-laying activity influenced its choice of copulatory role. Animals were isolated except when paired during daily, half-hour trials. In the first experiment, mature animals of different size (weight) but similar age were randomly paired. Animal size had no effect on the initial copulatory role chosen. In the second experiment, young, maturing A. juliana were paired with older animals. Young animals showed no preference in initial copulatory role either as a group or individually. Older A. juliana showed no copulatory preference as a group, but over half of the individuals demonstrated a consistent choice of one role. Some individuals acted almost exclusively as sperm donors, others as sperm recipients, suggesting that as an A. juliana ages, it is likely to develop a preference for a single copulatory role. A record of daily egg mass production was kept for all animals in the second experiment. Production of an egg mass since the last copulation did not affect the copulatory role chosen in the subsequent copulation.     

Characteristics and fate of the spermatozoa of Inachus phalangium (Decapoda, Majidae): description of novel sperm structures and evidence for an additional mechanism of sperm competition in Brachyura

Various aspects of the reproductive anatomy of the spider crab Inachus phalangium are investigated utilizing light and electron microscopy. Spermatozoal ultrastructure reveals the presence of a glycocalyx in the peripheral region of the periopercular rim, never recorded before in crustacean sperm cells. Sperm cell morphological traits such as semi-lunar acrosome shape, centrally perforate and flat operculum, and absence of a thickened ring, are shared only with Macropodia longirostris, confirming a close phylogenetic relationship of these species and their separation from the other members of the family Majidae. Spermatozoa are transferred to females inside spermatophores of different sizes, but during ejaculate transfer, larger spermatophores might be ruptured by tooth-like structures present on the ejaculatory canal of the male first gonopod, releasing free sperm cells. Such a mechanism could represent the first evidence of a second form of sperm competition in conflict with sperm displacement, the only mechanism of sperm competition known among Brachyura, enabling paternity for both dominant and smaller, non-dominant, males. In addition, we propose several hypotheses concerning the remote and proximal causes of the existence of large seminal receptacles in females of I. phalangium. Among these, genetically diverse progeny, reduction of sexual harassment and phylogenetic retention seem the most plausible, while acquisition of nutrients from seminal fluids, demonstrated in other arthropods, and suggested by previous studies, could be discarded on the basis of the presented data.     

Copulatory wounds in the monandrous ant species <Emphasis Type="Italic">Formica japonica</Emphasis> (Hymenoptera,Formicidae)

Males of several insect species inflict wounds on female genitalia during copulation, but the significance of such copulatory wounds for males is not clear. I compared the genitalia of virgin and mated Formica japonica females and for the first time report the occurrence of copulatory wounds in this monandrous ant species. All inseminated females examined had two types of melanized patches, indicating wound repair, and the serrated penis valves and sharp-pointed volsellar digitus of male genitalia were the likely instruments of these wounds. Physically damaging mating in monandrous species supports the view that copulatory wounds do not necessarily contribute to postcopulatory fitness gains for males via advantages in sperm competition or cryptic female choice. Received 10 September 2007; revised 15 October 2007; accepted 16 October 2007.     

Spermatophore transfer in the hermit crab Clibanarius vittatus (Crustacea,Anomura, Diogenidae)

Although mating has been described in several hermit crab species, the mechanics of spermatophore transfer have not previously been demonstrated. Evidence from pleopod and gonopore morphology, video observations, and inseminated females indicates that in Clibanarius vittatus the male applies a spermatophoric mass directly onto the female via the gonopores rather than with modified pleopods 1-2 (gonopods) and/or genital papillae as in many other decapods. The single second pleopod of males of C. vittatus has a simple endopod with no apparent modifications for sperm transfer. There are no genital papillae extending from the male gonopores. The globular spermatophores are aligned in rows surrounded by a seminal secretion in the male ducts (vasa deferentia that terminate in ejaculatory ducts opening to the exterior via the gonopores). During copulation, described from time-lapse video recordings, the ventral surface of the last thoracic segment of the male, bearing the gonopores, was apposed to the ventral cephalothorax of the female. A massive amount of seminal secretion containing spermatophore ribbons, termed here the spermatophoric mass and described for the first time in a hermit crab species, was observed covering the sternites and coxae of pereopods 1-5 of a recently copulated female. It is suggested that during copulation the male emits the contents of the ejaculatory ducts directly onto the female without the aid of gonopods or genital papillae. Although spermatophore transfer is simple in C. vittatus, the presence of modified anterior pleopods or elongate genital papillae (sexual tubes) in other paguroidean species suggests the possibility of a more complex insemination process in these other hermit crabs.     

Copulatory behaviour of the bank voleMyodes glareolus: matings with one and two males do not make a difference

In promiscuous species in which females mate with more than one male during oestrus, males may increase their sperm expenditure or change their copulatory behaviour in response to the risk of sperm competition. I used an experimental approach to investigate the pattern of copulatory behaviour of the bank voleMyodes glareolus Schreber, 1780 depending on whether the female mated with one or two males. The work showed that the copulatory period of the bank vole lasted about 80 minutes and consisted of 4–5 ejaculatory series, with multiple intromissions preceding ejaculation. There were no significant changes in number of intromissions across the first four ejaculatory series, but I did find a relationship between number of intromissions and first ejaculation latency; also, ejaculation latencies grew shorter as the ejaculatory series proceeded. Litter size did not differ significantly between females that mated with one male and those mating with two, nor did the reproductive success of males that mated with the same female. Mating with an oestrus female appears to be advantageous for bank vole males even if they mate as the second one, and the risk of sperm competition did not trigger changes in male copulatory behaviour. The similar durations of the copulatory period and patterns of change of ejaculation latencies during copulations with one and two males point to the role of the female in temporal copulatory behaviour of the bank vole.     

Copulation behavior inside and outside the beetleMacrohaltica jamaicensis (Coleoptera,Chrysomelidae)

Copulation behavior inMacrohaltica jamaicensis involved a complex, relatively stereotyped series of events both inside and outside the female. Only incomplete sperm transfer occurred in many copulations. Some aspects of male copulatory courtship behavior performed during and following copulation were consistently coordinated with particular stages in sperm transfer. This coordination suggests that copulatory courtship may function to induce critical internal female responses which sometimes do not occur, such as relaxing the bursal muscles to permit deeper penetration, and allowing sperm transfer to occur before the spermatophore is discarded.     

Spermatophore expulsion in the carrion beetle Silpha perforata (Coleoptera: Silphidae)

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.     

Role of the petasma and appendices masculinae during copulation and insemination in the penaeoid shrimp,Sicyonia dorsalis (Crustacea: Decapoda: Dendrobranchiata)

Summary

The role of presumed male gonopods in the insemination of females was investigated in the penaeoid shrimp Sicyonia dorsalis. Males with partially ablated petasmata or with ablated appendices masculinae did not copulate with females, while control males with exopods removed from the third pleopods copulated frequently and successfully inseminated females. However, males with petasmata altered by blockages at the tip or at the base did copulate with females but were unable to inseminate them. The hypothesis that the petasma of Sicyonia is a sperm injection device is rejected. Evidence against this hypothesis includes the structure of the gonopods, the position of the male at right angles below the female during copulation, the brevity of copulation, the frequency of copulation during normal matings, and the ability of males to inseminate only the spermatheca on one side per successful copulation. It is hypothesized that the male uses the petasma, supported by the endopods of the second pleopods, to hook onto the female thelycum, adjusting position so that one erect genital papilla directly injects sperm mass into the aperture of one of the paired spermathecae. It is suggested that female selection on male petasma structure and use has resulted in the complex form of the petasma, rather than a purely mechanical selection for an efficient sperm injection device.     

Differential sperm expenditure reveals a possible role for post‐copulatory sexual selection in a lekking moth

Male reproductive success in the lesser wax moth Achroia grisella is strongly determined by pre‐copulatory mate choice, during which females choose among males aggregated in small leks based on the attractiveness of ultrasonic songs. Nothing is known about the potential of post‐copulatory mechanisms to affect male reproductive success. However, there is evidence that females at least occasionally remate with a second male and that males are unable to produce ejaculates quickly after a previous copulation. Here we investigated the effects of mating history on ejaculate size and demonstrate that the number of transferred sperm significantly decreased from first (i.e., virgin) to second (i.e., nonvirgin) copulation within individual males. For males of identical age, the number of sperm transferred was higher in virgin than in nonvirgin copulations, too, demonstrating that mating history, is responsible for the decrease in sperm numbers transferred and not the concomitant age difference. Furthermore, the number of transferred sperm was significantly repeatable within males. The demonstrated variation in ejaculate size both between subsequent copulations as well as among individuals suggests that there is allocation of a possibly limited amount of sperm. Because female fecundity is not limited by sperm availability in this system, post‐copulatory mechanisms, in particular sperm competition, may play a previously underappreciated role in the lesser wax moth mating system.     

Ultrastructure of the reproductive system of the house dust mitesDermatophagoides farinae andD. pteronyssinus (Acari,Pyroglyphidae) with remarks on spermatogenesis and oogenesis

Several parts of the reproductive system of both sexes ofDermatophagoides farinae andD. pteronyssinus are investigated and compared by light-, scanning electron-, and transmission electron microscopy. New techniques have been employed for scanning of the internal structures of these mites. The male reproductive system consists of unpaired testis, paired vasa deferentia, an accessory gland, ejaculatory duct, and copulatory organ. The female reproductive system consists of bursa copulatrix, ductus bursae, receptaculum seminis, paired ducti receptaculi, ovaries, oviducts, one chorion gland, ovipositor, and oviporus. Testis as well as ovaries are characterized by syncytia of nutritional function. The specifics of spermatogenesis are discussed in connection with sperm transfer. Similarities between the construction of the ovaries and oogenesis in astigmatic mites and telotrophic meroistic ovaries in insects are discussed.     

Functional anatomy of male copulatory organs of Pomacea canaliculata (Caenogastropoda, Ampullariidae)

This study was aimed to investigate the functional morphology of copulation and sperm transfer in the invasive snail Pomacea canaliculata. Three-dimensional renderings of the male copulatory apparatus were made and showed elaborate systems for innervation and for hemolymph supply and drainage. A key component of the male copulatory apparatus is the penial sheath, which shows three specialized glands; the medial and distal glands may participate in adherence to the mantle cavity wall of the female during copulation. The outer gland has an epithelium composed of columnar cells with branched microvilli, mucous goblet cells and large granular secretory cells containing intragranular crystalloids, which produce an exocrine secretion during copulation. The interaction of male/female copulatory organs was studied in dissections of snap-frozen pairs. Sperm are left in the sperm pit, at the end of the pallial spermiduct. Afterwards, the muscular action of the penial bulb takes the sperm up to the vermiform penis, which slides from the penial pouch into the central groove of the penial sheath, and it later emerges through a T-shaped sulcus of this structure and enters the female vagina. Then, it climbs through the capsule duct, and its tip reaches the proximity of the seminal receptacle. A model of copulation and sperm transfer is presented on the basis of the new findings and on published literature.     

Group mating among Norway rats II. The social dynamics of copulation: Competition,cooperation, and mate choice

The social interactions within groups of Norway rats (Rattus norvegicus) had a strong impact on the individual pattern of copulation which, in turn, affects sperm precedence and the probability of implantation in this species. Males alternated uninterrupted ejaculatory series, augmenting each others' copulatory investment. Females took turns mating after receiving an intromission, collectively potentiating the males' copulatory behaviour; increasing the number of oestrous females increased the number of intromissions and ejaculations achieved by each male but did not affect the amount of copulation experienced by each female. These turn-taking patterns within each sex provided the opportunity to change partners and permitted the emergence of different sex-typical patterns of copulation. Furthermore, the dominant male contributed more intromissions and tended to give each female more ejaculations than the subordinates did. Dominant males were also more likely to inhibit the subordinates' sperm transport. Females competed among themselves for the opportunity to mate with a male as he approached ejaculation and were likely to protect more of the dominant male's sperm transport than the subordinate male's.