Female genital morphology and mating behavior of Orchestina (Arachnida: Araneae: Oonopidae)

The unusual reproductive biology of many spider species makes them compelling targets for evolutionary investigations. Mating behavior studies combined with genital morphological investigations help to understand complex spider reproductive systems and explain their function in the context of sexual selection. Oonopidae are a diverse spider family comprising a variety of species with complex internal female genitalia. Data on oonopid phylogeny are preliminary and especially studies on their mating behavior are very rare. The present investigation reports on the copulatory behavior of an Orchestina species for the first time. The female genitalia are described by means of serial semi-thin sections and scanning electron microscopy. Females of Orchestina sp. mate with multiple males. On average, copulations last between 15.4 and 23.54 min. During copulation, the spiders are in a position taken by most theraphosids and certain members of the subfamily Oonopinae: the male pushes the female back and is situated under her facing the female's sternum. Males of Orchestina sp. possibly display post-copulatory mate-guarding behavior. The female genitalia are complex. The genital opening leads into the uterus externus from which a single receptaculum emerges. The dorsal wall of the receptaculum forms a sclerite serving as muscle attachment. A sclerotized plate with attached muscles lies in the posterior wall of the uterus externus. The plate might be used to lock the uterus during copulation. The present study gives no direct evidence for cryptic female choice in Orchestina sp. but suggests that sexual selection occurs in the form of sperm competition through sperm mixing.     

Silhouettella loricatula (Arachnida, Araneae, Oonopidae): a Haplogyne spider with complex female genitalia

The female genital system of the oonopid Silhouettella loricatula is astonishingly complex. The genital opening is situated medially and leads into an oval receptaculum that is heavily sclerotized except for the ventral half of the posterior wall that appears chitinized only. A large striking sclerite lying in the posterior wall of the uterus externus is attached anteriorly to the receptaculum and continues dorsally into a globular appendix that bears a furrow. The uterus externus shows a peculiar modification in its anterior wall: a paddle-like sclerite with a nail-like posterior process. This sclerite lies opposite to the furrow proceeding in the globular appendix and may serve females to lock the uterus externus by muscle contractions. Massive muscles connect the sclerite with the anterior scutum of the opisthosoma and with two other sclerites that are attached to the receptaculum and serve as attachments for further muscles. Gland cells extend around a pore field of the receptaculum. They produce secretion that encloses spermatozoa in a discrete package (secretory sac) inside the receptaculum. In this way, the mixing of sperm from different males and thus sperm competition may be severely limited or completely prevented. During a copulation in the laboratory the ejection of a secretory sac that most probably contained spermatozoa was observed, indicating sperm dumping in S. loricatula. The ejection of the secretory sac may be caused by female muscle contractions or by male pedipalp movements. The majority of the investigated females have microorganisms in the receptacula that could represent symbionts or infectious agents. The microorganisms can be identified partly as bacteria. They are enclosed in secretion and are always found in the same position inside the receptaculum.     

Genital morphology of female goblin spiders (Arachnida: Araneae: Oonopidae) with functional implications

Spider genital morphology usually provides the best characters for taxonomy. Furthermore, functional genital morphology helps to understand the evolution of complex genitalia and their role in the context of sexual selection. The genital systems of most haplogyne spider families are poorly investigated with respect to their morphology. The present study investigates the female genitalia of the oonopids Oonops pulcher, Oonopinus kilikus, and Pseudotriaeris sp. by means of light microscopy and SEM. The male palps are briefly described. Females of O. pulcher store spermatozoa in an anterior and a posterior receptaculum (PRe). The genitalia resemble the primitive dysderoid genitalia supporting the hypothesis that the subfamily Oonopinae contains more basal oonopids. In O. kilikus, the anterior receptaculum is reduced to a sclerite. Spermatozoa are stored in a PRe. The receptacula of Pseudotriaeris sp. are reduced to sclerites. Spermatozoa in the uterus internus indicate that fertilization happens there or in the ovary. The anterior sclerite might serve females to lock the uterus during copulation as suggested for other gamasomorphines. The male palp of O. kilikus is simple, whereas the palps of O. pulcher and Pseudotriaeris sp. appear more complex. Complicated structures on the palp of Pseudotriaeris sp. indicate that males exert copulatory courtship.     

Genital morphology of the haplogyne spider <Emphasis Type="Italic">Harpactea lepida</Emphasis> (Arachnida,Araneae, Dysderidae)

Female Harpactea lepida possess a single genital opening leading into a diverticulum. This diverticulum shows no secretory layer. It continues posteriorly into a receptaculum which is associated with gland cells. In the two already described dysderids, Dysdera crocata and D. erythrina, the bilobed spermatheca lies anteriorly to the diverticulum. Gland cells are associated with the spermatheca and the diverticulum. In H. lepida, the sclerotized genital structures lie dorsally to the diverticulum and consist of a posterior and an anterior part. The posterior part shows a lamella extending laterally to sclerites functioning as muscle attachments. The anterior part has two roundish structures. A hollow stalk-like sclerite functioning as muscle attachment extends towards anterior. The posterior and the anterior part of the sclerotized genital structures fit together. A narrow uterine valve connecting the uterus externus with the diverticulum forms between them. It may be opened by muscles as also suggested for D. erythrina. In H. lepida, spermatozoa embedded in secretion are found in the diverticulum and the receptaculum. There is no evidence that they are stored under different conditions like in D. erythrina. Additional spermatozoa are found in the uterus externus of H. lepida which could be an indication for internal fertilization. Spermatogenesis occurs in cysts in the testes of male H. lepida. In the vasa deferentia, the ductus ejaculatorius and the palpal bulb, the spermatozoa are embedded in homogenous secretion. The palpal bulb has a distal extension bearing a crown-like structure. The embolus is situated at the base of the extension. In memoriam of Konrad Thaler.     

Female genitalia of goblin spiders (Arachnida: Araneae: Oonopidae): a morphological study with functional implications

Abstract. Fine morphological details of the genitalia have large potential consequences for the understanding of the reproductive biology of a particular species, especially when mating behavioral studies are difficult to conduct. Oonopidae are a highly diverse spider family comprising a variety of species with complex female reproductive systems, which may have evolved under sexual selection by cryptic female choice. The present study describes the female genitalia of five oonopid species belonging to both conventionally recognized subfamilies by means of semi‐thin sections and scanning electron microscopy. In addition, the male palps are briefly described. The organization of the female genitalia in Scaphiella hespera and Scaphiella sp. resembles the entelegyne type. A chitinized canal connects the receptaculum, where sperm are stored, with the uterus. Sperm are also present in the uterus and the canal is suggested to function as fertilization duct. The genitalia of the parthenogenetic species Triaeris stenaspis are surprisingly complex. A large sac with glands is proposed to represent the equivalent of a receptaculum in sexually reproducing females. In females of Opopaea recondita, sperm are stored in a bulge derivating from the uterus. Contractions of muscles attached to the bulge may lead to sperm dumping. The uterus can be closed by a sclerite in its anterior wall. The receptacula of females of Stenoonops reductus are joined together and contain masses of spermatozoa. Additional sperm were found in the receptacula connection suggesting that fertilization takes place there. The male palps of all the investigated species, except for S. hespera, seem to lack a distincly sclerotized sperm duct. Spermatozoa and secretions are stored in a large reservoir inside the genital bulb surrounded by glandular epithelium.     

Complex female genitalia indicate sperm dumping in armored goblin spiders (Arachnida,Araneae, Oonopidae)

In promiscuous females, sperm ejection from the sperm storage site can be a strong mechanism to influence sperm priority patterns. Sperm dumping is reported from different animals including birds, insects, and humans. In spiders, it has been documented for four species including the oonopid Silhouettella loricatula. Oonopidae are a diverse spider family comprising many species with peculiar female genitalia. Especially in species where studies of mating behavior are difficult, morphological investigations of the genitalia help to understand their function and evolution. In the present study, the genitalia of the oonopids Myrmopopaea sp., Grymeus sp., and Lionneta sp. are investigated by means of histological serial sections and scanning electron microscopy (SEM). The results are compared with previous findings on S. loricatula. In Myrmopopaea sp. and Grymeus sp., the same morphological components are present that are involved in sperm dumping in S. loricatula. Inside the receptaculum, sperm are enclosed in a secretory sac which can be moved to the genital opening and dumped during copulation by muscle contractions. The female genitalia of Lionneta sp. are asymmetric. They show the same characteristics as S. loricatula but all the investigated females were unmated. The results strongly suggest that sperm dumping occurs in Myrmopopaea sp., Grymeus sp., and Lionneta sp. and happens by the same mechanism as in S. loricatula. Sperm dumping might even be common within a clade of oonopids. As in S. loricatula, the sperm transfer forms in the investigated species consist of several spermatozoa. Papillae with unknown function occur on the receptacula of all females.     

Complex genital structures indicate cryptic female choice in a haplogyne spider (Arachnida,Araneae, Oonopidae,Gamasomorphinae)

Female genital structures with their allied muscles of the haplogyne spider Opopaea fosuma are described. A functional explanation of this system is given, which indicates that cryptic female choice may occur in these spiders: the anterior wall of their spermatheca is strongly sclerotized and possesses a cone-shaped hole in its upper part. A transverse sclerite that serves as muscle attachment bears a nail-like structure and lies in a chitinized area of the anterior wall of the uterus externus. Muscle contraction presses this nail into the hole of the spermatheca. In this way, the uterus externus gets both locked and fixed. Furthermore, as this occurs the copulatory orifice is enlarged and the resulting suction probably leads to previously deposited sperm being drawn from the spermatheca and dumped. This is a common mechanism used by females to influence a male's chances of fathering their offspring in a process known as cryptic female choice.     

SPECIES ISOLATION,GENITAL MECHANICS,AND THE EVOLUTION OF SPECIES-SPECIFIC GENITALIA IN THREE SPECIES OF MACRODACTYLUS BEETLES (COLEOPTERA,SCARABEIDAE, MELOLONTHINAE)

The question asked was why male genitalic structures have diverged in three syntopic species of Macrodactylus beetles. Four hypotheses were evaluated: 1. The ways in which male genitalia mesh with internal female structures indicate that selection for species isolation via mechanical exclusion (“lock and key”) is unlikely to explain the genitalic differences. 2. The specific mate recognition hypothesis also clearly fails to explain genitalic differences due to the implausibility of postulated environmental effects on genitalia, and lack of postulated coevolution of male and female morphologies. 3. Selection for species isolation via differences in genitalic stimulation (sensory lock and key) is unlikely due to relatively infrequent cross-specific pair formation and intromission in the field, and “excessive” numbers of species-specific genitalic structures and male courtship behavior patterns which nevertheless occasionally fail. It also fails to explain the frequent failure of intraspecific copulations to result in sperm transfer. This hypothesis cannot, however, be rejected as confidently as the previous hypotheses. 4. Conditions under which sexual selection by cryptic female choice could take place are common. Females frequently exercise their ability to prevent sperm transfer by conspecific males even after intromission has occurred, and females generally mate repeatedly, probably with different males. Males behave as if cryptic female choice is occurring, courting assiduously while their genitalia are within the female. Sexual selection by female choice could thus contribute to the divergence in genitalic structures.     

Genital Morphology and Sperm Storage in Pholcus phalangioides(Fuesslin, 1775) (Pholcidae; Araneae)

The genital morphology of female Pholcus phalangioidesis examined to clarify the composition of the uterus externus and the place of sperm storage in this species. Two conspicuous pore plates serve as exits for glandular secretion that gets discharged into the uterus externus. The secretion accumulates close to the pore plates and to some extent in the region of the heavily sclerotized valve that separates the uterus externus from the uterus internus. During copulation, the male transfers spermatozoa and male secretions into the female genital tract where they are embedded and stored in the female secretion. As Ph. phalangioidesdoes not possess any separate sperm storage organs such as receptacula seminis, the glandular secretion serves to store and fix the sperm mass in a specific position within the uterus externus itself.     

Experimental demonstration of possible cryptic female choice on male tsetse fly genitalia

A possible explanation for one of the most general trends in animal evolution - rapid divergent evolution of animal genitalia - is that male genitalia are used as courtship devices that influence cryptic female choice. But experimental demonstrations of stimulatory effects of male genitalia on female reproductive processes have generally been lacking. Previous studies of female reproductive physiology in the tsetse fly Glossina morsitans suggested that stimulation during copulation triggers ovulation and resistance to remating. In this study we altered the form of two male genital structures that squeeze the female's abdomen rhythmically in G. morsitans centralis and induced, as predicted, cryptic female choice against the male: sperm storage decreased, while female remating increased. Further experiments in which we altered the female sensory abilities at the site contacted by these male structures during copulation, and severely altered or eliminated the stimuli the male received from this portion of his genitalia, suggested that the effects of genital alteration on sperm storage were due to changes in tactile stimuli received by the female, rather than altered male behavior. These data support the hypothesis that sexual selection by cryptic female choice has been responsible for the rapid divergent evolution of male genitalia in Glossina; limitations of this support are discussed. It appears that a complex combination of stimuli trigger female ovulation, sperm storage, and remating, and different stimuli affect different processes in G. morsitans, and that the same processes are controlled differently in G. pallidipes. This puzzling diversity in female triggering mechanisms may be due to the action of sexual selection.     

Female genital system of the folding-trapdoor spider Antrodiaetus unicolor (Hentz, 1842) (Antrodiaetidae, Araneae): ultrastructural study of form and function with notes on reproductive biology of spiders

The genitalia of the female folding-trapdoor spider Antrodiaetus unicolor are characterized by two pairs of spermathecae that are arranged in a single row and connected to the roof of the bursa copulatrix. Each single spermatheca is divided into three main parts: stalk, bowl, and bulb, which are surrounded by the spermathecal gland. The epithelium of the spermathecal gland is underlain by a muscle meshwork and consists of different types of cells partly belonging to glandular cell units (Class 3 gland cells) that extend into pores in the cuticle of the stalk and bowl. Interestingly, the bulb lacks glandular pores and is characterized by a weakly sclerotized cuticle. This peculiarly structured bulb probably plays an important role in the discharge of the sperm mass. It is suggested that by contraction of the muscle layer the sperm mass may be squeezed out, when the bulb invaginates and expands into the spermathecal lumen, pushing the sperm to the uterus lumen. Each glandular unit consists of usually one or two central secretory cells that are for the most part surrounded by a connecting cell that again is surrounded by a canal cell. The canal cell, finally, is separated from the other epithelial cells (intercalary cells) located between the glandular units by several thin sheath cells that form the outer enveloping layer of the unit. The secretions are released through a cuticular duct that originates proximally between the apical part of the connecting cell and the apical microvilli of the secretory cells and runs into a pore of the spermathecal cuticle. The glandular products of the Class 3 gland cells likely contribute to the conditions allowing long-term storage of the spermatozoa in this species. Details regarding the ovary, the uterus internus, and the uterus externus are reported. Most of the secretion that composes the chorion of the egg is produced in the ovary. Glandular cell units observed in the uterus externus differ structurally from those in the spermathecae and likely play a different role. Finally, we briefly discuss our results on the female genitalia of A. unicolor in the light of knowledge about the reproductive biology of spiders.     

Functional genital morphology of armored spiders (Arachnida: Araneae: Tetrablemmidae)

This study describes the female genitalia of the tetrablemmid spiders Brignoliella acuminata, Monoblemma muchmorei, Caraimatta sbordonii, Tetrablemma magister, and Ablemma unicornis by means of serial semi‐thin sections and scanning electron microscopy and compares the results with previous findings on Indicoblemma lannaianum. Furthermore, the male palps and chelicerae are briefly described. The general vulval organization of females is complex and shows similarities in all of the investigated species. The copulatory orifice is situated near the posterior margin of the pulmonary plate. The opening of the uterus externus lies between the pulmonary and the postgenital plate. Paired copulatory ducts lead to sac‐like receptacula. Except for A. unicornis, the male emboli of all investigated species are elongated and thread‐like. However, they are too short to reach the receptacula. Hence, the spermatozoa have to be deposited inside the copulatory ducts. The same situation was also found in I. lannaianum. Females of this species store sperm encapsulated in secretory balls in their receptacula. The secretion is produced by glands adjoining the receptacula. The presence of paired fertilization ducts and spermatozoa in the uterus internus suggested that fertilization takes place internally in I. lannaianum. Secretory balls in the receptacula are found in all of the investigated species in this study, showing that sperm are stored in the same way. The place of fertilization may also be identical since dark particles, presumably spermatozoa, are located in the uterus internus of all investigated species except for T. magister. However, fertilization ducts are only found in B. acuminata and M. muchmorei. A sclerotized central process with attached muscles is present in A. unicornis, M. muchmorei, C. sbordonii and T. magister. Only in A. unicornis does the central process show an internal lumen and hold spermatozoa. In the other species, it could be used to lock the uterus during copulation in order to prevent sperm from getting into it as suggested for certain oonopid species. The uterus externus of all investigated species shows a sclerotized dorsal fold with attached muscles, previously described as “inner vulval plate.” Contractions of the muscles lead to a widening of the dorsal fold, thus creating enough space for the large oocytes to pass the narrow uterus externus. The males of all investigated species have apophyses on their chelicerae. At least in B. acuminata and A. unicornis, where females have paired grooves on the preanal plate, these apophyses allow males to grasp the female during copulation as described for I. lannaianum. © 2008 Wiley‐Liss, Inc.     

Frequent Failure of Male Monopolization Strategies as a Cost of Female Choice in the Black Widow Spider Latrodectus tredecimguttatus

In many mating systems, males strive for securing paternity through monopolizing females. As male monopolization attempts often contradict female interests, this conflict may fuel an evolutionary arms race. In the widow spider genus Latrodectus, females are commonly polyandrous, whereas males are monogynous, hence restricted to mate with a single female, making paternity protection particularly important. Potential mating plugs (specialized embolus sclerites of male copulatory organs) have been discovered in the complex female genital tracts of several Latrodectus species. In this study, we investigated mating strategies in the Mediterranean black widow spider Latrodectus tredecimguttatus and tested the adaptive value of female attacks against male monopolization efforts. In a double mating experiment, we manipulated the number of insertions (=copulations) for first and second males to assess female behaviour and male embolus sclerite placement success. Our results indicate that first males′ embolus sclerites inside the females′ sperm stores physically block sclerites of subsequent males. While female attacks did not affect the deposition of potential mating plugs, they significantly reduced copulation duration. Irrespective of female aggression, male sclerite placement failure occurred frequently, but large males were more successful than smaller competitors. We suggest that the complex genital morphology in both sexes may have co‐evolved antagonistically and female morphology could serve to favour large males for fertilization.     

Spermatophores, female genitalia, and courtship behaviour of two whip spider species, Charinus africanus and Damon tibialis (Chelicerata: Amblypygi)

This paper describes courtship behaviour, spermatophore morphology, and the female genitalia of the African whip spiders Charinus africanus Hansen, 1921 (Charinidae) and Damon tibialis (Simon, 1876) (Phrynichidae). In C. africanus, only the first part of courtship behaviour, up to spermatophore formation, could be observed; though different in detail, it is similar to that of many other species. The small spermatophore of C. africanus contains one large median sperm package. Charinus africanus is one of the Charinus species with thin finger-like gonopods and the first species with such gonopods of which the spermatophore is known. Spermatophores and female genitalia of D. tibialis are similar, though different in details, to those of Trichodamon and Musicodamon. They thus suggest that these two genera are correctly included in the Damoninae.     

Complex genital system of a haplogyne spider (Arachnida, Araneae, Tetrablemmidae) indicates internal fertilization and full female control over transferred sperm

The female genital organs of the tetrablemmid Indicoblemma lannaianum are astonishingly complex. The copulatory orifice lies anterior to the opening of the uterus externus and leads into a narrow insertion duct that ends in a genital cavity. The genital cavity continues laterally in paired tube-like copulatory ducts, which lead into paired, large, sac-like receptacula. Each receptaculum has a sclerotized pore plate with associated gland cells. Paired small fertilization ducts originate in the receptacula and take their curved course inside the copulatory ducts. The fertilization ducts end in slit-like openings in the sclerotized posterior walls of the copulatory ducts. Huge masses of secretions forming large balls are detectable in the female receptacula. An important function of these secretory balls seems to be the encapsulation of spermatozoa in discrete packages in order to avoid the mixing of sperm from different males. In this way, sperm competition may be completely prevented or at least severely limited. Females seem to have full control over transferred sperm and be able to express preference for spermatozoa of certain males. The lumen of the sperm containing secretory balls is connected with the fertilization duct. Activated spermatozoa are only found in the uterus internus of females, which is an indication of internal fertilization. The sperm cells in the uterus internus are characterized by an extensive cytoplasm and an elongated, cone-shaped nucleus. The male genital system of I. lannaianum consists of thick testes and thin convoluted vasa deferentia that open into the wide ductus ejaculatorius. The voluminous globular palpal bulb is filled with seminal fluid consisting of a globular secretion in which only a few spermatozoa are embedded. The spermatozoa are encapsulated by a sheath produced in the genital system. The secretions in females may at least partly consist of male secretions that could be involved in the building of the secretory balls or play a role in sperm activation. The male secretions could also afford nutriments to the spermatozoa.     

Female genital morphology in the secondarily haplogyne spider genus Glenognatha Simon, 1887 (Araneae,Tetragnathidae), with comments on its phylogenetic significance

Female genital morphology of secondarily haplogyne spiders has been poorly studied, hampering the analysis of its possible phylogenetic significance. We conduct a comparative morphological study of 12 species of the secondarily haplogyne spider genus Glenognatha Simon, 1887 using scanning electron microscopy. Representatives of the closely related genera Pachygnatha Sundevall, 1823 and Dyschiriognatha Simon, 1893 were also examined. The female genitalia of Glenognatha, Dyschiriognatha, and Pachygnatha species examined are composed of a spiracle‐shape gonopore, a membranous chamber, a pair of copulatory ducts (CD) leading to spermathecae and a large uterus externus (UE). The most significant variation among Glenognatha species, previously unregistered within Araneoidea, is related with the absence or presence of CD and spermathecae. In addition, several characters as the form and distribution of long stem gland ductules and compartmentalization of the UE may be important for phylogenetic inference at species and generic level. Our results corroborate the close relationship between Dyshiriognatha and Glenognatha. A table with potentially informative female genitalic characters for phylogenetic inference within Glenognatha is provided. Understanding the general structure of the female genitalia in secondarily haplogyne taxa is a crucial step in order to propose characters for phylogenetic inference and to understand its possible functional significance. J. Morphol. 275:1027–1040, 2014. © 2014 Wiley Periodicals, Inc.     

Dimorphism of right–left asymmetry in the female genitalia of the brachypterous grasshopper Parapodisma mikado (Orthoptera: Acrididae)

Several insects exhibit morphological asymmetry in the mouthparts or genitalia. In a part of species with asymmetric genitalia, two mirror‐image forms of the genitalia are reported to occur in a population. This dimorphism, called chiral dimorphism, is usually observed in male genitalia, but its examples in female genitalia are very limited. Here, we report that the females of the brachypterous grasshopper Parapodisma mikado are equipped with an asymmetric sclerite in the copulatory bursa, and that two mirror‐image forms of the sclerite occur in local populations. This dimorphism was detected in all of seven populations examined, and the ratio of the two forms was approximately 2:1 for the right : left forms. In one population, the ratio of the two forms did not vary among three consecutive years. Thus, chiral dimorphism in the female genitalia is kept almost constant spatiotemporally. Mating experiments indicated that the direction of female genitalia did not affect the direction to which the males twist their abdomen (right or left side) during mating or the duration of mating. We propose two hypotheses, a neutral developmental mechanism and sexual conflict, for the maintenance of chiral dimorphism in the genitalia of P. mikado females.