Spermatogenesis and sperm—spermatheca relations in Spirorbis spirorbis (L.)

The differentiation from early spermatid to spermatozoon is described with special emphasis on the formation of the helix of chromatin and mitochondrial junctions. The role of microtubules in morphogenesis is discussed.

New observations on the role of the recently described spermatheca are presented; phagocytosis and digestion of spermatozoa are proven, and the various origins of the sperm found in the spermatheca are specified.     

Impact of male mating history on the postmating resumption of sexual receptivity and lifetime reproductive success in Choristoneura rosaceana females

Abstract.  The first objective of the present study is to test the hypothesis that the decrease in the number of eupyrene spermatozoa in the spermatheca is directly associated with the resumption of sexual receptivity in female moths, an aspect that has not been examined in previous studies. The obliquebanded leafroller, Choristoneura rosaceana , is used and females mated with previously mated males have a shorter refractory period than those mated with virgins. This difference is associated with a faster rate of movement of sperm from the spermatheca. Overall, the length of the female refractory period coincides with the mean time required for the number of eupyrene sperm in the spermatheca to drop to approximately 3000, regardless of male mating history. Although such a decline in sperm numbers may be a factor responsible for the resumption of sexual receptivity, this is clearly not the only one because more than 40% of females remate even though sperm numbers in the spermatheca are well above this threshold. Virgin males do not vary the mass or the content of their ejaculate as a function of the female's reproductive status and this may increase the risk of sperm competition if the female is previously mated. The second objective of this study is to examine the effect of previous male mating history on female reproductive potential. Females mated with previously mated males have a significantly lower fecundity than those mated with virgin males. However, in all treatments, remating increases both female longevity and lifetime fecundity. There is also a significant effect of female mass on the length of the refractory period and on lifetime fecundity, with large females resuming sexual receptivity sooner and laying more eggs than small ones, regardless of male mating history.     

Sperm reduces female longevity and increases melanization of the spermatheca in the bumblebee <Emphasis Type="Italic">Bombus terrestris</Emphasis> L.

Here we present evidence that the male mating products (sperm and gland products) reduce survival during hibernation of queens of the bumblebee B. terrestris. Most remarkably, the inseminated queens are significantly more likely to have melanized spermathecae than their virgin sisters. Although we could not detect a direct relationship between these two findings they are quite remarkable since B. terrestris is a monandrous and comparably long-lived insect where sexual conflict is unlikely to evolve. The reduced survival can probably be attributed to a general cost of maintaining the sperm, whereas the presence of melanized spermathecae in the inseminated queens may indicate a pathogen transferred during mating or genetic incompatibilities between males and queens. Received 30 December 2007; revised 27 April 2008; accepted 1 May 2008.     

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.     

EVOLUTION OF MULTIPLE KINDS OF FEMALE SPERM-STORAGE ORGANS IN DROSOPHILA

Females of all species belonging to the family Drosophilidae have two kinds of sperm-storage organs: paired spherical spermathecae and a single elongate tubular seminal receptacle. We examined 113 species belonging to the genus Drosophila and closely allied genera and describe variation in female sperm-storage organ use and morphology. The macroevolutionary pattern of organ dysfunction and morphological divergence suggests that ancestrally both kinds of organs stored sperm. Loss of use of the spermathecae has evolved at least 13 times; evolutionary regain of spermathecal function has rarely if ever occurred. Loss of use of the seminal receptacle has likely occurred only once; in this case, all descendant species possess unusually elaborate spermathecae. Data further indicate that the seminal receptacle is the primary sperm-storage organ in Drosophila. This organ exhibits a pattern of strong correlated evolution with the length of sperm. The evolution of multiple kinds of female sperm-storage organs and the rapidly divergent and correlated evolution of sperm and female reproductive tract morphology are discussed.     

Morphology of the female genital ducts of the blue land crab Cardisoma guanhumi (Crustacea: Brachyura: Gecarcinidae)

This is a histological and histochemical analysis of the terminal portion of the female reproductive system and genital ducts of the blue land crab (Cardisoma guanhumi). Animals were collected in the Jaguaribe estuary (Ceará, Brazil) and dissected. Genital duct fragments were fixed and submitted to different staining techniques. The female reproductive system consists of a pair of ovaries and a pair of genital ducts. In the mid‐posterior portion of each lobe, the ovaries communicate with the genital ducts, which are subdivided into oviduct, spermatheca, vagina, and gonopore. Histologically, the spermatheca of C. guanhumi is composed of columnar secretory epithelium and is divided into a dorsal zone and a ventral zone, the latter covered internally by a cuticle layer. Both zones are enveloped by a thin layer of loose connective tissue. Histological cross sections revealed the vagina to be concave, a pattern considered phylogenetically more advanced than the simple, tubular form. Our findings suggest fertilization is internal, favoring sperm from the most recent copulation.     

The female postabdomen and internal genitalia of the basal moth genus Agathiphaga (Insecta: Lepidoptera: Agathiphagidae): morphology and phylogenetic implications

The female postabdomen of Agathiphaga vitiensis terminates in a telescope‐type extensible oviscapt with an apial ‘oviscapt probe’ composed of fused segments behind VIII. Exceptionally within the Lepidoptera two pairs of long ‘anterior apophyses’ arise from segment VIII, from the dorsum and venter. Agathiphaga has the most elaborate postabdominal musculature recorded from female Lepidoptera, comprising 24 muscle sets of which nine may be family autapomorphies. Apophysis musculature does not permit unambiguous homologizing of the single anterior apophysis in Lepidoptera–Glossata with either the dorsal or ventral pair in Agathiphaga, but is compatible with an interpretation of the glossatan anterior apophyses as a composite formation. Nine muscle sets shared with rhyacophilid caddisflies are ascribed to the amphiesmenopteran ground plan. The spermathecal duct represents an intermediate stage between the simple type present in Micropterigidae and the ‘two‐compartment type’ characteristic of almost all other Lepidoptera. The spermatheca has no lagena. The bursa copulatrix is small and simple. Accessory glands are very large, simple sacs. There are 40 + ovarioles per ovary. A terminal cloaca is extremely short. The numerous ovarioles potentially support a sister‐group relationship between Agathiphagidae and all other Lepidoptera, whereas the spermathecal duct histology supports the alternative conservative placement of the family as sister group of all nonmicropterigid Lepidoptera. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159 , 905–920.     

Mating biology of the leaf-cutting ants Atta colombica and A. cephalotes

Copulation behavior has often been shaped by sexually selected sperm competition or cryptic female choice. However, manipulation of previously deposited ejaculates is unknown in the social Hymenoptera and the degree to which sperm competes after insemination or is actively selected by females has remained ambiguous. We studied the mating process in the leaf-cutting ants Atta colombica and A. cephalotes, which belong to one of the few derived social insect lineages where obligate multiple mating has evolved. As copulations often occur at night and in remote places, direct observations were impossible, so we had to reconstruct the sequential copulation events by morphological analysis of the male and female genitalia and by tracking the process of sperm transfer and sperm storage. We show that Atta male genitalia have two external rows of spiny teeth, which fit into a specialized pouch organ in the female sexual tract. Reconstruction of the sperm storage process indicated that sperm is transferred to the spermatheca during or immediately after ejaculation and without being mixed with sperm and seminal fluids from other males. A convergent mechanism of direct sperm transfer to the spermatheca of queens is known from two species of dwarf honeybees. Direct sperm transfer may restrict female control over the sperm storage process and the number of males that contribute to the stored sperm.     

Sperm use economy of honeybee (Apis mellifera) queens

The queens of eusocial ants, bees, and wasps only mate during a very brief period early in life to acquire and store a lifetime supply of sperm. As sperm cannot be replenished, queens have to be highly economic when using stored sperm to fertilize eggs, especially in species with large and long‐lived colonies. However, queen fertility has not been studied in detail, so that we have little understanding of how economic sperm use is in different species, and whether queens are able to influence their sperm use. This is surprising given that sperm use is a key factor of eusocial life, as it determines the fecundity and longevity of queens and therefore colony fitness. We quantified the number of sperm that honeybee (Apis mellifera) queens use to fertilize eggs. We examined sperm use in naturally mated queens of different ages and in queens artificially inseminated with different volumes of semen. We found that queens are remarkably efficient and only use a median of 2 sperm per egg fertilization, with decreasing sperm use in older queens. The number of sperm in storage was always a significant predictor for the number of sperm used per fertilization, indicating that queens use a constant ratio of spermathecal fluid relative to total spermathecal volume of 2.364 × 10^?6 to fertilize eggs. This allowed us to calculate a lifetime fecundity for honeybee queens of around 1,500,000 fertilized eggs. Our data provide the first empirical evidence that honeybee queens do not manipulate sperm use, and fertilization failures in worker‐destined eggs are therefore honest signals that workers can use to time queen replacement, which is crucial for colony performance and fitness.     

Distortion of the spermathecae of phytoseiid mites (Acari: Phytoseiidae) in slide preparation

The shape and dimensions of the spermathecae are taxonomically important characteristics in phytoseiid mites. In experiments with Neoseiulus californicus (McGregor) and Typhlodromus pyri Scheuten, the shape of the cervix of the spermatheca changed considerably and its diameter was increased by 42–49% when mites were flattened, compared to being mounted with 140m spacers underneath the coverslips. Dimensions of the dorsal shield were also affected by flattening, increasing by 3–5%.