Fitness advantages of the biased use of paired laterally symmetrical penises in an insect

The evolution of laterality, that is 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 [OR] of 3.50) and insemination (probability of transferring a detectable amount of sperm: OR 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.     

Behavioral and morphological asymmetries in chukar Alectoris chukar copulation

Birds often exhibit greater reproductive tract development on the left side than right side. Behavioral evidence from the three species for which data has been published indicates that these species copulate more frequently on the left side of females than on the right side. Missing from the literature are studies that compare asymmetry in copulation behavior to asymmetry in reproductive tract morphology of the same individuals of both sexes within a single species. To better understand the potential for cryptic sexual selection to influence avian copulation, we measured asymmetries in chukar Alectoris chukar copulation using 24 male and 29 female chukar brought into captivity from the wild. Chukar copulated (n=37) more from the left side (n=30) of females than the right side (n=7). The left testis of males was consistently greater in size, mass and volume than the right testis. The left ovary and oviduct of females was consistently functional with no observable development of the right ovary or oviduct. Left-side bias in direction of copulation, larger left testes, and functional left vaginal openings may act in concert to deliver spermatozoa to the oviduct, promoting fertilization.     

Presence of an adipokinetic peptide in the corpus cardiacum of Dermaptera but not in the neurohaemal aorta, and chemical and functional identification of the peptide

Corpora cardiaca of the earwigs Labidura riparia and Forficula auricularia contain a substance that causes hyperlipaemia in migratory locusts and hypertrehalosaemia in the American cockroaches. A conspecific bioassay in L. riparia revealed that this factor is lipid-mobilizing. Isolation of the neuropeptide was achieved by single-step RP-HPLC. The primary structure of the earwig adipokinetic peptide was elucidated by automated Edman degradation in combination with matrix-assisted laser desorption/ionization mass spectrometry. It is a blocked octapeptide, pGlu-Val-Asn-Phe-Ser-Thr-Gly-Trp-NH₂, previously denoted as Grb-AKH and first identified in Gryllus bimaculatus ( Gäde & Rinehart 1987 ). The synthetic peptide co-chromatographed under various conditions with the native peptide and, in biological assays, resulted in lipid-mobilization in L. riparia when injected in low concentration.     

Impact of cryptic female choice on insemination success: Larger sized and longer copulating male squid ejaculate more,but females influence insemination success by removing spermatangia

In polyandrous mating systems, sperm competition and cryptic female choice (CFC) are well recognized as postcopulatory evolutionary forces. However, it remains challenging to separate CFC from sperm competition and to estimate how much CFC influences insemination success because those processes usually occur inside the female's body. The Japanese pygmy squid, Idiosepius paradoxus, is an ideal species in which to separate CFC from sperm competition because sperm transfer by the male and sperm displacement by the female can be observed directly at an external location on the female's body. Here, we counted the number of spermatangia transferred to, removed from, and remaining on the female body during single copulation episodes. We measured behavioral and morphological characteristics of the male, such as duration of copulation and body size. Although males with larger body size and longer copulation time were capable of transferring larger amounts of sperm, females preferentially eliminated sperm from males with larger body size and shorter copulation time by spermatangia removal; thus, CFC could attenuate sperm precedence by larger males, whereas it reinforces sperm precedence by males with longer copulation time. Genetic paternity analysis revealed that fertilisation success for each male was correlated with remaining sperm volume that is adjusted by females after copulation.     

Filariomyces forficulae: occurrence and effects on the predatory earwig, Labidura riparia

Filariomyces forficulae occurs commonly on the earwig, Labidura riparia, in Florida. The hypopial stage of a mite, Histiostoma sp., often associated with L. riparia is also sometimes infected by the same fungus. Some other earwig species that occur with L. riparia were not found to be hosts. Sites of fungal infection on the earwig were highly variable and influenced by several factors. F. forficulae was transmitted by several types of insect contact including mating with varying efficiencies and by a mechanical inoculation technique. Developmental time required by the fungus from ascospore to mature perithecia was 10–12 days at 24°C. In laboratory studies there were small but consistent differences between longevities of infected and noninfected groups of earwigs and infected populations of earwigs died sooner than noninfected ones. Infection resulted in differences in pattern of egg production; however, no numerically significant differences in total egg production or egg-hatching ability between the two groups were found.     

Sperm transfer during mating in the pharaoh's ant, Monomorium pharaonis

Abstract.  Sperm transfer in the pharaoh's ant Monomorium pharaonis (L.) is studied by making longitudinal sections through the gasters of mating pairs fixed in copula. Sperm is transferred inside a spermatophore similar to those found in two other ants, Diacamma sp. from Japan and Carebara vidua . Sharp teeth-ridges are present on the penis valves and, during copulation, these teeth make contact with a thick and soft cuticular layer covering the bursa copulatrix. This ensures an attachment long enough for the successful transfer of the spermatophore to the right position inside the female oviduct. The thick cuticle also protects the queen from serious damage by the male's sharp claspers. After a first successful copulation, sperm is still present inside the male's seminal vesicles, suggesting that males can mate multiply. Additional experiments, where single, initially virgin males are presented to several virgin females, confirm this.     

Novel copulatory structures and reproductive functions in Amphiboloidea (Gastropoda, Heterobranchia, Pulmonata)

Abstract. Two new families of amphiboloid gastropods were recently erected, largely due to the very distinct structural and functional configurations of their distal reproductive systems. The spermovipositors in monaulic Salinator spp. (Amphibolidae) are functionally unique in Gastropoda, and it is suggested that they perform both oviposition and sperm transfer/receipt during non-reciprocal copulation. In contrast, the remarkably complex penises in syntremous diaulic Phallomedusa spp. (Phallomedusidae) are used exclusively for sperm transfer during reciprocal copulation. The phallomedusid penis is structurally unique among gastropods because it is protruded by pivoting around a fixed point rather than extending by eversion, and bears elaborate appendages to improve traction during copulation. The complex and functionally ambiguous distal reproductive structures of Maningrida (Maningrididae) differ from other amphibolids in the arrangement and structure of their prostate and copulatory structures. Genital armature of varying complexity occurs in all amphiboloidean families. There may be a correlation between the absence of a long-term sperm storage structure (spermatheca) and the evolutionary diversification of copulatory structures in these gastropods.     

The functional morphology of penile erection: tissue designs for increasing and maintaining stiffness

Inflatable penises have evolved independently at least fourtimes in amniotes, specifically in mammals, turtles, squamates,and the archosaurs. Males in these lineages therefore sharethe functional problem of building a penis out of soft and flexibletissues that can increase its flexural stiffness and resistbending during copulation. Research on penile erectile tissuesin mammals and turtles shows that these two taxa have convergentlyevolved an axial orthogonal array of collagen fibers to reinforcethe penis during erection and copulation; in both lineages,the collagen fibers in the array are crimped and folded in theflaccid penis. Collagen fiber straightening during erectionincreases the stiffness of the tissue and allows changes inpenile radius that increase its second moment of area: bothof these changes increase the flexural stiffness of the penisas a whole. And once erect, axial orthogonal arrays have thehighest flexural stiffness of any fiber arrangement. The highdegree of anatomical convergence (to the level of microanatomicalfeatures) within mammals and turtles suggests that the stiffnessrequirements for copulation produce an extremely restrictiveselective regime in organisms that evolve inflatable penises.     

Unique set of copulatory organs in mantises: Concealed female genital opening and extremely asymmetric male genitalia

Several insects exhibit strong asymmetry in male genital shape, but the functions of this asymmetry is unknown. In the four species of the family Mantidae belonging to the genera Tenodera, Statilia and Hierodula, male genitalia consist of a more complex left‐side lobe, with two well‐pointed sclerotized processes, the apical process (paa) and the distal process (pda). Female genitalia are symmetric, and the genital opening (gonopore) is concealed by placement of the ovipositor (ovi) into the subgenital plate (sgp). Mating with experimental males, in which either paa or pda was cut, demonstrated that paa is essential for successful copulation. By fluorescence detection of the surface of females mated with males in which the paa was coated with fine fluorescent beads, the paa attachment site was determined to be the left edge of the female sgp. This finding suggests that copulation begins with exposure of the female gonopore by the male hooking the paa to the sgp and unfastening the ovi from the sgp, as associated with other parts of the male genitalia. The extremely asymmetric male genitalia also determine their mating posture. The male, mounting the female, bends his abdomen from the right side of his mate to attach his paa to her sgp. We found no antisymmetry in male genitalia, and never observed reversal (leftward) abdominal bending by the males. This was the fixed mating posture, even in virgin males, suggesting its innateness.     

Axial orthogonal fiber reinforcement in the penis of the Nine-banded Armadillo (Dasypus novemcinctus)

Examination of histological sections from flaccid and artificially erected nine-banded armadillo (Dasypus novemcinctus) penises confirms that the mammalian corpus cavernosum is the first known biological hydrostat reinforced by collagen fibers arranged at 0° and 90° to its long axis. The morphology of this axial orthogonal fiber array affects the mechanical behavior of mammalian penises during erection and copulation. Specifically, the axial orthogonal array gives the erect penis a reproducible shape, maximum size and resistance to tensile, compressive, and bending forces. These features are more appropriate for the mechanical regime associated with copulation than those found in structures reinforced by crossed-helical fibers, although the axial orthogonal array also gives the corpus cavernosum a tendency to fail by kinking. Crimped collagen fibers in the flaccid array as well as three-dimensional folding of the wall in the flaccid corpus cavernosum allow the structure to expand during erection. J. Morphol. 233:249–255, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Why Did a Female Penis Evolve in a Small Group of Cave Insects?

The evolution of a female penis is an extremely rare event and is only known to have occurred in a tribe of small cave insects, Sensitibillini (Psocodea: Trogiomorpha: Prionoglarididae). The female penis, which is protrudable and inserted into the male vagina‐like cavity during copulation to receive semen, is thought to have evolved independently twice in this tribe, in the Brazilian Neotrogla and the African Afrotrogla. These findings strongly suggest that there are some factors unique to Sensitibillini that have facilitated female penis evolution. Here, several hypothetical factors are presented that may have enabled the evolution of the female penis in Sensitibillini. The female–female competition for nutritious semen, the oligotrophic environment, and the twin insemination slots with switching valve are considered to be the driving factors for female penis evolution. Additionally, the following factors are considered responsible for relaxing the constraint against female penis evolution: preexistence of the female‐above mating position, the elongated duct connecting the female pre‐penis with the sperm storage organ, and the small male genital cavity accepting the female genital tubercle bearing the opening of this duct. Understanding the factors enabling female penis evolution may also shed light on the evolution of the male penis.     

Phylogeny of earwigs (Insecta: Dermaptera) based on molecular and morphological evidence: reconsidering the classification of Dermaptera

Abstract. Dermaptera (earwigs) is a cosmopolitan order of insects, the phylogenetic relationships of which are poorly understood. The phylogeny of Dermaptera was inferred from large subunit ribosomal (28S), small subunit ribosomal (18S), histone-3 (H3) nuclear DNA sequences, and forty-three morphological characters. Sequence data were collected for thirty-two earwig exemplar taxa representing eight families in two suborders: Hemimeridae (suborder Hemimerina); Pygidicranidae, Anisolabididae, Labiduridae, Apachyidae, Spongiphoridae, Chelisochidae and Forficulidae (suborder Forficulina). Eighteen taxa from ten additional orders were also included, representing Ephemeroptera, Odonata, Orthoptera, Phasmida, Embiidina, Mantodea, Isoptera, Blattaria, Grylloblattodea and Zoraptera. These data were analysed via direct optimization in poy under a range of gap and substitution values to test the sensitivity of the data to variations in parameter values. These results indicate that the epizoic Hemimerus is not sister to the remaining Dermaptera, but rather nested as sister to Forficulidae + Chelisochidae. These analyses support the paraphyly of Pygidicranidae and Spongiphoridae and the monophyly of Chelisochidae, Forficulidae, Anisolabididae and Labiduridae.     

Identification of 10 microsatellite loci in the earwig Labidura riparia (Dermaptera,Labiduridae)

Ten microsatellite loci were isolated from the earwig Labidura riparia (Pallas, 1773). The polymorphism of the loci was assessed in 24 individuals from one population. The number of alleles ranged from four to 11 alleles and observed and expected heterozygosities from 0.250 to 0.833 and from 0.551 to 0.861, respectively.     

Inter‐population mating success in Australian dengue vector mosquitoes: effects of laboratory colonization and implications for the spread of transgenics

Variability between Aedes aegypti populations in north Queensland, Australia, has the potential to impact the successful implementation of new population replacement mosquito releases for dengue control. Four Ae. aegypti colonies originating from different locations (Cairns, Mareeba, Innisfail, and Charters Towers), along with one F1 field‐derived population from Cairns, were inter‐crossed to determine any incompatibilities in copulation, insemination, and production of viable offspring. Greater copulation and insemination rates were observed when males recently introduced from the wild (‘Cairns‐Wild’ population) were mated with long‐term laboratory females. Egg viability rates for all crosses ranged from 90.2–98.2%, with no significant differences observed between crosses. Greater egg production was seen in some populations, and when corrected for wing‐length, egg production was greatest in a Mareeba x Innisfail cross (19.55 eggs/mm wing length) and lowest for the Charters Towers intra‐population cross (14.35 eggs/mm). Additionally, behavioral differences were observed between laboratory and wild mosquitoes from the Cairns location, suggesting possible laboratory conditioning. Finally, despite controlled larval rearing conditions, size differences between populations existed with Charters Towers mosquitoes consistently smaller than the other populations. The spread of genes or bacterial symbionts between these populations is unlikely to be hindered by pre‐existing reproductive barriers.     

Histomorphology of the glans penis in Vespertilionidae and Phyllostomidae species (Chiroptera,Mammalia)

The penises of bats are taxonomically distinctive in size and shape. In addition, they are variable in microscopic anatomy, indicating that histomorphological studies of copulatory organs of bats may help understanding their successful reproductive strategies. We studied adult males of 13 species of vespertilionid and phyllostomid bats. Both families exhibited the basic structure of the vascular penis of mammals: the hydrostatic elements of the corpora cavernosa and the corpus spongiosum surrounding the urethra, as well as accessory cavernous tissue. Variation in the position and amount of the tissues were observed in these families. Vespertilionid bats have a small glans penis with abundant accessory cavernous tissue on the prepuce and a highly variable baculum. The baculum varied in size and morphology, even among congeneric species, such as the three Lasiurus species and the two Myotis species. Phyllostomid species possess no bacula, but vascular structures are present to produce penile stiffening, particularly on the glans. Variation in the microscopic anatomy of the phyllostomid prepuce was observed, for example, Artibeus species had accessory cavernous tissue surrounded by a tunica albuginea, but Carollia perspicillata had two bundles of striated musculature and some adipose tissue; abundant pigments were present in the prepuce of most species.     

How the length of genital parts affects copulation performance in a carabid beetle: implications for correlated genital evolution between the sexes

To identify factors leading to the correlated evolution of exaggerated male and female genitalia, we studied the effects of the variable dimensions of corresponding functional genital parts (male copulatory piece and female vaginal appendix) on copulatory performance in the polygamous carabid beetle Carabus (Ohomopterus) maiyasanus. We used mating pairs of individuals from two populations to increase the variances in genital dimensions and determined the copulation performance (insemination and spermatophore replacement, and copulation time) in single‐ and double‐mating situations. In single mating, insemination success was not affected by genital dimensions, although the copulation time was significantly shorter when the male aedeagus was longer. In the double‐mating experiment, insemination and replacement of spermatophores by the second male succeeded more frequently when the copulatory piece was shorter and the vaginal appendix was longer, and when the difference between the length of the copulatory piece and the vaginal appendix was smaller. Thus, a matching of the corresponding genital parts between the sexes increases the male's reproductive success in sperm competition, but elongation of the copulatory piece cannot be explained simply by the improvement in male reproductive success. We discuss possible factors for the elongation of genital parts in terms of sexual conflict and reproductive interference through interspecific copulation.     

Mating Behavior, Sexual Selection, and Copulatory Courtship in a Promiscuous Beetle

The function of male movements during copulation is unclear. These movements may be a result of the necessary mechanics of insemination, or they may also have further function, for instance, stimulating or courting a female during mating, perhaps influencing female mate choice. We present data from three experiments exploring the mating behavior and copulatory movements of the highly promiscuous beetle Psilothrix viridicoeruleus. Male mating success in the struggle over mating was not related to male or female size (measured by weight) but successful males were more vigorous in terms of copulatory movements. These males took longer to mount females but copulated longer and remained mounted longer. We discuss these results in terms of the mating system of Psilothrix and also in terms of observations of the timing of insemination during copulation. We suggest that copulatory movements in this species are best understood as copulatory courtship.     

A TEST FOR ENVIRONMENTAL EFFECTS ON BEHAVIORAL ISOLATION IN TWO SPECIES OF KILLIFISH

Behavioral isolation is a common and potent mechanism of reproductive isolation. Determining the extent to which behavioral isolation varies with environmental conditions is critical to understanding speciation and the maintenance of species boundaries. Here, we tested the effect of salinity on behavioral isolation (female species recognition, male–male competition, and male species recognition) between two closely related killifish (Lucania goodei and L. parva) that differ in salinity tolerance. We performed no‐choice assays and behavioral trials where males could compete and court females in fresh water (0 ppt) and brackish water (15 ppt). We found high levels of behavioral isolation that did not vary as a function of salinity. In behavioral trials, male species recognition of females was strong and asymmetric between the two species. Lucania goodei males preferred conspecifics and rarely courted or mated with L. parva females. Lucania parva males preferred conspecifics but readily courted and mated with L. goodei females. This asymmetry matches previously documented asymmetries in hybrid offspring fitness. Crosses between L. parva males and L. goodei females produce fully viable/fertile hybrids, but crosses between L. goodei males and L. parva females produce males with reduced fertility. Hence, behavioral isolation may have evolved in part due to reinforcement.     

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.