Intersexual cooperation during male clasping of external female genitalia in the spider Physocyclus dugesi (Araneae, Pholcidae)

Sexual conflict may influence the shape and evolution of body structures that males use to grasp females during mating. Not only sexual coercion but also intersexual cooperation may be involved during clasping behavior. Among pholcid spiders, secondary sexual modifications of the male chelicerae, such as apophyses with spines or tooth-like processes, function to grasp the female by specific parts of her external genitalia such as grooves or apophyses of the epigynum. We analyzed how the female and the male respond when their structures for clasping are experimentally modified in the pholcid Physocyclus dugesi. We used three treatment groups for virgin females that differed in the manipulation of the epigynum apophyses (uncovered, partially covered, and fully covered by a plaster) and two groups of males (uncovered and fully covered cheliceral apophyses). We found that females are mainly cooperative to courting males not only when the female genital apophyses were experimentally covered but also when the male cheliceral apophyses were covered. The current data also indicate behavioral flexibility in males during courtship, especially when they had difficulty in genital intromission. Our experimental results, together with previous observational studies, support a modulated-cooperative scenario between the sexes for cheliceral clasping and genital intromission in pholcid spiders.     

Copulation behaviour of Glossina pallidipes (Diptera: Muscidae) outside and inside the female, with a discussion of genitalic evolution

If species-specific male genitalia are courtship devices under sexual selection by cryptic female choice, then species-specific aspects of the morphology and behaviour of male genitalia should often function to stimulate the female during copulation. The morphology and behaviour of the complex, species-specific male genitalia of the tsetse fly, Glossina pallidipes Austen, were determined from both direct observations and dissections of flash-frozen copulating pairs; we found that some male genitalic traits probably function to stimulate the female, while others function to restrain her. The male clamps the ventral surface of the female's abdomen tightly with his powerful cerci. Clamping does not always result in intromission. Clamping bends the female's body wall and her internal reproductive tract sharply, posteriorly and dorsally, and pinches them tightly. The male performed sustained, complex, stereotyped, rhythmic squeezing movements with his cerci that were not necessary to mechanically restrain the female and appeared instead to have a stimulatory function. Six different groups of modified setae on and near the male's genitalia rub directly against particular sites on the female during squeezing. The designs of these setae correlate with the force with which they press on the female and the probable sensitivity of the female surfaces that they contact. As expected under the hypothesis that these structures are under sexual selection by female choice, several traits suspected to have stimulatory functions have diverged in G. pallidipes and its close relative, G. longipalpis. Additional male non-genitalic behaviour during copulation, redescribed more precisely than in previous publications, is also likely to have a courtship function. The elaborate copulatory courtship behaviour and male genitalia may provide the stimuli that previous studies showed to induce female ovulation and resistance to remating.     

Cryptic forcible insemination: male snakes exploit female physiology, anatomy, and behavior to obtain coercive matings

Whether males can inseminate uncooperative females is a central determinant of mating system evolution that profoundly affects the interpretation of phenomena such as multiple mating by females, mate choice, reproductive seasonality, and courtship tactics. Forcible insemination is usually inferred from direct physical battles between the sexes and has been dismissed on intuitive grounds for many kinds of animals. For example, snakes have elongate flexible bodies (making it difficult for a male to restrain a female physically), males are typically smaller than females, and copulation requires female cloacal gaping to enable intromission. Male garter snakes (Thamnophis sirtalis) do not display any overt aggression during courtship and simply lie over the female and exhibit rhythmic pulsating caudocephalic waves of muscular contraction; previous studies have interpreted this behavior as a mechanism for eliciting female receptivity. In contrast, we show that male garter snakes forcibly inseminate females. They do so by taking advantage of specific features of snake physiology, respiratory anatomy, and antipredator behavior. The snake lung extends along most of the body, with the large posterior section (the saccular lung) lacking any respiratory exchange surface. Rhythmic caudocephalic waves by courting male garter snakes push anoxic air from the saccular lung forward and across the respiratory surfaces such that females cannot obtain oxygen. Their stress response involves cloacal gaping, which functions in other contexts to repel predators by extruding feces and musk but in this situation permits male intromission. Thus, superficially benign courtship behaviors may involve cryptic coercion even in species for which intuition dismisses any possibility of forcible insemination.     

Female behaviour and the interaction of male and female genital traits mediate sperm transfer during mating

Natural selection and post‐copulatory sexual selection, including sexual conflict, contribute to genital diversification. Fundamental first steps in understanding how these processes shape the evolution of specific genital traits are to determine their function experimentally and to understand the interactions between female and male genitalia during copulation. Our experimental manipulations of male and female genitalia in red‐sided garter snakes (Thamnophis sirtalis parietalis) reveal that copulation duration and copulatory plug deposition, as well as total and oviductal/vaginal sperm counts, are influenced by the interaction between male and female genital traits and female behaviour during copulation. By mating females with anesthetized cloacae to males with spine‐ablated hemipenes using a fully factorial design, we identified significant female–male copulatory trait interactions and found that females prevent sperm from entering their oviducts by contracting their vaginal pouch. Furthermore, these muscular contractions limit copulatory plug size, whereas the basal spine of the male hemipene aids in sperm and plug transfer. Our results are consistent with a role of sexual conflict in mating interactions and highlight the evolutionary importance of female resistance to reproductive outcomes.     

Experimental modifications imply a stimulatory function for male tsetse fly genitalia,supporting cryptic female choice theory

One of the most sweeping of all patterns in morphological evolution is that animal genitalia tend to diverge more rapidly than do other structures. Abundant indirect evidence supports the cryptic female choice (CFC) explanation of this pattern, which supposes that male genitalia often function to court females during copulation; but direct experimental demonstrations of a stimulatory function have been lacking. In this study, we altered the form of two male genital structures that squeeze the female’s abdomen rhythmically in Glossina pallidipes flies. As predicted by theory, this induced CFC against the male: ovulation and sperm storage decreased, while female remating increased. Further experiments showed that these effects were due to changes in tactile stimuli received by the female from the male’s altered genitalia, and were not due to other possible changes in the males due to alteration of their genital form. Stimulation from male genital structures also induces females to permit copulation to occur. Together with previous studies of tsetse reproductive physiology, these data constitute the most complete experimental confirmation that sexual selection (probably by CFC) acts on the stimulatory properties of male genitalia.     

Coevolution of male and female genital morphology in waterfowl

Most birds have simple genitalia; males lack external genitalia and females have simple vaginas. However, male waterfowl have a phallus whose length (1.5->40 cm) and morphological elaborations vary among species and are positively correlated with the frequency of forced extra-pair copulations among waterfowl species. Here we report morphological complexity in female genital morphology in waterfowl and describe variation vaginal morphology that is unprecedented in birds. This variation comprises two anatomical novelties: (i) dead end sacs, and (ii) clockwise coils. These vaginal structures appear to function to exclude the intromission of the counter-clockwise spiralling male phallus without female cooperation. A phylogenetically controlled comparative analysis of 16 waterfowl species shows that the degree of vaginal elaboration is positively correlated with phallus length, demonstrating that female morphological complexity has co-evolved with male phallus length. Intersexual selection is most likely responsible for the observed coevolution, although identifying the specific mechanism is difficult. Our results suggest that females have evolved a cryptic anatomical mechanism of choice in response to forced extra-pair copulations.     

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.     

Indirect partner choice through manipulation of male behaviour by female fowl, Gallus gallus domesticus

The direct and indirect consequences of female copulatory behaviour for copulation success have seldom been quantified. In feral fowl, most copulations were forced by males and copulation success was determined by two factors. First, female differential resistance and solicitation directly affected copulation success and were displayed non-randomly with respect to male social status. Second, another female copulatory behaviour, the distress call, had an indirect effect on both copulation success and the quality of copulation partners. Distress calls triggered male attention to a copulation, which increased the probability of higher-ranking males than the copulating male disrupting the copulation and inseminating the calling female. Females preferentially uttered distress calls when mounted by low-ranking males. Both copulation resistance and distress calling influenced copulation success, but only distress calling increased the probability of copulation disruption by other males. Consistent with the effect of direct selection, differential distress calling indirectly biased copulation success in favour of dominant males. Female fowl may thus ameliorate the effect of male sexual coercion by manipulating male behaviour.     

Conflict resolution in the Odonata: implications for understanding female mating patterns and female choice

Predictions of mating patterns in animals have focused on males and how they compete for fertilizations by controlling females. With reference to the Odonata, a taxon in which mating requires cooperation of the female, the active role that females play in mating decisions is often ignored, leading to the premature conclusion that male coercion of females is common. A critical review of the outcome of sexual conflict among odonates leads me to alternative explanations of female mating patterns that need to be refuted before concluding that males coerce matings. Because Anisoptera males have greater control over tandem formation, they have a greater potential for coercion than Zygoptera males. However, Anisoptera females may simply be willing to remate more often if they receive insufficient sperm to fertilize an entire egg clutch. Contrary to prior assumptions, in both suborders, male defence of oviposition sites does not preclude females from choosing among sites or among males. I find that the evolution of non-aggressive sexual signals by males is a reliable indication that sexual conflict has been resolved in favour of female interests. Although I predict that the benefits to females of choice of male phenotype should rarely exceed the cost of such discrimination in Odonata, female choice is most likely to evolve in territorial species whose males must endure high physiological stress in order to mate, and when site quality is not a reliable predictor of the genetic quality of a potential mate.     

Female reproductive strategies in orangutans,evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion

Intersexual conflicts over mating can engender antagonistic coevolution of strategies, such as coercion by males and selective resistance by females. Orangutans are exceptional among mammals for their high levels of forced copulation. This has typically been viewed as an alternative mating tactic used by the competitively disadvantaged unflanged male morph, with little understanding of how female strategies may have shaped and responded to this behaviour. Here, we show that male morph is not by itself a good predictor of mating dynamics in wild Bornean orangutans but that female conception risk mediated the occurrence and quality of male–female interactions. Near ovulation, females mated cooperatively only with prime flanged males who they encountered at higher rates. When conception risk was low, willingness to associate and mate with non-prime males increased. Our results support the hypothesis that, together with concealed ovulation, facultative association is a mechanism of female choice in a species in which females can rarely avoid coercive mating attempts. Female resistance, which reduced copulation time, may provide an additional mechanism for mate selection. However, coercive factors were also important as prime males were frequently aggressive to females and females used mating strategies consistent with infanticide avoidance.     

Complex copulatory behavior and the proximate effect of genital and body size differences on mechanical reproductive isolation in the millipede genus Parafontaria

The role of species-specific genitalia in reproductive isolation is unclear. Males of the millipede genus Parafontaria use gonopods (modified eighth legs) charged with sperm from the genital openings of the second legs as intromittent organs. Males perform both preliminary and true intromission during mating. During preliminary intromission, a male attempts to insert his gonopods into the female genitalia before charging the gonopods with sperm. If this intromission is completed, it is followed by the ejaculation of sperm to the gonopods and true intromission for insemination. In two sympatric species of Parafontaria that lack effective precopulatory isolation, copulation was terminated without insemination because of preliminary intromission failure caused by mismatched genital and body sizes. Thus, mechanical isolation between these sympatric species resulted from morphological differentiation mediated by the obligatory preliminary intromission. These findings demonstrate the proximate importance of genital and body size differences for reproductive isolation within this genus of millipede.     

Female-limited polymorphism in the copulatory organ of a traumatically inseminating insect

Sexual conflict can produce several evolutionary outcomes, one of which is female-limited trait polymorphism. We examine the African bat bug Afrocimex constrictus (Cimicidae), a species where both sexes are subjected to traumatic intromission from males. We show that males possess female genital structures that in related species ameliorate the costs of traumatic insemination. Moreover, the male form of these structures differs morphologically from the standard female form. Examination of females in our isolated study population revealed a discrete polymorphism in female genitalia. Some females had the typical cimicid form, while others had genitalia that more closely resembled the distinctive male form. Males, as well as females with the distinctive male form, experienced fewer traumatic copulations than the typical female morph. We propose that some females mimic the bizarre male condition in order to reduce the frequency of costly traumatic inseminations. To our knowledge this is the first example of a distinct female-limited genital polymorphism: its nature, as well as its association with traumatic sexual interactions, strongly suggests that sexual conflict underpins this unique phenomenon.     

Persistent courtship reduces male and female longevity in captive tsetse flies Glossina morsitans morsitans Westwood (Diptera: Glossinidae)

Where males can increase their mating success by harassing femalesuntil they accept copulation, harassing tactics can be expectedto evolve to a point where they have costs to the longevityof both sexes. By experimentally manipulating the sex ratioin captive groups of tsetse flies Glossina morsitans morsitans,we demonstrated that the longevity of females declines wheresex ratios are biased toward males, while the longevity of malesdeclines where the sex ratio is biased toward females. Neitherirradiation of males nor prevention of copulation by blockingor damaging the external male genitalia increased the longevityof females caged with them, suggesting that female longevitywas reduced by the physical aspects of male harassment ratherthan by components of the ejaculate     

Male competition reverses female preference for male chemical cues

Females must choose among potential mates with different phenotypes in a variety of social contexts. Many male traits are inherent and unchanging, but others are labile to social context. Competition, for example, can cause physiological changes that reflect recent wins and losses that fluctuate throughout time. We may expect females to respond differently to males depending on the outcome of their most recent fight. In Bolitotherus cornutus (forked fungus beetles), males compete for access to females, but copulation requires female cooperation. In this study, we use behavioral trials to determine whether females use chemical cues to differentiate between males and whether the outcome of recent male competition alters female preference. We measured female association time with chemical cues of two size‐matched males both before and after male–male competition. Females in our study preferred to associate with future losers before males interacted, but changed their preference for realized winners following male competitive interactions. Our study provides the first evidence of change in female preference based solely on the outcome of male–male competition.     

Intromission Induces and Insemination Reduces Female Immune Response in the Medfly

Sexual reproduction exposes females to immune threats. The immune response of females to these threats may conflict with male reproductive interests. We examine the hypothesis that in the Mediterranean fruit fly, Ceratitis capitata, female immune activity during and after copulation reflects this conflict, and its resolution. By comparing the temporal changes in immune status of females paired with normal males to virgin females of the same age, or to those paired with surgically altered males (that perform normal courtship without intromission), we determined the specific effects of courtship, intromission and insemination on female immune response. At the initiation of mating, levels of the immune enzyme Phenoloxidase (PO) were higher in mated females compared to virgin females. Females who copulated with normal males, compared to females paired with males lacking external genitalia, had significantly higher levels of PO. However, 2 h after the beginning of mating PO levels decreased significantly, and increased again 24 h later. These changes may be interpreted as a sequential resolution of the ongoing conflict of interest between males and females, with the advantage shifting from one sex to another.     

Female sexual behavior displayed by androgenized female rhesus macaques

Adult, prenatally androgenized female rhesus macaques (female pseudohermaphrodites) that had been ovariectomized were treated with estradiol benzoate (20 micrograms/day) and paired with males at weekly intervals for 4 weeks beginning on Day 12 of injection. Their sexual behavior was compared to that of a control group of females. The sexual behavior of the males toward the two groups of genetic females (control females with normal female genitalia and hermaphrodites with well-formed male genitalia) was also observed. Females and hermaphrodites were equally receptive to male invitations to copulate. Although there were some differences in the specific components of proceptive behavior displayed by the two groups, the overall differences were negligible. Earlier studies had shown that infant and juvenile hermaphrodites resemble males in patterns of play and sexual behavior. When treated with testosterone as adults and paired with receptive females, they displayed mounting patterns typical of males--one of seven hermaphrodites achieved intromission and ejaculated. It has now been demonstrated that when treated with estrogen and paired with males, they responded as females. Hence, the capacity to behave sexually as males is not incompatible with the capacity to respond sexually as females under certain hormonal and environmental conditions.     

Physical Restraint or Stimulation? The Function(s) of the Modified Front Legs of Male Archisepsis diversiformis (Diptera, Sepsidae)

Four hypotheses that could explain the elaborate species-specific morphology of the clasping organs on the front legs of male Archisepsis diversiformis flies were tested: direct male–male combat, mechanical fit, male–female conflict of interests, and male stimulation of the female. Experimental modification of the shape of the male clasper and of the female wing base where the male clasped the female both strongly reduced the chances that a mount would result in copulation. This reduction was not predicted by the male–male combat hypothesis but was predicted by the others. Males in the field did nave to fight other males to remain mounted on females, as expected by the male–male combat hypothesis. Reduced male copulatory success was not due to inferior male ability to grasp and hold onto the female's wings, as predicted by the mechanical fit and male–female conflict hypotheses but to a reduction in the likelihood that the female would allow intromission, as predicted by the stimulation hypothesis. By a process of elimination, and in combination with data from a previous morphological study, the data support the hypothesis that the species-specific aspects of grasping organs in these flies function to stimulate females. Further behavioral data will be needed to test alternative possibilities.     

The retrolateral tibial apophysis in spiders—shaped by sexual selection?

The functional significance of the retrolateral tibial apophysis (rta) on the male pedipalps in four spider species with different mating positions is investigated with the help of histological serial sections prepared after freeze-fixing copulating pairs with liquid nitrogen. The results of this study, as well as most data in previous works, suggest that the rta is mostly used to fix the male pedipalp to the female epigyne in order to ensure the intromission of the sperm transferring embolus. This is in accordance with the female choice hypothesis on genitalia which predicts that species-specific genital structures should directly or indirectly contact the female during copulation and thus be shaped by sexual selection.     

Male copulatory sensory stimulation induces female ejection of rival sperm in a damselfly

Male damselflies possess very specialized genitalia. Females mate multiply and store sperm in two sperm storage organs, the bursa copulatrix and the spermatheca. During copulation, males physically remove the sperm stored in these organs using their genitalia. I document a novel mechanism by which males gain access to the spermatheca in Calopteryx haemorrhoidalis asturica. The mechanism is based on male stimulation of the female sensory system that controls egg fertilization and laying. During copulation, the aedeagus (a male genitalic structure indirectly involved in sperm transfer) distorts the cuticular plates in the female genital tract that bear mechanoreceptive sensilla. This stimulation results in sperm ejection from the spermatheca. Aedeagus width is positively correlated with the amount of sperm ejected. I propose that males have exploited a pre-existing female sensory bias to gain access to otherwise physically unreachable sperm. These results shed light on the issue of the origin of female preferences in current models of sexual selection and on the evolution of genitalia via sexual selection. It is postulated that females might use this process as a form of post-copulatory sexual selection on the basis of males'' genitalia.