Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals

The duration of sperm storage by females differs markedly between reptiles (maximum: 2555 d [7 years] and birds (maximum: 117d), with mammals showing both very short (< 1 d) and relatively long periods (maximum: 198 days). The females of many reptiles, probably all birds and some mammals have specialized structures for storing sperm, suggesting that selection for sperm storage has operated on females. Sperm storage, together with delayed implantation and delayed development, separates copulation from fertilization, and hence, copulation from the timing of birth. All three types of separation mechanism occur in mammals. Delayed implantation cannot occur in reptiles and birds because their eggs do not implant, but delayed development occurs in some reptiles. Comparisons among vertebrate classes suggest that sperm storage in the female tract may have an upper limit of a little over 100 days in endotherms: non-hibernating mammals have circumvented this limit by using delayed implantation as an uncoupling mechanism. A long reproductive cycle (up to four years) probably makes sperm storage obligatory for some reptiles. We consider existing hypotheses for prolonged sperm storage and the other reproductive delays, and propose a new hypothesis. Our hypothesis extends Sandell's (1990) hypothesis which states that in mammals delayed implantation has evolved to allow females to time both their copulation and birth seasons optimally. We propose that the other separation mechanisms, namely sperm storage and delayed development, have also evolved for this reason. Sandell suggested that the optimal time for females to copulate is when the opportunities to obtain the best quality male exist, and thus the dislocation of copulation and birth seasons has occurred through sexual selection. We propose that the other two separation mechanisms may also have evolved through sexual selection, in part at least. Of the three separation mechanisms, sperm storage has additional advantages for females in that it also allows them to modify their choice of male after copulation has occurred, through sperm competition. Thus we propose that: (1) all separation mechanisms have evolved when the optimal time for copulation is not compatible with either the optimal time for fertilization (birds) or the optimal time for birth, given a constant gestation period (reptiles, birds and mammals); (2) separation mechanisms have evolved through sexual selection enabling females to improve the quality of the male that fertilizes their eggs, either through pre-copulatory male-male competition (via any of the separation mechanisms) or through post-copulatory sperm competition (via sperm storage).     

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.     

Ultrasonic courtship songs of male Asian corn borer moths assist copulation attempts by making the females motionless

Males of the Asian corn borer moth Ostrinia furnacalis (Guenée) produce an ultrasonic courtship song of extremely low‐intensity during copulation attempts. The song has been shown to significantly increase the mating success of the male; however, the mode of action of the sound in courtship remains to be resolved. Behavioural experiments using pairs with deafened females or muted males show that, without the aid of the sound, 63% of males eventually succeed in mating after several copulation attempts, whereas the remainder (37%) make repeated attempts in vain until interrupted by the escape of the female. Because few (2%) males fail to copulate when females hear the courtship song, it is evident that the song has an effect on females, promoting the success of copulation attempts. In support of this view, males produce louder songs if the first copulation attempt fails, suggesting that the males increase their sound levels to achieve successful copulation. It is suggested that the ultrasonic songs of the male render the females motionless, which is the same response as that to ultrasonic bat calls. Because even slight movements by the female can interfere with the attempt of the male to copulate, it is likely that, by making her motionless, the success rate of a single copulation attempt is increased greatly.     

Sexual coevolution in the traumatically inseminating plant bug genus Coridromius

Sexual conflict has recently been proposed as a driving force behind the rapid diversification of genitalia among sexually reproducing organisms. In traumatically inseminating insects, males stab females in the side of the body with needle‐like genitalia, ejaculating into their body cavity. Such mating is costly to females and has led to the evolution of cost‐reducing ‘paragenitalia’ in some species. Whereas some consider this evidence of sexually antagonistic coevolution, others remain unconvinced. Variation in the reproductive morphology of both sexes – particularly males – is alleged to be negligible, contradicting the expectations of a coevolutionary arms race. Here, we use a phylogeny of the traumatically inseminating plant bug genus Coridromius to show that external female paragenitalia have evolved multiply across the genus and are correlated with changes in male genital shape. This pattern is characteristic of an evolutionary arms race driven by sexual conflict.     

Remote copulation: male adaptation to female cannibalism

Sexual cannibalism by females and associated male behaviours may be driven by sexual conflict. One such male behaviour is the eunuch phenomenon in spiders, caused by total genital emasculation, which is a seemingly maladaptive behaviour. Here, we provide the first empirical testing of an adaptive hypothesis to explain this behaviour, the remote copulation, in a highly sexually cannibalistic orb-web spider Nephilengys malabarensis. We demonstrate that sperm transfer continues from the severed male organ into female genitals after the male has been detached from copula. Remote copulation increases the total amount of sperm transferred, and thus probably enhances paternity. We conclude that the mechanism may have evolved in response to sexual cannibalism and female-controlled short copulation duration.     

Males of the orb-web spider Argiope bruennichi sacrifice themselves to unrelated females

Costs of inbreeding can lead to total reproductive failure and inbreeding avoidance is, therefore, common. In classical sex roles with no paternal care, the selective pressure to avoid inbreeding is mostly on the female, which carries the higher costs. In some orb-web spiders, this situation is very different because females are polyandrous and males are monogynous or at most bigynous. Additionally, females of many entelegyne orb weavers are thought to bias paternity post-copulatorily towards a desired mate. This increases the selective pressure on males to adjust their investment in a mating with regard to the compatibility to a female.Here, we examine whether genetic relatedness influences mating behaviour in the orb-web spider Argiope bruennichi. We mated either a sibling or a non-sibling male to a female in single copulation trials and compared copulation duration, cannibalism rate and female fecundity.Our experiment revealed that males prolonged their copulation duration and were cannibalized more frequently when mating with a non-sibling female. Males mating with a sibling female were more likely to escape cannibalism by copulating briefly, thus presumably increasing their chances of re-mating with a more compatible female. This suggests that males can adaptively adjust their investment relating to the compatibility of a female.     

Restrictive mating by females on black grouse leks

In bird species with pair bonds, extra-pair matings could allow females to choose genetically superior males. This is not needed in lekking species because female choice is not constrained by pairing opportunities. However, polyandry has been reported in most lekking species studied so far. Using 12 microsatellite loci, we determined the paternity of 135 broods of black grouse sampled between 2001 and 2005 (970 hatchlings and 811 adult birds genotyped). The paternity assignments were combined to lek observations to investigate the mating behaviour of black grouse females. About 10% of the matings seemed to take place with males displaying solitarily. Forty per cent of the copulations between males displaying on the studied leks and radio-tagged females were not recorded. This was due to difficulties in identifying the females and because our observations did not cover all the possible time for matings. However, females of the undetected copulations had chosen males that were already known to be successful on the leks. There was a strong consistency between the observations and true paternity, even when the copulation was disturbed by a neighbouring male. Multiple mating and multiple paternities were rare. We can now confidently ascertain that most females mate only once with one male for the whole clutch. This mating behaviour requires that a single insemination is sufficient to fertilize a clutch and that females can determine whether the sperm has been successfully transferred. Grouse Tetraoninae with many lekking species may be the only bird taxon that has evolved these traits.     

Safer sex with feeding females: sexual conflict in a cannibalistic spider

Mating strategies are to a large degree shaped by conflictsbetween the sexes, causing a rapid antagonistic coevolutionof traits involved in reproduction. The view that sexual cannibalismrepresents a form of sexual conflict leads to the predictionof male traits that facilitate escape from cannibalistic females.A variety of traits have been suggested to serve this functionin spiders, where sexual cannibalism is comparatively common.Empirical evidence, however, is virtually absent. Here we showexperimentally that opportunistic mating with feeding females,which has been reported from several species of orb-weavingspiders, greatly reduces the risk of cannibalism and injuryfor males in the spider Nephila fenestrata. This has directconsequences for a male's fertilization success because survivingmales can reduce the female's remating probability by guardingher against rivals. Although copulation with previously matedfemales sometimes appears to be mechanically impossible, secondmales that do copulate can expect to fertilize on average 64%of a female's eggs. Our results support the view that opportunisticmating may have evolved as a male tactic in a context of sexualconflict over sexual cannibalism.     

Climbing to reach females: Romeo should be small

The race for reaching mates by the time they are receptive, or sexual selection by scramble competition, has received little attention. We argue that smaller males are favored in species in which the male must climb to reach females located in high habitat patches. This new explanation we term the "gravity hypothesis" of sexual size dimorphism (SSD). We show that a simple biomechanical model of animal movement predicts that: (1) selection should favor a comparatively smaller size in the searching sex when searching involves climbing; and (2) this effect should be stronger in larger species than in smaller species. In reaching high habitats, smaller, faster searchers will be favored either through sexual selection by scramble competition and/or by escaping predation easier by running faster on vertical surfaces. Different spider species are found at a wide range of heights. We compiled a dataset of spider taxa and arranged their habitats according to four height categories, ranked from soil surface to trees. We show that, after controlling for phylogeny, both predictions of the gravity hypothesis of SSD are met. Thus, it appears that the constraint imposed by gravity on climbing males is a selective factor in determining male dwarfism.