Ultimate Causation of Aggressive and Forced Copulation in Birds: Female Resistance, the CODE Hypothesis, and Social Monogamy

SYNOPSIS. Except in ducks and geese (Anseriforms), aggressiveor forced copulation in birds is rare. The rarity of forcedcopulation in birds theoretically is dueto morphological andphysiological mechanisms of female resistance that place fertilizationmost often under female control. Traits theoretically associatedwith resistance by females include: digestive epithelium liningthe section of the cloaca receiving sperm and powerful doacalmusculature used to eject contents, including waste materialand sperm. These traits suggest that the Immediate FertilizationEnhancement Hypothesis may be an inadequate ultimate explanationfor forced copulation when it occurs. Ideas in Heinroth (1911)and Brownmiller (1975) suggested an alternative, the CODE Hypothesis,which says that aggressive copulation creates a dangerous environmentfor females. This, in turn, fosters male mating advantage viasocial monogamy, because selection sometimes favors femaleswho trade sexual and social access for protection from maleaggression. Thus, theoretically, "trades" of protection forcopulation favor the evolution of social monogamy even in specieswith little or no paternal care. Individual males may accrueselective advantages through direct benefits, kin-selected benefits,or reciprocal altruism. The CODE hypothesis for social monogamypredicts variation in extrapair paternity from preferred mates,variation in male reproductive success, and variation amongfemales' post-insemination resistance mechanisms as functionsof variation among females' vulnerabilities (ecological andintrinsic) to aggressive copulation. Observers will base intraspecifictests on variation among females in their vulnerabilities tomale aggression against them.     

Sperm storage and copulation duration in a sexually cannibalistic spider

Female St Andrew’s Cross spiders control copulation duration by timing sexual cannibalism and may thereby control paternity if cannibalism affects sperm transfer. We have investigated the effect of copulation duration on sperm transfer and documented sperm storage patterns when we experimentally reduced the ability of females to attack and cannibalise the male. Virgin males and females were paired and randomly allocated either to a control treatment, where females were allowed to attack and cannibalise the male during copulation, or to an experimental treatment, where females were unable to cannibalise the male. The latter was achieved by placing a paintbrush against her chelicerae during copulation. Our experimental manipulation did not affect copulation duration or sperm storage. However, the number of sperm stored by the female increased with copulation duration only if the male was cannibalised, suggesting that cannibalism increases relative paternity not only through prolonged copulation duration following a fair raffle model but also through the cannibalism act itself. Future studies should explore whether cannibalised males ejaculate more sperm or whether females selectively store the sperm of cannibalised males.     

Sperm storage mediated by cryptic female choice for nuptial gifts

Polyandrous females are expected to discriminate among males through postcopulatory cryptic mate choice. Yet, there is surprisingly little unequivocal evidence for female-mediated cryptic sperm choice. In species in which nuptial gifts facilitate mating, females may gain indirect benefits through preferential storage of sperm from gift-giving males if the gift signals male quality. We tested this hypothesis in the spider Pisaura mirabilis by quantifying the number of sperm stored in response to copulation with males with or without a nuptial gift, while experimentally controlling copulation duration. We further assessed the effect of gift presence and copulation duration on egg-hatching success in matings with uninterrupted copulations with gift-giving males. We show that females mated to gift-giving males stored more sperm and experienced 17% higher egg-hatching success, compared with those mated to no-gift males, despite matched copulation durations. Uninterrupted copulations resulted in both increased sperm storage and egg-hatching success. Our study confirms the prediction that the nuptial gift as a male signal is under positive sexual selection by females through cryptic sperm storage. In addition, the gift facilitates longer copulations and increased sperm transfer providing two different types of advantage to gift-giving in males.     

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.     

Post-mating prezygotic barriers to gene exchange between hybridizing field crickets

Studies of sexual selection in speciation have traditionally focused on mate preference, with less attention given to traits that act between copulation and fertilization. However, recent work suggests that post-mating prezygotic barriers may play an important role in speciation. Here, we evaluate the role of such barriers in the field crickets, Gryllus firmus and Gryllus pennsylvanicus. Gryllus pennsylvanicus females mated with G. firmus males produce viable, fertile offspring, but when housed with both species produce offspring sired primarily by conspecifics. We evaluate patterns of sperm utilization in doubly mated G. pennsylvanicus females and find no evidence for conspecific sperm precedence. The reciprocal cross (G. firmus female × G. pennsylvanicus male) produces no progeny. Absence of progeny reflects a barrier to fertilization rather than reduced sperm transfer, storage or motility. We propose a classification scheme for mechanisms underlying post-mating prezygotic barriers similar to that used for premating barriers.     

Female infidelity and genetic compatibility in birds: the role of the genetically loaded raffle in understanding the function of extrapair paternity

Despite two decades of research into over one hundred species, the function of extrapair paternity to female birds remains unclear. Recent studies have demonstrated patterns between extrapair paternity and the genetic similarity of females with social partners and extrapair males. We believe that selection on females to gain genetically compatible fathers for their offspring offers a possible general explanation for the function of extrapair paternity. The idea of sexual selection being driven by genetic compatibility is widely considered by workers on other taxa but has been largely ignored by studies of birds. Genetic compatibility could be optimised by females through a behavioural process before copulation or through a postcopulatory process. Postcopulatory processes such as cryptic female choice have been recently demonstrated in birds and would allow female birds to use a 'genetically loaded raffle' to target compatible genes through sperm competition. We discuss the general weaknesses of studies of extrapair paternity to date and suggest a number of avenues for future research that will help to elucidate the function of extrapair paternity and widespread genetic polyandry in birds.     

An integrative view of sexual selection in Tribolium flour beetles

Sexual selection is a major force driving the evolution of diverse reproductive traits. This evolutionary process is based on individual reproductive advantages that arise either through intrasexual competition or through intersexual choice and conflict. While classical studies of sexual selection focused mainly on differences in male mating success, more recent work has focused on the differences in paternity share that may arise through sperm competition or cryptic female choice whenever females mate with multiple males. Thus, an integrative view of sexual selection needs to encompass processes that occur not only before copulation (pre-mating), but also during copulation (peri-mating), as well as after copulation (post-mating), all of which can generate differences in reproductive success. By encompassing mechanisms of sexual selection across all of these sequential reproductive stages this review takes an integrative approach to sexual selection in Tribolium flour beetles (Coleoptera: Tenebrionidae), a particularly well-studied and economically important model organism. Tribolium flour beetles colonize patchily distributed grain stores, and juvenile and adult stages share the same food resources. Adults are highly promiscuous and female reproduction is distributed across an adult lifespan lasting approximately 1 year. While Tribolium males produce an aggregation pheromone that attracts both sexes, there appears to be little pre-mating discrimination among potential mates by either sex. However, recent work has revealed several peri-mating and post-mating mechanisms that determine how offspring paternity is apportioned among a female's mates. During mating, Tribolium females reject spermatophore transfer and limit sperm numbers transferred by males with low phenotypic quality. Although there is some conflicting evidence, male copulatory leg-rubbing appears to be associated with overcoming female resistance to insemination and does not influence a male's subsequent paternity share. Evidence suggests that Tribolium beetles have several possible post-mating mechanisms that they may use to bias paternity. Male sperm precedence has been extensively studied in Tribolium spp. and the related Tenebrio molitor, and several factors influencing male paternity share among a female's progeny have been identified. These include oviposition time, inter-mating interval, male strain/genotype, the mating regimen of a male's mother, male starvation, and tapeworm infection. Females exert muscular control over sperm storage, although there is no evidence to date that females use this to differentiate among mates. Females could also influence offspring paternity by re-mating with additional males, and T. castaneum females more readily accept spermatophores when they are re-mating with more attractive males. Additional work is needed to examine the possible roles played by both male and female accessory gland products in determining male paternity share. Sexual selection during pre-mating episodes may be reinforced or counteracted by peri- and post-copulatory selection, and antagonistic coevolution between the sexes may be played out across reproductive stages. In Tribolium, males' olfactory attractiveness is positively correlated with both insemination success and paternity share, suggesting consistent selection across different reproductive stages. Similar studies across sequential reproductive stages are needed in other taxa to provide a more integrative view of sexual selection.     

Sperm competition risk and male genital anatomy: comparative evidence for reduced duration of female sexual receptivity in primates with penile spines

Selection pressures influencing the way in which males stimulate females during copulation are not well understood. In mammals, copulatory stimulation can influence female remating behaviour, both via neuroendocrine mechanisms mediating control of sexual behaviour, and potentially also via effects of minor injury to the female genital tract. Male adaptations to increase copulatory stimulation may therefore function to reduce sperm competition risk by reducing the probability that females will remate. This hypothesis was tested using data for primates to explore relationships between male penile anatomy and the duration of female sexual receptivity. It was predicted that penile spines or relatively large bacula might function to increase copulatory stimulation and hence to reduce the duration of female sexual receptivity. Results of the comparative analyses presented show that, after control for phylogenetic effects, relatively high penile spinosity of male primates is associated with a relatively short duration of female sexual receptivity within the ovarian cycle, although no evidence was found for a similar relationship between baculum length and duration of female sexual receptivity. The findings presented suggest a new potential function for mammalian penile spines in the context of sexual selection, and add to growing evidence that sperm competition and associated sexual conflict are important selection pressures in the evolution of animal genitalia.     

Female-mediated differential sperm storage in a fly with complex spermathecae, Scatophaga stercoraria

Multiple spermathecae potentially allow selective sperm use, provided that sperm from rival males are stored differentially, that is, in different proportions across storage compartments. In the yellow dung fly, Scatophaga stercoraria, females have three spermathecae arranged as a doublet and singlet. To test whether females store the sperm of rival males actively and differentially, we mated fixed male pairs to three females. After copulation, females were (1) dissected immediately before they could start laying a clutch of eggs, (2) left awake for 30 min but prevented from oviposition, or (3) anaesthetized with carbon dioxide for 30 min to interfere with the muscular control presumably required for sperm transport from the site of insemination to the spermathecae. For each female, we estimated the proportion of the second male's sperm stored in her spermathecae (S(2)value), using sperm length as a male marker. After copulation, the S(2)values in the singlet and doublet spermathecae differed significantly, indicating differential sperm storage during copulation. Postcopulatory treatment affected differential sperm storage significantly. Females dissected immediately had lower S(2)values in the doublet than in the singlet spermatheca, while females left awake showed the reverse pattern for the same two males. This reversal did not occur when females were treated with carbon dioxide. The results indicate differential storage of sperm from different males during copulation and that female muscular activity can affect storage and separation of competing ejaculates beyond copulation. Copyright 2000 The Association for the Study of Animal Behaviour.     

The Y chromosome as a battle ground for sexual selection

The Y chromosome was once thought to be devoid of genetic information. However, recent work shows that it contains numerous genes related to sperm production and dimorphic traits (such as body size and tooth development). Among mammals, these traits influence a male's competitive ability in male-male contests and in sperm competition. Therefore, sexual selection could have favoured genes on the Y chromosome that enhance male fertilization success because they spread unaltered through the male line. In contrast, female heterogamety among birds makes it possible for genes that benefit females to spread through the female line, a mechanism that could explain the prevalence of female choice.