Receipt Of Sperm Research Articles

The evolution of sex peptide: sexual conflict, cooperation, and coevolution.

ABSTRACTA central paradigm in evolutionary biology is that the fundamental divergence in the fitness interests of the sexes (‘sexual conflict’) can lead to both the evolution of sex‐specific traits that reduce fitness for individuals of the opposite sex, and sexually antagonistic coevolution between the sexes. However, clear examples of traits that evolved in this way – where a single trait in one sex demonstrably depresses the fitness of members of the opposite sex, resulting in antagonistic coevolution – are rare. The Drosophila seminal protein ‘sex peptide’ (SP) is perhaps the most widely cited example of a trait that appears to harm females while benefitting males. Transferred in the ejaculate by males during mating, SP triggers profound and wide‐ranging changes in female behaviour and physiology. Early studies reported that the transfer of SP enhances male fitness while depressing female fitness, providing the foundations for the widespread view that SP has evolved to manipulate females for male benefit. Here, we argue that this view is (i) a simplification of a wider body of contradictory empirical research, (ii) narrow with respect to theory describing the origin and maintenance of sexually selected traits, and (iii) hard to reconcile with what we know of the evolutionary history of SP's effects on females. We begin by charting the history of thought regarding SP, both at proximate (its production, function, and mechanism of action) and ultimate (its fitness consequences and evolutionary history) levels, reviewing how studies of SP were central to the development of the field of sexual conflict. We describe a prevailing paradigm for SP's evolution: that SP originated and continues to evolve to manipulate females for male benefit. In contrast to this view, we argue on three grounds that the weight of evidence does not support the view that receipt of SP decreases female fitness: (i) results from studies of SP's impact on female fitness are mixed and more often neutral or positive, with fitness costs emerging only under nutritional extremes; (ii) whether costs from SP are appreciable in wild‐living populations remains untested; and (iii) recently described confounds in genetic manipulations of SP raise the possibility that measures of the costs and benefits of SP have been distorted. Beyond SP's fitness effects, comparative and genetic data are also difficult to square with the idea that females suffer fitness costs from SP. Instead, these data – from functional and evolutionary genetics and the neural circuitry of female responses to SP – suggest an evolutionary history involving the evolution of a dedicated SP‐sensing apparatus in the female reproductive tract that is likely to have evolved because it benefits females, rather than harms them. We end by exploring theory and evidence that SP benefits females by functioning as a signal of male quality or of sperm receipt and storage (or both). The expanded view of the evolution of SP that we outline recognises the context‐dependent and fluctuating roles played by both cooperative and antagonistic selection in the origin and maintenance of reproductive traits.

Effects of Mating on Gene Expression in Female Insects: Unifying the Field.

Simple SummaryInsects play many important roles including in ecosystems, food production, pathogen transmission, and production of materials. As a result, humans are interested in understanding how to control insect population sizes for control, propagation, or conservation efforts. In many insect species, female reproductive output is promoted by mating and components of the ejaculate. Beyond just the impact of receiving sperm, mating and ejaculate components can result in increased rate of oocyte development, ovulation, and oviposition as well as other changes such as reduced mating receptivity. To understand how mating causes these changes, researchers have investigated changes in female gene expression that occur after mating. In this review, we summarize the current state of knowledge on mating-induced gene expression changes in female insects and the methods used for conducting such studies. We find that genes related to immune response, chemosensation, and metabolism are commonly regulated across species. We suggest future research paths to facilitate the comparison of studies on mating-regulated gene expression across insect species.There is intense interest in controlling insect reproductive output. In many insect species, reproductive output is profoundly influenced by mating, including the receipt of sperm and seminal fluid molecules, through physiological and behavior changes. To understand these changes, many researchers have investigated post-mating gene expression regulation. In this review, we synthesize information from studies both across and within different species about the impact of mating, or components of mating, on female gene expression patterns. We found that genes related to the roles of metabolism, immune-response, and chemosensation are regulated by mating across many different insect species. We highlight the few studies that have taken the important next step of examining the functional consequences of gene expression regulation which is crucial in order to understand the mechanisms underlying the mating-regulated control of female lifespan and reproduction and to make use of such knowledge to propagate or control insect populations. The potential of cross-study comparisons is diminished by different studies using different methods. Thus, we also include a consideration of how future studies could be designed to facilitate cross-study comparisons and a call for collaboration across researchers studying different insect species and different aspects of insect biology.

Disentangling female postmating responses induced by semen transfer components in a simultaneous hermaphrodite

Optimizing reproductive success is an essential part of evolution for both sexes. Females can optimize mating by avoiding superfluous mating advances and insemination, since both take time away from other activities and may incur costs related to sperm receipt. While many separate-sexed organisms are known to exhibit mate avoidance, much less is known about this for simultaneous hermaphrodites. We addressed this here, using a simultaneously hermaphroditic species that can choose to mate in either of the two sex roles during each mating interaction. Recently, avoidance behaviours in response to natural matings were observed in the hermaphroditic pond snail Lymnaea stagnalis, potentially deterring insemination. To disentangle whether such behaviours are mediated by the mechanical act of mating or the receipt of accessory gland proteins and/or sperm, we intravaginally injected individuals with control or test fluids. Our results show that the avoidance behaviours, crawl-out and biting, were more frequently expressed when individuals were inseminated with accessory gland proteins and/or sperm. These behavioural components of the recipient increased time in courtship prior to insemination, which is concordant with the hypothesis that the partner tries to discourage the potential sperm donor from inseminating. Understanding the mechanism underlying the effects that molluscan accessory gland proteins induce contributes to our understanding of the molecular basis of the recipient's (behavioural) responses as well as how such biochemical postcopulatory strategies evolve.

The developmental environment modulates mating-induced aggression and fighting success in adult female Drosophila.

Competition over access to resources early in life can influence development, and, in turn, affect competitive phenotypes in reproductive adults. Theory predicts that competition between adult females should be especially context‐dependent, because of constraints imposed by high costs of reproduction. However, the potential impact of developmental environments on competition in adult females remains little understood.In Drosophila melanogaster, the developmental environment can strongly influence adult condition, and prime adult competitive behaviour. In this species, female–female aggression is dependent on reproductive state and increases after mating due to the receipt of sperm and seminal fluid components. However, the effects of the developmental environment on adult female aggression, and any potential interactions with mating status, are unknown.To address this problem, we first raised flies at low and high larval density, which altered competition over limited resources, produced large and small adult females, respectively, and potentially primed them for differing levels of adult competition. We then fought the resulting adult females, either as virgins, or after receiving aggression‐stimulating ejaculates at mating, to test for interacting effects.We found, as expected, that mating elevated contest duration. However, this mating‐induced boost in aggression was strongly exacerbated for high density (small) females. Low density (large) females won more contests overall, but were not more successful in fights after mating. In contrast, mating increased the fighting success in females raised in high density environments.Our results suggest that individuals who experience competitive, resource‐limited, rearing conditions are more sensitive to the aggression‐stimulating effects of the male ejaculate. This finding highlights the importance of the developmental environment in mediating adult social interactions and provides support for the theory that female–female aggression should be highly context‐dependent. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13214/suppinfo is available for this article.

Female behaviour prior to additional sperm receipt in the hermaphroditic pond snail Lymnaea stagnalis

In many species, sexual resistance by females can fluctuate depending on different physiological and/or ecological conditions. Based on theory, we decided to test whether the simultaneous hermaphrodite Lymnaea stagnalis becomes more reluctant to mate in the female role after receipt of an ejaculate. We aimed to test whether receipt of an ejaculate affects the expression of recipient behaviours, and whether this can have a potential effect on the outcome of mating interactions. We found that the expression of Crawl-out and Biting behaviours increased significantly in recently inseminated snails. Our data also indicated that an increase in expression of these latter behaviours can have direct effects on the outcome of the mating interactions. These findings suggest that under the influence of recent insemination, this hermaphroditic snail is more reluctant to accept another mating in the female role and may try to actively discourage the mounting snail (sperm donor). Hence, despite the fact that these simultaneous hermaphrodites express both sexual functions, there can still be variation in motivation to mate in either role.

Comparative analysis of medical, legal, and ethical considerations for establishing a standard operating protocol for artificial insemination by donor

Artificial insemination by donor is an important means of improving the likelihood of pregnancy in couples affected by male factor infertility, but it poses medical, legal, and ethical issues due to the involvement of third parties, such as the sperm donor. In Korea, the Bioethics and Safety Act was enacted for the purpose of preventing and eliminating unethical research on germ cells, and such research was limited to matters related to the use of assisted reproductive technologies, centering on embryos, oocytes, and protecting the health of oocyte donors. However, this law is incomplete in terms of specific standards or regulations relating to the donation and receipt of sperm. In Korea, artificial insemination by donor has been carried out without a standard operating protocol for donation and receipt of sperm, which would include testing sperm donors for diseases, limiting the number of donor offspring, compensation for donations, and the role of anonymity and non-anonymity. The diversity of policies worldwide shows that each country has its unique set of guidelines tailored for its own specific needs and practical considerations. Herein, I present a standard operating protocol of medical, legal, and ethical principles for artificial insemination by donor that is suitable for domestic circumstances, along with a comparison of recommendations and guidelines of other countries concerning sperm donation issues.

Sperm and sex peptide stimulate aggression in female Drosophila.

Introductory paragraphFemale aggression towards other females is associated with reproduction in many taxa, and traditionally thought to be related to the protection or provisioning of offspring, such as through increased resource acquisition. However, the underlying reproductive factors causing aggressive behaviour in females remain unknown. Here we show that female aggression in the fruit fly Drosophila melanogaster is strongly stimulated by the receipt of sperm at mating, and in part by an associated seminal fluid protein, the sex peptide. We further show that the post-mating increase in female aggression is decoupled from the costs of egg production and from post-mating decreases in sexual receptivity. Our results suggest that male ejaculates can have a surprisingly direct influence on aggression in recipient females. Male ejaculate traits thus influence the female social competitive environment with potentially far-reaching ecological and evolutionary consequences.

Reproductive behaviour: Make love, then war.

Female aggression is enhanced after mating. Genetic manipulation and behavioural observation show that the receipt of sperm, and a seminal fluid protein, enhances female Drosophila aggression towards other females.

Female Fitness Optimum at Intermediate Mating Rates under Traumatic Mating

Traumatic mating behaviors often bear signatures of sexual conflict and are then typically considered a male strategy to circumvent female choice mechanisms. In an extravagant mating ritual, the hermaphroditic sea slug Siphopteron quadrispinosum pierces the integument of their mating partners with a syringe-like penile stylet that injects prostate fluids. Traumatic injection is followed by the insertion of a spiny penis into the partner’s gonopore to transfer sperm. Despite traumatic mating, field mating rates exceed those required for female fertilization insurance, possibly because costs imposed on females are balanced by direct or indirect benefits of multiple sperm receipt. To test this idea, we exposed animals to a relevant range of mating opportunity regimes and assessed the effects on mating behavior and proxies of female fitness. We find penis intromission duration to decrease with mating rates, and a female fecundity maximum at intermediate mating rates. The latter finding indicates that benefits beyond fertilization insurance can make higher mating rates also beneficial from a female perspective in this traumatically mating species.

Female Drosophila melanogaster suffer reduced defense against infection due to seminal fluid components

Reduced defense against infection is commonly observed as a consequence of reproductive activity, but little is known about how post-mating immunosuppression occurs. In this work, we use Drosophila melanogaster as a model to test the role of seminal fluid components and egg production in suppressing post-mating immune defense. We also evaluate whether systemic immune system activity is altered during infection in mated females. We find that post-mating reduction in female defense depends critically on male transfer of sperm and seminal fluid proteins, including the accessory gland protein known as “sex peptide.” However, the effect of these male factors is dependent on the presence of the female germline. We find that mated females have lower antimicrobial peptide gene expression than virgin females in response to systemic infection, and that this lower expression correlates with higher systemic bacterial loads. We conclude that, upon receipt of sperm and seminal fluid proteins, females experience a germline-dependent physiological shift that directly or indirectly reduces their overall ability to defend against infection, at least in part through alteration of humoral immune system activity.

Hermaphrodite sex role preferences: the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana

Costs and benefits associated with matings and the effects of mating frequency on fitness commonly differ between the sexes. As a result, outcrossing simultaneous hermaphrodites may prefer to copulate in the more rewarding sex role, generating conflicts over sperm donation and sperm receipt between mates. Because recent sex role preference models remain controversial, we contrast here some of their assumptions and predictions in the sea slug Chelidonura sandrana. For this hermaphrodite with sperm storage and internal fertilisation, risk-averse models assume that fitness pay-offs are constantly higher in the female than in the male function in any single mating. Moreover, excluding mutual partner assessment, these models predict male mating behaviour to be independent of receiver traits. The competing gender ratio hypothesis assumes that relative fitness pay-offs, and thus the preferred mating roles, vary and may reverse between matings and predicts that ejaculation strategies co-vary with receiver quality. We found that field mating rates of C. sandrana substantially exceeded what is required to maintain female fertility and fecundity, indicating large variation in direct female benefits between matings. We further demonstrate that male copulation duration adaptively increased with partner body size (i.e. fecundity) but decreased with recent partner promiscuity. These findings are compatible with the gender ratio hypothesis but contradict risk-averse models.

Gender trading in a hermaphrodite

Although males and females may face severe sexual conflicts [1], the decision over who donates and who receives sperm is fixed. This is not necessarily the case in simultaneous hermaphrodites, where each mate may insist on copulating as ‘male,' ‘female' or both. The resulting conflicts over gender provide an opportunity to study conflict-solving strategies. By directly manipulating mating interests in the sea slug Chelidonura hirundinina , we present the first unequivocal evidence for ‘sperm trading' [2], a mating strategy where sperm donation is conditional on sperm receipt. Trading enforces reciprocity, offering a simple solution for the gender conflict.

Do “sperm trading” simultaneous hermaphrodites always trade sperm?

Sperm trading can be a mechanism to solve the conflict over sex roles in hermaphrodites with copulation, sperm competition, and sperm digestion. If present, sperm donation depends on sperm receipt, resulting in conditional reciprocal inseminations. Conditional reciprocity can involve three traded commodities: penis intromissions on a yes-or-no basis, intromission durations (indicating ejaculate size), or sperm transfer. If present, animals that refuse to donate (cheaters) should be deserted by their partner or receive smaller ejaculates. We tested whether any of these commodities is traded in the simultaneously hermaphroditic sea slug, Chelidonura sandrana. Matings involve a stereotypic single sex role alternation. As a result, reciprocity was more frequent than expected under random mating, supporting trading of penis intromissions. Contrary to the predictions under trading of ejaculate sizes, intromission durations were not balanced between mating partners. To test trading of sperm transfer itself, we interrupted the sperm groove that transports sperm into the penis during copulation. Treated animals (experimental cheaters) could still copulate normally but could not transfer sperm. When paired to a cheater, sham-treated control animals did not respond to the absence of sperm receipt, neither by desertion nor by shortening intromission. We thus reject trading of insemination durations and sperm transfer in C. sandrana. Although trading of intromissions may be present, we discuss why reciprocity in this species may also be a by-product of the mutual willingness of both partners to donate as well as receive sperm, and not an indicator of sperm trading. Copyright 2005.

Mating, seminal fluid components, and sperm cause changes in vesicle release in the Drosophila female reproductive tract.

Mating induces changes in female insects, including in egg production, ovulation and laying, sperm storage, and behavior. Several molecules and effects that induce these changes have been identified, but their proximate effects on females remain unexplored. We examined whether vesicle release occurs as a consequence of mating; we used transgenic Drosophila that allow monitoring of secretory granule release at nerve termini. Changes in release occur at specific times postmating in different regions of the female reproductive tract: soon after mating in the lower reproductive tract, and later in the upper reproductive tract. Some changes are triggered by receipt of sperm, others by male seminal proteins, and still others by the act of mating itself (or other unidentified effectors). Our findings indicate that the female reproductive tract is a multi-organ system whose regions are modulated separately by mating and mating components. This modulation could create an environment conducive to increased reproductive capacity.

Sperm trading and sex roles in the hermaphroditic opisthobranch sea slug Navanax inermis : eager females or opportunistic males?

The sea slug Navanax inermis (Gastropoda, Opisthobranchia) is a well-known example of a simultaneous hermaphrodite in which mating partners trade sperm. According to previous work by others, sperm trading follows from a general preference for the female role when the expected variance in reproductive success in the male role is higher and the risk of failure therefore larger. However, this view contradicts theoretical and empirical studies of other systems, which predict a general preference for the male role; sperm trading is assumed to follow from the fact that individuals benefit from sperm receipt as a nutritional compensation for sperm investment. In this study, we investigate the behaviour of N. inermis in more detail. In addition to observations of regular pairs, we also paired individuals with a partner that had been isolated for 33 days in order to induce changes in sex-role preference in the non-isolated partner. We also collected all clutches produced throughout the study to check for signs of infertility as a consequence of allosperm depletion. Fertility of field-collected and isolated individuals suggested that sperm depletion occurs under natural conditions and may be caused by a lack of partners. Although this argues in favour of female preference, low mating rates both reduce variance in male reproductive success and remove the intent to use sperm for nutritional purposes, thus eliminating the conditions under which both hypotheses are intended to operate. The observational data indicate that animals are eager to mate as males, particularly at the beginning of a mating session. Intromissions lasted longer when a simultaneous intromission was received from the partner. Increases in intromission were recorded in non-isolated individuals with partners which were previously isolated and therefore more attractive as females. This response would not have been expected were the female role the preferred one. A summary of the arguments concerning preference for either gender suggests some preference for the male role, but indicates that sexual preferences may actually change or become neutral within an individual, even in the course of a mating session. Overall, our results clearly confirm previously published observations of sperm trading in N. inermis . © 2003 The Linnean Society of London . Biological Journal of the Linnean Society, 2003, 78 , 105 - 116. ADDITIONAL KEYWORDS: sexual conflict ‐ sexual selection ‐ Gastropoda ‐ reciprocity ‐ gamete trading ‐ sperm trading ‐ egg trading.

Sambia Sexual Culture: Essays from the Field

Gilbert Herdt, Sexual Culture: Essays from the Field, Chicago and London: University of Chicago Press, 1999, xi + 327 pages.Reviewer: Andrew P. LyonsWilfrid Laurier UniversityTwenty years have now passed since the publication of Guardians of the Flutes which was arguably the best ethnographic examination of sexuality since Malinowski's Sexual Life of Savages. Gilbert Herdt returned to New Guinea several times until 1993 when a nearly fatal bout of malaria led him to curtail his visits. This volume draws on those later field trips. Herdt re-examines and develops themes which he first discussed in Guardians. He also discusses the significance of his work not only for social anthropology but also for the Gay Liberation Movement. All of the nine essays in the volume originally appeared elsewhere and most readers will have read a few of them already. However, they fit very well together, and the author has contributed an excellent theoretical introduction. Readers unacquainted with Herdt's ethnography should note that it describes a population which prescribed homoerotic fellatio as a necessary part of male social development. There was no sexual play in the period prior to initiation. Prepubertal youths in the first stages of initiation were fellators; adolescents in the third stage of initiation were fellated by the younger boys. Marriage to females occured at the end of the initiation cycle. These customs reflected a system of thought in which mature male sexuality was tenuously achieved and always threatened by feminine, specifically menstrual pollution. An adequate supply of sperm was stored in the growing boy as a result of fellation. The receipt of sperm in heterosexual intercourse enabled women to produce breast milk.The notes on the book cover describe Herdt as a renowned anthropologist, a description which may provoke some jealousy but which does attest to his achievement. Until 1980 the anthropology of sexuality occupied a marginal place in our discipline. This was partly because sexuality was excluded by existing paradigms such as structural-functionalism and cultural ecology, and, more surprisingly, by later developments in psychological anthropology. In large measure this was because there was little middle ground between sociological approaches which regarded sexuality as too natural, too universal (see p. 4) and too threatening to sociological method to be worthy of consideration, and behaviouristic or ethological approaches which are neglectful of social meanings Within anthropology the study of sexuality could only be subsumed under such headings as kinship and gender.Another cause of neglect was the degree of professional, political and humanitarian risk involved in such investigations. Esther Newton has complained that her work on drag-queens was not regarded as legitimate research (Newton, 2000: 223). Of course the homosexual student of sexuality faces additional barriers. Sometimes they reflect pure prejudice; on other occasions biases may be more subtle. Kath Weston (1998: 189-211) has complained that her own work on lesbian sexuality within the USA has led to a degree of professional marginalization (such research, argue critics is not real fieldwork).Very often, the disclosure of information may be perceived as harmful to populations and individuals who are subject to the surveillance of outsiders as well as exploitation by sexual tourists. Such reports may also embarrass cultural insiders who wish to distance themselves from tribal traditions. It is for this reason that Herdt disguised the identity of the Sambia of the Eastern Highlands of Papua New Guinea. Last but not least the obtaining of information on matters sexual involves the establishing and affirming of a degree of trust which is most difficult to create as well as linguistic skills of a high order. There is no society without sexual taboos; there are few without rules of privacy or secrecy with respect to some matters. …

Seminal fluid regulation of female sexual attractiveness in Drosophila melanogaster.

Finding a willing and suitable mate is critical for sexual reproduction. Visual, auditory, and chemical cues aid in locating and/or attracting partners. After mating, females from many insect species become less attractive. This is caused by changes in the quantity and/or quality of pheromones synthesized by the female and to changes in the female's behavior. For example, female insects may stop releasing pheromones, assume a mate refusal posture, or move less in response to males. Many postmating changes in female insects are triggered by seminal fluid proteins from the male's accessory gland proteins (Acps) and by sperm. To determine the role of seminal fluid components in mediating changes in attractiveness, we measured the attractiveness of Drosophila melanogaster females that had been mated to genetically altered males that lack sperm and/or Acps. We found that the drop in female attractiveness occurs in two phases. A short-term drop in attractiveness is triggered independent of the receipt of sperm and Acps. Maintenance of lowered attractiveness is dependent upon sperm.

Lack of response to sex-peptide results in increased cost of mating in dunce Drosophila melanogaster females

Drosophila melanogaster females homozygous for the dunce mutation have been reported to mate more often than females of a wild type stock (Canton-S). We have investigated the basis of this increased receptivity, by examining the response of dunce females, females of a revertant stock with the same genetic background and Canton-S females to injection with a component of the male accessory fluid (the ‘sex-peptide’, SP). dunce virgin females injected with SP showed no decline in receptivity towards courting males, whereas receptivity in control females was inhibited. dunce females also showed no inhibition of remating associated with the transfer of any non-sperm components at mating (the ‘copulation effect’) but did show a loss of receptivity due to the receipt of sperm (the ‘sperm effect’). The high remating rate of dunce females can therefore be attributed at least in part to their aberrant response to the receptivity-inhibiting SP. dunce females were no more susceptible than control females to the effects of a single mating; there was no significant difference in lifespan between dunce females mated once soon after eclosion and virgin dunce females. Twice-mated dunce females, however, had significantly shorter lifespans than virgin dunce females; this effect was not apparent in control dunce + revertant females. The high cost of mating incurred by dunce females is therefore due to a combination of their elevated remating rate and an increase in sensitivity to the effects of a fixed number of matings.

Longevity in Caenorhabditis elegans reduced by mating but not gamete production.

Theories of life-history evolution propose that trade-offs occur between fitness components, including longevity and maximal reproduction. In Drosophila, female lifespan is shortened by increased egg production, receipt of male accessory fluid and courting. Male lifespan is also reduced by courting and/or mating. Here we show that in the nematode Caenorhabditis elegans, mating with males reduces the lifespan of hermaphrodites by a mechanism independent of egg production or receipt of sperm. Conversely, males appear unaffected by mating. Thus, in C. elegans there is no apparent trade-off between longevity and increased egg or sperm production, but there is a substantial cost to hermaphrodites associated with copulation.

Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products.

Female Drosophila melanogaster with environmentally or genetically elevated rates of mating die younger than controls. This cost of mating is not attributable to receipt of sperm. We demonstrate here that seminal fluid products from the main cells of the male accessory gland are responsible for the cost of mating in females, and that increasing exposure to these products increases female death rate. Main-cell products are also involved in elevating the rate of female egg-laying, in reducing female receptivity to further matings and in removing or destroying sperm of previous mates. The cost of mating to females may therefore represent a side-effect of evolutionary conflict between males.