Postmating Female Control: 20 Years of Cryptic Female Choice
Authors: Renée C. Firman, Clelia Gasparini, Mollie K. Manier, Tommaso Pizzari
Journal: Trends in Ecology & Evolution (2017)

In 1996, Eberhard crystallized the idea of CFC as an engine of sexual selection and initiated the study of female-driven processes. Demonstrating CFC, which is defined as female-mediated morphological, behavioral, or physiological mechanisms that operate to bias fertilization toward the sperm of specific male(s), requires dissecting male and female variance components of sperm retention or paternity. Technologies developed over the past 20 years have helped elucidate the proximate mechanisms underpinning fertilization and have accelerated the field of CFC. Females may bias sperm use at successive stages of the reproductive process, including shortly after mating, during sperm transit and/or storage, and at fertilization. CFC can have fundamental repercussions for sexual selection on males, female fitness, and, consequently, sexual conflict and intersexual coevolution, with ramifications for related evolutionary phenomena (e.g., speciation). Cryptic female choice (CFC) represents postmating intersexual selection arising from female-driven mechanisms at or after mating that bias sperm use and impact male paternity share. Although biologists began to study CFC relatively late, largely spurred by Eberhard's book published 20 years ago, the field has grown rapidly since then. Here, we review empirical progress to show that numerous female processes offer potential for CFC, from mating through to fertilization, although seldom has CFC been clearly demonstrated. We then evaluate functional implications, and argue that, under some conditions, CFC might have repercussions for female fitness, sexual conflict, and intersexual coevolution, with ramifications for related evolutionary phenomena, such as speciation. We conclude by identifying directions for future research in this rapidly growing field. Cryptic female choice (CFC) represents postmating intersexual selection arising from female-driven mechanisms at or after mating that bias sperm use and impact male paternity share. Although biologists began to study CFC relatively late, largely spurred by Eberhard's book published 20 years ago, the field has grown rapidly since then. Here, we review empirical progress to show that numerous female processes offer potential for CFC, from mating through to fertilization, although seldom has CFC been clearly demonstrated. We then evaluate functional implications, and argue that, under some conditions, CFC might have repercussions for female fitness, sexual conflict, and intersexual coevolution, with ramifications for related evolutionary phenomena, such as speciation. We conclude by identifying directions for future research in this rapidly growing field. Darwin's exposition on sexual selection (see Glossary) was restricted to premating episodes in internal fertilizers; for males, these episodes comprised intrasexual competition to access receptive females, and intersexual selection exerted by females discriminating among prospective partners [1Darwin C.R. The Descent of Man and Selection in Relation to Sex. John Murray, 1871Crossref Google Scholar]. Approximately one century later, Geoff Parker intuited that intrasexual selection can continue after mating, because widespread polyandry leads to sperm competition [2Parker G.A. Sperm competition and its evolutionary consequences in the insects.Biol . Rev. 1970; 45: 525-567Crossref Google Scholar]. This realization raised the possibility that intersexual selection also occurs during and after mating if polyandrous females can bias sperm utilization [3Childress D. Hartl D.L. Sperm preference in Drosophila melanogaster.Genetics. 1972; 71: 417-427PubMed Google Scholar], a process that Randy Thornhill called ' cryptic female choice' (CFC) [4Thornhill R. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps.Am. Nat. 1983; 122: 765-788Crossref Scopus (470) Google Scholar] (Figure 1A). In 1996, Bill Eberhard crystallized the idea of CFC as an engine of sexual selection in his book Female Control: Sexual Selection by Cryptic Female Choice [5Eberhard W.G. Female Control: Sexual Selection by Cryptic Female Choice. Princeton University Press, 1996Crossref Google Scholar], elaborating on Thornhill's initial definition of CFC as female-mediated morphological, behavioral, or physiological mechanisms that bias fertilization toward the sperm of specific males. Eberhard was instrumental in extending postmating sexual selection to the study of female-driven processes [5Eberhard W.G. Female Control: Sexual Selection by Cryptic Female Choice. Princeton University Press, 1996Crossref Google Scholar]. Molecular tools, along with in vitro and in vivo technologies developed over the past 20 years, have helped elucidate the proximate mechanisms underpinning fertilization and, combined with the increasing appreciation for female roles in sexual selection, have accelerated the study of CFC [6Arnqvist G. Cryptic female choice.in: Shuker D. Simmons L.W. The Evolution of Insect Mating Systems. Oxford University Press, 2014: 204-220Crossref Google Scholar]. Here, we appraise progress in the field 20 years after the publication of Eberhard's pivotal book. We distinguish between proximate mechanisms and functional implications of CFC. First, we explain criteria for demonstrating CFC, outline proximate mechanisms underpinning CFC, critically review empirical evidence, and detail current approaches for resolving these mechanisms. We then investigate functional implications of CFC, and discuss its evolutionary significance for females, males, and intersexual coevolution. Wherever possible, we include examples that represent clear demonstrations of CFC and associated fitness consequences, and we also speculate about potential or hypothetical examples of CFC. While a comprehensive survey of the literature is beyond the scope of this review, we hope to encourage discussion and further research in areas where unequivocal evidence is still lacking. CFC is mediated by subtle and complex processes, and often comprises covert mechanisms that are within the female reproductive tract (FRT), which historically have proven technically difficult to study. Measuring CFC is further complicated by the necessary co-occurrence of sperm competition. To demonstrate CFC, we need to: (i) identify a female trait or behavior that affects sperm uptake and/or utilization at or after mating; and (ii) show that this female response is differential and nonrandom, such that the sperm of certain males are predictably favored or disfavored based on factors such as phenotype or genotype. Box 1 outlines a general quantitative framework to test CFC; below, we review recent empirical approaches addressing (i) and (ii).Box 1Defining and Demonstrating CFCCFC is operationally defined as variation in fertilization success among males due to nonrandom, differential responses of females; thus, demonstrating CFC requires dissecting male and female variance components of sperm retention or paternity. Although demonstrating CFC has been historically debated [84Birkhead T.R. Defining and demonstrating postcopulatory female choice – again.Evolution. 2000; 54: 1057-1060PubMed Google Scholar], the approach outlined below is now widely accepted. The simplest case is a factorial design where females are exposed to sperm of individual males to distinguish consistent patterns of sperm utilization from random error. Each male–female combination is replicated using the same or genetically similar individuals (e.g., full-sibs, isogenic, or inbred lines). We partition Sum of Squares within (SSwithin, error) and between (SSbetween) male–female combinations; SSbetween is then partitioned across the male and female main effects and their male × female interaction. When SSwithin >SSbetween, variation is random across male–female combinations, while SSwithin <SSbetween indicates significant differences. A good example of this general approach is provided by a study of Drosophila melanogaster [85Bjork A. et al.Complex interactions with females and rival males limit the evolution of sperm offence and defence.Proc. R. Soc. B. 2007; 274: 1779-1788Crossref PubMed Scopus (62) Google Scholar], in which the repeated use of individual males with individual females enabled the authors to estimate the repeatability of P1 and P2. A significant female effect indicates consistent differences among females in sperm utilization (e.g., they might lose sperm from SSO at faster rate), regardless of male identity. This scenario can have interesting repercussions for sexual selection on males if males mate nonrandomly with respect to female type, but does not in itself represent CFC. A significant male effect indicates consistent variation among males independent of female identity due to either male effects (e.g., variation in ejaculate fertilizing efficiency) or directional CFC for certain male traits. The two alternatives are not mutually exclusive, and special care is required to distinguish male and female mechanisms. One approach is to measure ejaculate phenotypes related to competitive fertilization success (e.g., sperm numbers or velocity) and generate expectations of paternity share based on the relative values of these male traits. Deviations from such expectations are inconsistent with sperm competition explanations and instead lend support to CFC. For example, Parker et al. [86Parker G.A. et al.Analysing sperm competition data: simple models for predicting mechanisms.Behav . Ecol. Sociobiol. 1990; 27: 55-65Crossref Scopus (172) Google Scholar] generated expectations for P2 based on S2, and this approach was later modified for non-normal data [87Eggert A.K. et al.Linear models for assessing mechanisms of sperm competition: the trouble with transformations.Evolution. 2003; 57: 173-176Crossref PubMed Scopus (30) Google Scholar, 88Neff B.D. Wahl L.M. Mechanisms of sperm competition: testing the fair raffle.Evolution. 2004; 58: 1846-1851Crossref PubMed Scopus (25) Google Scholar] and multiple SSOs [89Manier M.K. et al.An analytical framework for estimating fertilization bias and the fertilization set from multiple sperm-storage organs.Am. Nat. 2013; 182: 552-561Crossref PubMed Scopus (39) Google Scholar]. Finally, a significant male × female interaction indicates nondirectional CFC, consistent differences across male–female combinations in utilization or fertilization success [90Birkhead T.R. et al.Nontransitivity of paternity in a bird.Evolution. 2004; 58: 416-420Crossref PubMed Scopus (65) Google Scholar].This approach can be expanded to include sperm competition between two males and attributing variation in P2 to the female, first male, second male, or male × male and female × male × male interactions. We can also test hypotheses that certain factors influence CFC by including male or female genotype or phenotype as a main or random effect, depending on experimental design. In the case of directional CFC on a continuous variable, we can use selection analysis to express male fitness (fertilization success, W) as a function of the male phenotype, z, targeted by CFC (Equation I):W=β(z)+ε[I], where ε is an error term, W and z represent standardized male fitness and phenotype, respectively, and β represents the standardized gradient of postmating intersexual selection on z (i.e., β = S/σp, where S is the CFC selection differential). However, the causal relationship between male trait and female response can only be demonstrated through experimental manipulations. CFC is operationally defined as variation in fertilization success among males due to nonrandom, differential responses of females; thus, demonstrating CFC requires dissecting male and female variance components of sperm retention or paternity. Although demonstrating CFC has been historically debated [84Birkhead T.R. Defining and demonstrating postcopulatory female choice – again.Evolution. 2000; 54: 1057-1060PubMed Google Scholar], the approach outlined below is now widely accepted. The simplest case is a factorial design where females are exposed to sperm of individual males to distinguish consistent patterns of sperm utilization from random error. Each male–female combination is replicated using the same or genetically similar individuals (e.g., full-sibs, isogenic, or inbred lines). We partition Sum of Squares within (SSwithin, error) and between (SSbetween) male–female combinations; SSbetween is then partitioned across the male and female main effects and their male × female interaction. When SSwithin >SSbetween, variation is random across male–female combinations, while SSwithin <SSbetween indicates significant differences. A good example of this general approach is provided by a study of Drosophila melanogaster [85Bjork A. et al.Complex interactions with females and rival males limit the evolution of sperm offence and defence.Proc. R. Soc. B. 2007; 274: 1779-1788Crossref PubMed Scopus (62) Google Scholar], in which the repeated use of individual males with individual females enabled the authors to estimate the repeatability of P1 and P2. A significant female effect indicates consistent differences among females in sperm utilization (e.g., they might lose sperm from SSO at faster rate), regardless of male identity. This scenario can have interesting repercussions for sexual selection on males if males mate nonrandomly with respect to female type, but does not in itself represent CFC. A significant male effect indicates consistent variation among males independent of female identity due to either male effects (e.g., variation in ejaculate fertilizing efficiency) or directional CFC for certain male traits. The two alternatives are not mutually exclusive, and special care is required to distinguish male and female mechanisms. One approach is to measure ejaculate phenotypes related to competitive fertilization success (e.g., sperm numbers or velocity) and generate expectations of paternity share based on the relative values of these male traits. Deviations from such expectations are inconsistent with sperm competition explanations and instead lend support to CFC. For example, Parker et al. [86Parker G.A. et al.Analysing sperm competition data: simple models for predicting mechanisms.Behav . Ecol. Sociobiol. 1990; 27: 55-65Crossref Scopus (172) Google Scholar] generated expectations for P2 based on S2, and this approach was later modified for non-normal data [87Eggert A.K. et al.Linear models for assessing mechanisms of sperm competition: the trouble with transformations.Evolution. 2003; 57: 173-176Crossref PubMed Scopus (30) Google Scholar, 88Neff B.D. Wahl L.M. Mechanisms of sperm competition: testing the fair raffle.Evolution. 2004; 58: 1846-1851Crossref PubMed Scopus (25) Google Scholar] and multiple SSOs [89Manier M.K. et al.An analytical framework for estimating fertilization bias and the fertilization set from multiple sperm-storage organs.Am. Nat. 2013; 182: 552-561Crossref PubMed Scopus (39) Google Scholar]. Finally, a significant male × female interaction indicates nondirectional CFC, consistent differences across male–female combinations in utilization or fertilization success [90Birkhead T.R. et al.Nontransitivity of paternity in a bird.Evolution. 2004; 58: 416-420Crossref PubMed Scopus (65) Google Scholar]. This approach can be expanded to include sperm competition between two males and attributing variation in P2 to the female, first male, second male, or male × male and female × male × male interactions. We can also test hypotheses that certain factors influence CFC by including male or female genotype or phenotype as a main or random effect, depending on experimental design. In the case of directional CFC on a continuous variable, we can use selection analysis to express male fitness (fertilization success, W) as a function of the male phenotype, z, targeted by CFC (Equation I):W=β(z)+ε[I], where ε is an error term, W and z represent standardized male fitness and phenotype, respectively, and β represents the standardized gradient of postmating intersexual selection on z (i.e., β = S/σp, where S is the CFC selection differential). However, the causal relationship between male trait and female response can only be demonstrated through experimental manipulations. The causal relationship between a male trait and patterns of female sperm utilization can be illuminated by experimentally manipulating male phenotype while controlling for, or blocking, other factors. For context-dependent phenotypes, such as social status or relatedness, a powerful design involves allowing females to evaluate the same male in different contexts. Changes in female sperm utilization and/or fertilization success associated with such manipulations are consistent with CFC (e.g., [7Pilastro A. et al.Cryptic female preference for colorful males in guppies.Evolution. 2004; 58: 665-669Crossref PubMed Scopus (138) Google Scholar]). However, plastic male responses (e.g., differential sperm allocation) must be controlled for, increasing the difficulty of demonstrating CFC. Artificial insemination (AI) or in vitro assays of sperm utilization and fertilization can be used to control ejaculate traits and eliminate the influence of premating mechanisms (e.g., [8Martin-Coello J. et al.Sperm competition promotes asymmetries in reproductive barriers between closely related species.Evolution. 2009; 63 (613–613)Crossref PubMed Scopus (37) Google Scholar, 9Firman R.C. Simmons L.W. Gametic interactions promote inbreeding avoidance in house mice.Ecol . Lett. 2015; 18: 937-943Crossref PubMed Scopus (35) Google Scholar, 10Gasparini C. Pilastro A. 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One solution uses among-male variation in sperm traits to test differential positioning in the female sperm storage organ (SSO) [13Pattarini J.M. et al.Mechanisms underlying the sperm quality advantage in Drosophila melanogaster.Evolution. 2006; 60: 2064-2080Crossref PubMed Google Scholar] or fertilization success [14Bennison C. et al.Long sperm fertilize more eggs in a bird.Proc . R. Soc. London B. 2015; 282: 20141897Crossref PubMed Scopus (76) Google Scholar]. Competitive PCR of microsatellites has been used to quantify S2 for individual males within the SSOs of multiply mated females [15Holman L. et al.Random sperm use and genetic effects on worker caste fate in Atta colombica leaf-cutting ants.Mol . Ecol. 2011; 20: 5092-5102Crossref PubMed Scopus (23) Google Scholar, 16Bretman A. et al.Promiscuous females avoid inbreeding by controlling sperm storage.Mol . Ecol. 2009; 18: 3340-3345Crossref PubMed Scopus (110) Google Scholar]. Differential labeling of sperm from multiple males has allowed high-resolution characterization of postmating mechanisms, including those related to CFC [8Martin-Coello J. et al.Sperm competition promotes asymmetries in reproductive barriers between closely related species.Evolution. 2009; 63 (613–613)Crossref PubMed Scopus (37) Google Scholar, 9Firman R.C. Simmons L.W. Gametic interactions promote inbreeding avoidance in house mice.Ecol . Lett. 2015; 18: 937-943Crossref PubMed Scopus (35) Google Scholar, 17Lymbery R.A. et al.Fluorescent sperm offer a method for tracking the real-time success of ejaculates when they compete to fertilise eggs.Sci . Rep. 2016; 6: 22689Crossref PubMed Scopus (9) Google Scholar]. The recent development of transgenic males producing live sperm expressing green or red fluorescent proteins has enabled unprecedented insights into the behavior of sperm within the FRT, and CFC mechanisms [18Manier M.K. et al.Resolving mechanisms of competitive fertilization success in Drosophila melanogaster.Science. 2010; 328: 354-357Crossref PubMed Scopus (244) Google Scholar, 19Lüpold S. et al.Female mediation of competitive fertilization success in Drosophila melanogaster.Proc . Natl. Acad. Sci. U. S. A. 2013; 110: 10693-10698Crossref PubMed Scopus (87) Google Scholar, 20Ala-Honkola O. Manier M.K. Multiple mechanisms of cryptic female choice act on intraspecific male variation in Drosophila simulans.Behav . Ecol. Sociobiol. 2016; 70: 519-532Crossref Scopus (11) Google Scholar, 21Droge-Young E.M. et al.Resolving mechanisms of short-term competitive fertilization success in the red flour beetle.J . Insect Physiol. 2016; 93–94: 1-10Crossref PubMed Scopus (13) Google Scholar]. Eberhard identified multiple proximate mechanisms through which females might bias fertilization at successive stages of the reproductive process [5Eberhard W.G. Female Control: Sexual Selection by Cryptic Female Choice. Princeton University Press, 1996Crossref Google Scholar]. Here, we focus on prezygotic mechanisms at and shortly after mating, mediating sperm storage in the SSO, and at fertilization (Figure 1B). Females might first influence paternity by controlling the timing and order of competing inseminations. Females of the moth Ephestia kuehniella influence P2 by remating sooner, through displacement of the first spermatophore from the SSO [22Xu J. Wang Q. Mechanisms of last male precedence in a moth: sperm displacement at ejaculation and storage sites.Behav . Ecol. 2010; 21: 714-721Crossref Scopus (25) Google Scholar]. Moreover, the outcome of sperm competition is often mediated by the number of sperm inseminated by different males. While ejaculate size is largely under male control, females might influence sperm transfer through spermatophore acceptance or by actively terminating copulation. An elegant study in the guppy Poecilia reticulata showed that a male inseminates more sperm if his mate perceives him to be relatively attractive [7Pilastro A. et al.Cryptic female preference for colorful males in guppies.Evolution. 2004; 58: 665-669Crossref PubMed Scopus (138) Google Scholar]. Although poorly investigated, female control over copulation duration represents an effective mechanism for mediating which sperm enter the fertilizing pool [23Herberstein M.E. Sperm storage and copulation duration in a sexually cannibalistic spider.J . Ethol. 2011; 29: 9-15Crossref Scopus (35) Google Scholar, 24Pilastro A. et al.Copulation duration, insemination efficiency and male attractiveness in guppies.Anim . Behav. 2007; 74: 321-328Crossref Scopus (70) Google Scholar] In several species, a proportion of the ejaculate is lost shortly following ejaculation and female processes, such as differential sperm ejection, digestion, and incapacitation, influence which sperm are retained. In some invertebrates, differential sperm ejection is associated with male size [21Droge-Young E.M. et al.Resolving mechanisms of short-term competitive fertilization success in the red flour beetle.J . Insect Physiol. 2016; 93–94: 1-10Crossref PubMed Scopus (13) Google Scholar, 25Ala-Honkola O. et al.No evidence for postcopulatory inbreeding avoidance in Drosophila melanogaster.Evolution. 2011; 65: 2699-2705Crossref PubMed Scopus (28) Google Scholar], species identity [26Manier M.K. et al.Postcopulatory sexual selection generates speciation phenotypes in Drosophila.Curr . Biol. 2013; 23: 1853-1862Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar], and courtship duration [27Peretti A.V. Eberhard W.G. Cryptic female choice via sperm dumping favours male copulatory courtship in a spider.J . Evol. Biol. 2010; 23: 271-281Crossref PubMed Scopus (55) Google Scholar]. Similarly, sperm ejection by female feral fowl Gallus domesticus might disfavor inseminations by socially subdominant males [28Pizzari T. Birkhead T.R. Female feral fowl eject sperm of subdominant males.Nature. 2000; 405: 787-789Crossref PubMed Scopus (289) Google Scholar, 29Dean R. et al.The risk and intensity of sperm ejection in female birds.Am . Nat. 2011; 178: 343-354Crossref PubMed Scopus (40) Google Scholar] (Figure 2). Female kittiwakes Rissa tridactyla can utilize sperm ejection to reduce the risk of fertilization by sperm aging within the FRT from previous copulations, which compromises offspring viability [30Wagner R.H. et al.Female choice of young sperm in a genetically monogamous bird.Proc . R. Soc. London B. 2004; 271: S134-S137Crossref PubMed Scopus (44) Google Scholar]. Sperm ejection might be male induced in the socially polyandrous dunnock Prunella modularis, where the male pecks the female cloaca before mating, which stimulates ejection of previously stored semen from other males [31Davies N.B. Polyandry, cloaca-pecking and sperm competition in dunnocks.Nature. 1983; 302: 334-336Crossref Scopus (95) Google Scholar], although the extent to which males control this female response remains unclear. Mechanisms of sperm uptake can also create opportunities for CFC, such as contractions of the FRT that facilitate sperm passage from lower to upper FRT in red garter snakes Thamnophis sirtalis parietalis [32Friesen C.R. et al.Female behaviour and the interaction of male and female genital traits mediate sperm transfer during mating.J . Evol. Biol. 2016; 29: 952-964Crossref PubMed Scopus (25) Google Scholar]. In some primates, the degree of sperm uptake has been linked to contractions associated with female orgasm, and female Japanese macaques Macaca fuscata are more likely to achieve orgasm-like responses when mating with socially dominant males [33Troisi A. Carosi M. Female orgasm rate increases with male dominance in Japanese macaques.Anim . Behav. 1998; 56: 1261-1266Crossref PubMed Scopus (27) Google Scholar], suggesting preferential sperm uptake for these males. Finally, sperm might be attacked by innate or acquired immune responses, phagocytosed, digested, or incapacitated within the FRT, such as by spermicidal action (e.g., Drosophila pseudoobscura [34Holman L. Snook R. A sterile sperm caste protects brother fertile sperm from female-mediated death in Drosophila pseudoobscura.Curr . Biol. 2008; 18: 292-296Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar]). Females might also exert their control by alleviating sperm incapacitation by rival ejaculates (e.g., bees and ants [35den Boer S.P.A. et al.Seminal fluid mediates ejaculate competition in social insects.Science. 2010; 327: 1506-1509Crossref PubMed Scopus (146) Google Scholar]). Out of all of these prestorage female-mediated phenomena, evidence that they function as CFC appears clearer for differential sperm ejection in relation to male phenotypes, although even here the causal effect of female response on paternity share remains largely unresolved. If sperm reach storage having escaped ejection, digestion, or incapacitation, they might interact with sperm from other males through displacement, stratification, or mixing. Eberhard first suggested that FRT complexity can increase female control over sperm storage and paternity [5Eberhard W.G. Female Control: Sexual Selection by Cryptic Female Choice. Princeton University Press, 1996Crossref Google Scholar]. Indeed, SSO morphology can influence the degree to which sperm are stored and/or displaced. Female dung flies Scathophaga stercoraria with four SSOs might be better able to control paternity compared with females with only three SSOs [36Ward P.I. Cryptic female choice in the yellow dung fly Scathophaga stercoraria (L.).Evolution. 2000; 54: 1680-1686Crossref PubMed Scopus (122) Google Scholar]. In Drosophila melanogaster, longer sperm are favored when stored in longer female seminal receptacles (SR) [37Miller G.T. Pitnick S. Sperm-female coevolution in Drosophila.Science. 2002; 298: 1230-1233Crossref PubMed Scopus (364) Google Scholar] due to their superior ability to displace, and resist displacement by, shorter sperm [38Lüpold S. et al.How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster.Curr . Biol. 2012; 22: 1667-1672Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar], exemplifying that mechanisms of CFC and sperm competition are not mutually exclusive and often work through a process of male–female interaction. Once stored, sperm can be lost from the SSOs in a process referred to as sperm 'dumping' [39Snook R.R. Hosken D.J. Sperm death and dumping in Drosophila.Nature. 2004; 428: 939-941Crossref PubMed Scopus (154) Google Scholar] (Figure 1B). Dumping has been suggested to occur in several invertebrate taxa (e.g., [40Barnett M. et al.Female mediation of sperm competition in the millipede Alloporus uncinatus (Diplopoda: Spirostreptidae).Behav . Ecol. Sociobiol. 1995; 36: 413-419Crossref Scopus (18) Google Scholar]). As a key determinant of fertilizing efficiency, sperm swimming performance offers an important mechanism through which females can bias fertilization. Female reproductive fluids are emerging as widespread modulators of sperm swimming. Differential sperm chemotaxis was first demonstrated in a mussel Mytilus galloprovincialis, where chemoattractants in the fluid associated with the eggs differentially mediate the migration of sperm of individual males by changing sperm swimming behavior [41Oliver M. Evans J.P. Chemi