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.
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).
Meiotic drivers are genetic variants that selfishly manipulate the production of gametes to increase their own rate of transmission, often to the detriment of the rest of the genome and the ...individual that carries them. This genomic conflict potentially occurs whenever a diploid organism produces a haploid stage, and can have profound evolutionary impacts on gametogenesis, fertility, individual behaviour, mating system, population survival, and reproductive isolation. Multiple research teams are developing artificial drive systems for pest control, utilising the transmission advantage of drive to alter or exterminate target species. Here, we review current knowledge of how natural drive systems function, how drivers spread through natural populations, and the factors that limit their invasion.
Both naturally occurring and synthetic ‘meiotic drivers’ violate Mendel's law of equal segregation and can rapidly spread through populations even when they reduce the fitness of individuals carrying them.
Synthetic drivers are being developed to spread desirable genes in natural populations of target species. How ecology influences the population dynamics of meiotic drivers is important for predicting the success of synthetic drive elements.
An enduring puzzle concerns why some meiotic drivers persist at stable, intermediate frequencies rather than sweeping to fixation.
Drivers can have a wide range of consequences from extinction to changes in mating system.
Males and females rarely have identical evolutionary interests over reproduction, and when the fitness of both sexes is dependent upon paternity outcomes, sexual conflict over fertilization is ...inevitable. In internal fertilizers, the female tract is a formidable selective force on the number and integrity of sperm that reach the egg. Selection on sperm quality is intensified when females mate multiply and rival males are forced to compete for fertilizations. While male adaptations to sperm competition have been well documented (e.g., increased sperm fertilizing capacity), much less attention has been given to the evolutionary consequences of postmating sexual conflict for egg form and function. Specifically, increased sperm competitiveness can be detrimental by giving rise to an elevation in reproductive failure resulting from polyspermy. Spanning literature on both internal and external fertilizers, in this review I discuss how females respond to sperm competition via fertilization barriers that mediate sperm entry. These findings, which align directly with sexual conflict theory, indicate that females have greater control over fertilization than has previously been appreciated. I then consider the implications of gametic sexual conflict in relation to the development of reproductive isolation and speculate on potential mechanisms accounting for “egg defensiveness.” Finally, I discuss the functional significance of egg defensiveness for both the sexes, and sperm selection for females.
Male genitalia exhibit a taxonomically widespread pattern of rapid and divergent evolution. Sexual selection is generally believed to be responsible for these patterns of evolutionary divergence, ...although empirical support for the sexual selection hypothesis comes mainly from studies of insects. Here we show that sexual selection is responsible for an evolutionary divergence in baculum morphology among populations of house mice Mus domesticus. We sourced mice from three isolated populations known to be subject to differing strengths of postcopulatory sexual selection and bred them under common-garden conditions. Mice from populations with strong postcopulatory sexual selection had bacula that were relatively thicker compared with mice from populations with weak selection. We used experimental evolution to determine whether these patterns of divergence could be ascribed to postcopulatory sexual selection. After 27 generations of experimental evolution, populations of mice subjected to postcopulatory sexual selection evolved bacula that were relatively thicker than populations subjected to enforced monogamy. Our data thereby provide evidence that postcopulatory sexual selection underlies an evolutionary divergence in the mammalian baculum and supports the hypothesis that sexual selection plays a general role in the evolution of male genital morphology across evolutionary diverse taxonomic groups.
Although initially lagging behind discoveries being made in other taxa, mammalian sperm competition is now a productive and advancing field of research. Sperm competition in mammals is not merely a ...'sprint-race' between the gametes of rival males, but rather a race over hurdles; those hurdles being the anatomical and physiological barriers provided by the female reproductive tract, as well as the egg and its vestments. With this in mind, in this review, I discuss progress in the field while focusing on the female perspective. I highlight ways by which sperm competition can have positive effects on female reproductive success and discuss how competitive outcomes are not only owing to dynamics between the ejaculates of rival males, but also attributable to mechanisms by which female mammals bias paternity toward favourable sires. Drawing on examples across different species-from mice to humans-I provide an overview of the accumulated evidence which firmly establishes that sperm competition is a key selective force in the evolution of male traits and detail how females can respond to increased sperm competitiveness with increased egg resistance to fertilization. I also discuss evidence for facultative responses to the sperm competition environment observed within mammal species. Overall, this review identifies shortcomings in our understanding of the specific mechanisms by which female mammals 'select' sperm. More generally, this review demonstrates how, moving forward, mammals will continue to be effective animal models for studying both evolutionary and facultative responses to sperm competition. This article is part of the theme issue 'Fifty years of sperm competition'.
Studies of fertilization biology often focus on sperm and egg interactions. However, before gametes interact, mammalian sperm must pass through the cumulus layer; in mice, this consists of several ...thousand cells tightly glued together with hyaluronic acid and other proteins. To better understand the role of cumulus cells and their extracellular matrix, we perform proteomic experiments on cumulus oophorus complexes (COCs) in house mice (Mus musculus), producing over 24,000 mass spectra to identify 711 proteins. Seven proteins known to stabilize hyaluronic acid and the extracellular matrix were especially abundant (using spectral counts as an indirect proxy for abundance). Through comparative evolutionary analyses, we show that three of these evolve rapidly, a classic signature of genes that influence fertilization rate. Some of the selected sites overlap regions of the protein known to impact function. In a follow-up experiment, we compared COCs from females raised in two different social environments. Female mice raised in the presence of multiple males produced COCs that were smaller and more resistant to dissociation by hyaluronidase compared to females raised in the presence of a single male, consistent with a previous study that demonstrated such females produced COCs that were more resistant to fertilization. Although cumulus cells are often thought of as enhancers of fertilization, our evolutionary, proteomic, and experimental investigations implicate their extracellular matrix as a potential mediator of fertilization outcomes. Summary sentence Cumulus cell protein identification reveals potential roles in fertilization outcomes. Graphical Abstract
A shift from the traditional perspective that maternal stress is invariably costly has instigated recent interest into its adaptive role in offspring sex allocation. Stress generated by social ...instability has been linked to offspring sex ratio biases that favour the production of female offspring, which converges with the theoretical prediction that mothers in the poor condition are better off investing in daughters rather than sons. However, previous research has failed to disentangle two different processes: the passive consequence of maternal stress on sex-specific mortality and the adaptive effect of maternal stress at the time of conception. Here, I show that exposure to high male density social conditions leads to elevated stress hormone levels and female-biased
offspring sex ratios in house mice (
), and identify that sex-specific offspring production-not sex-specific mortality-is the mechanism accounting for these sex ratio skews. This outcome reflects the optimal fitness scenario for mothers in a male-dominated environment: the production of daughters, who are guaranteed high mate availability, minimizes male-male competition for their sons. Overall, this study supports the idea that maternal stress has the potential to be adaptive and advances our understanding of how exposure to different social conditions can influence sex allocation in mammals.
When females mate with multiple partners, sperm from rival males compete to fertilize the ova. Studies of experimental evolution have proven the selective action of sperm competition on male ...reproductive traits. However, while reproductive traits may evolve in response to sperm competition, this does not necessarily provide evidence that sperm competitive ability responds to selection. Indeed, a study of Drosophila failed to observe divergence in sperm competitive ability of males in lines selected for enhanced sperm offence and defence.
Adopting the naturally polygamous house mouse (Mus domesticus) as our vertebrate model, we performed an experimental evolution study and observed genetic divergence in sperm quality; males from the polygamous selection lines produced ejaculates with increased sperm numbers and greater sperm motility compared to males from the monogamous lines. Here, after 12 generations of experimental evolution, we conducted competitive matings between males from lineages evolving under sperm competition and males from lineages subject to relaxed selection. We reduced variation in paternity arising from embryo mortality by genotyping embryos in utero at 14 days gestation. Our microsatellite data revealed a significant paternity bias toward males that evolved under the selective regime of sperm competition.
We provide evidence that the sperm competitiveness phenotype can respond to selection, and show that improved sperm quality translates to greater competitive fertilisation success in house mice.
Investigations into the evolution of reproductive barriers have traditionally focused on closely related species, and the prevalence of conspecific sperm precedence. The effectiveness of conspecific ...sperm precedence at limiting gene exchange between species suggests that gametic isolation is an important component of reproductive isolation. However, there is a paucity of tests for evidence of sperm precedence during the earlier stages of divergence, for example among isolated populations. Here, we sourced individuals from two allopatric populations of house mice (Mus domesticus) and performed competitive in vitro fertilisation assays to test for conpopulation sperm precedence specifically at the gametic level. We found that ova population origin did not influence the outcome of the sperm competitions, and thus provide no evidence of conpopulation or heteropopulation sperm precedence. Instead, we found that males from a population that had evolved under a high level of postcopulatory sexual selection consistently outcompeted males from a population that had evolved under a relatively lower level of postcopulatory sexual selection. We standardised the number of motile sperm of each competitor across the replicate assays. Our data therefore show that competitive fertilizing success was directly attributable to differences in sperm fertilizing competence.
Evolutionary biologists have argued that there should be a positive relationship between sperm size and sperm velocity, and that these traits influence a male's sperm competitiveness. However, ...comparative analyses investigating the evolutionary associations between sperm competition risk and sperm morphology have reported inconsistent patterns of association, and in vitro sperm competition experiments have further confused the issue; in some species, males with longer sperm achieve more competitive fertilization, while in other species males with shorter sperm have greater sperm competitiveness. Few investigations have attempted to address this problem. Here, we investigated the relationship between sperm morphology and sperm velocity in house mice (Mus domesticus). We conducted in vitro sperm velocity assays on males from established selection lines, and found that sperm midpiece size was the only phenotypic predictor of sperm swimming velocity.
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