RESUMEN
Studies of socially mediated phenotypic plasticity have demonstrated adaptive male responses to the 'competitive' environment. Despite this, whether variation in the paternal social environment also influences offspring reproductive potential in an intergenerational context has not yet been examined. Here, we studied the descendants of wild-caught house mice, a destructive pest species worldwide, to address this knowledge gap. We analysed traits that define a 'competitive' phenotype in the sons of males (sires) that had been exposed to either a high-male density (competitive) or high-female density (non-competitive) environment. We report disparate reproductive strategies among the sires: high-male density led to a phenotype geared for competition, while high-female density led to a phenotype that would facilitate elevated mating frequency. Moreover, we found that the competitive responses of sires persisted in the subsequent generation, with the sons of males reared under competition having elevated sperm quality. As all sons were reared under common-garden conditions, variation in their reproductive phenotypes could only have arisen via nongenetic inheritance. We discuss our results in relation to the adaptive advantage of preparing sons for sperm competition and suggest that intergenerational plasticity is a previously unconsidered aspect in invasive mammal fertility control.
Asunto(s)
Semen , Espermatozoides , Animales , Ratones , Masculino , Femenino , Espermatozoides/fisiología , Reproducción , Adaptación Fisiológica , Mamíferos , Conducta Sexual AnimalRESUMEN
Male-male competition after mating (sperm competition) favours adaptations in male traits, such as elevated sperm numbers facilitated by larger testes. Ultimately, patterns of female distribution will affect the strength of sperm competition by dictating the extent to which males are able to prevent female remating. Despite this, our understanding of how the spatial and temporal distributions of mating opportunities have shaped the evolutionary course of sperm competition is limited. Here, we use phylogenetic comparative methods to explore interspecific variation in testes size in relation to patterns of female distribution in Australian rodents. We find that as mating season length (temporal distribution of females) increases, testes size decreases, which is consistent with the idea that it is difficult for males to prevent females from remating when overlap among oestrous females is temporally concentrated. Additionally, we find that social species (spatially clustered) have smaller testes than non-social species (spatially dispersed). This result suggests that males may be effective in monopolizing reproduction within social groups, which leads to reduced levels of sperm competition relative to non-social species where free-ranging females cannot be controlled. Overall, our results show that patterns of female distribution, in both space and time, can influence the strength of post-mating sexual selection among species.
Asunto(s)
Espermatozoides , Testículo , Animales , Australia , Femenino , Masculino , Filogenia , RoedoresRESUMEN
Reproductive proteins typically have high rates of molecular evolution, and are assumed to be under positive selection from sperm competition and cryptic female choice. However, ascribing evolutionary divergence in the genome to these processes of sexual selection from patterns of association alone is problematic. Here, we use an experimental manipulation of postmating sexual selection acting on populations of house mice and explore its consequences for the expression of seminal vesicle secreted (SVS) proteins. Following 25 generations of selection, males from populations subjected to postmating sexual selection had evolved increased expression of at least two SVS genes that exhibit the signature of positive selection at the molecular level, SVS1 and SVS2. These proteins contribute to mating plug formation and sperm survival in the female reproductive tract. Our data thereby support the view that sexual selection is responsible for the evolution of these seminal fluid proteins.
Asunto(s)
Proteínas de Secreción de la Vesícula Seminal/genética , Selección Sexual , Animales , Evolución Biológica , Femenino , Expresión Génica , Masculino , RatonesRESUMEN
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.
Asunto(s)
Células del Cúmulo/fisiología , Matriz Extracelular/fisiología , Fertilización/fisiología , Ratones/fisiología , Proteoma , Animales , Evolución Biológica , Femenino , Fertilización/genéticaRESUMEN
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 in utero offspring sex ratios in house mice (Mus musculus domesticus), 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.
Asunto(s)
Ratones/fisiología , Razón de Masculinidad , Estrés Fisiológico/fisiología , Animales , Conducta Animal , Femenino , Masculino , Mamíferos , ReproducciónRESUMEN
Mammal sex allocation research has focused almost exclusively on maternal traits, but it is now apparent that fathers can also influence offspring sex ratios. Parents that produce female offspring under conditions of intense male-male competition can benefit with greater assurance of maximized grand-parentage. Adaptive adjustment in the sperm sex ratio, for example with an increase in the production of X-chromosome bearing sperm (CBS), is one potential paternal mechanism for achieving female-biased sex ratios. Here, we tested this mechanistic hypothesis by varying the risk of male-male competition that male house mice perceived during development, and quantifying sperm sex ratios at sexual maturity. Our analyses revealed that males exposed to a competitive 'risk' produced lower proportions of Y-CBS compared to males that matured under 'no risk' of competition. We also explored whether testosterone production was linked to sperm sex ratio variation, but found no evidence to support this. We discuss our findings in relation to the adaptive value of sperm sex ratio adjustments and the role of steroid hormones in socially induced sex allocation.
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Razón de Masculinidad , Espermatozoides , Animales , Femenino , Masculino , Mamíferos , Ratones , Conducta Sexual AnimalRESUMEN
Landscape topography and the mobility of individuals will have fundamental impacts on a species' population structure, for example by enhancing or reducing gene flow and therefore influencing the effective size and genetic diversity of the population. However, social organization will also influence population genetic structure. For example, species that live and breed in cooperative groups may experience high levels of inbreeding and strong genetic drift. The western pebble-mound mouse (Pseudomys chapmani), which occupies a highly heterogeneous, semi-arid landscape in Australia, is an enigmatic social mammal that has the intriguing behaviour of working cooperatively in groups to build permanent pebble mounds above a subterranean burrow system. Here, we used both nuclear (microsatellite) and mitochondrial (mtDNA) markers to analyse the range-wide population structure of western pebble-mound mice sourced from multiple social groups. We observed high levels of genetic diversity at the broad scale, very weak genetic differentiation at a finer scale and low levels of inbreeding. Our genetic analyses suggest that the western pebble-mound mouse population is both panmictic and highly viable. We conclude that high genetic connectivity across the complex landscape is a consequence of the species' ability to permeate their environment, which may be enhanced by "boom-bust" population dynamics driven by the semi-arid climate. More broadly, our results highlight the importance of sampling strategies to infer social structure and demonstrate that sociality is an important component of population genetic structure.
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Ecosistema , Muridae/genética , Conducta Social , Animales , Australia , ADN Mitocondrial , Variación Genética , Genotipo , Repeticiones de MicrosatéliteRESUMEN
Males are known to adjust their expenditure on testes growth and sperm production in response to sperm competition risk. Genital morphology can also contribute to competitive fertilization success but whether male genital morphology can respond plastically to the sperm competition environment has received little attention. Here, we exposed male house mice to two different sperm competition environments during their sexual development and quantified phenotypic plasticity in baculum morphology. The sperm competition environment generated plasticity in body growth. Males maturing under sperm competition risk were larger and heavier than males maturing under no sperm competition risk. We used a landmark-based geometric morphometric approach to measure baculum size and shape. Independent of variation in body size, males maintained under risk of sperm competition had a relatively thicker and more distally extended baculum bulb compared with males maintained under no sperm competition risk. Plasticity in baculum shape paralleled evolutionary responses to selection from sperm competition reported in previous studies of house mice. Our findings provide experimental evidence of socially mediated phenotypic plasticity in male genitalia.
Asunto(s)
Genitales Masculinos/anatomía & histología , Ratones/crecimiento & desarrollo , Conducta Sexual Animal , Espermatozoides/fisiología , Animales , Tamaño Corporal , Masculino , Ratones/anatomía & histología , Fenotipo , Maduración SexualRESUMEN
Due to the physiological cost of sperm production, males are expected to be prudent in their expenditure and adjust their investment according to current social conditions. Strategic adjustments in sperm expenditure during development can be made via changes in testes size, sperm production rates or testes tissue composition. Here, using house mice, we test the hypothesis that elevated sperm production is driven by a plastic response in the spatial organization of the testes. We reared males under different social conditions (competitive vs. noncompetitive) and quantified sperm number and the proportion of sperm-producing tissue within the testes. Further, because sperm quality is a critical determinant of competitive fertilization success, we used computer-assisted sperm analysis to quantify six sperm motility traits. Our investigation revealed that males reared in an environment with a perceived risk of reproductive competition produced more sperm in the absence of changes in testes morphology. We discuss this result in relation to fixed and flexible phenotypically plastic responses to future competitive conditions, and conclude that adaptive adjustments in sperm number in response to the social environment are likely attributable to variation in sperm production rate. Further, we found no difference in in vitro sperm motility parameters among males from the different social environment regimes. Overall, this investigation improves our understanding of the mechanisms of male plastic responses to reproductive competition experienced during sexual development.
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Conducta Competitiva , Espermatogénesis/fisiología , Testículo/anatomía & histología , Animales , Masculino , Ratones , Medio Social , Recuento de Espermatozoides , Motilidad Espermática , Espermatozoides/fisiología , Testículo/fisiologíaRESUMEN
Drive genes are genetic elements that manipulate the 50% ratio of Mendelian inheritance in their own favour, allowing them to rapidly propagate through populations. The action of drive genes is often hidden, making detection and identification inherently difficult. Yet drive genes can have profound evolutionary consequences for the populations that harbour them: most known drivers are detrimental to organismal gamete development, reproduction and survival. In this study, we identified the presence of a well-known drive gene called t haplotype post hoc in eight replicate selection lines of house mice that had been evolving under enforced monandry or polyandry for 20 generations. Previous work on these selection lines reported an increase in sperm competitive ability in males evolving under polyandry. Here, we show that this evolutionary response can be partly attributed to gene drive. We demonstrate that drive-carrying males are substantially compromised in their sperm competitive ability. As a consequence, we found that t frequencies declined significantly in the polyandrous lines while remaining at stable, high levels in the monandrous lines. For the first time in a vertebrate, we thus provide direct experimental evidence that the mating system of a species can have important repercussions on the spread of drive genes over evolutionary relevant timescales. Moreover, our work highlights how the covert action of drive genes can have major, potentially unintended impact on our study systems.
Asunto(s)
Evolución Molecular , Genética de Población , Patrón de Herencia , Ratones/genética , Espermatozoides/fisiología , Animales , Femenino , Aptitud Genética , Haplotipos , Masculino , Reproducción/genéticaRESUMEN
Reproduction among related individuals is generally maladaptive. Inbreeding imposes significant costs on individual reproductive success, and can decrease population fitness. Theory predicts that polyandrous females can avoid inbreeding by exploiting paternity-biasing mechanisms that enable differential sperm 'use'. Evidence of sperm selection is difficult to demonstrate because patterns of non-random paternity can be generated by a variety of different mechanisms. Here, using in vitro fertilisation in mice, we provide evidence of sperm selection at the gametic level. We mixed the sperm of sibling and non-sibling males, and observed a fertilisation bias towards the sperm of non-sibling males. The number of motile sperm and sperm swimming performance did not differ between competitors among the replicate assays. Therefore, our result can only be ascribed to egg-driven sperm selection against related sperm. We conclude that the expression or secretion of gametic proteins could provide the molecular basis for this mechanism of cryptic female choice.
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Endogamia , Ratones/genética , Óvulo/fisiología , Reproducción/genética , Espermatozoides/fisiología , Animales , Femenino , Fertilización In Vitro , Modelos Lineales , Masculino , Preferencia en el Apareamiento Animal , LinajeRESUMEN
Theoretical models have suggested that sperm competition can lead to increased ova resistance to fertilization. While there is some comparative evidence that this might be true, there is no experimental evidence to show that ova defensiveness evolves in response to sperm competition. We performed a series of in vitro fertilization assays to gauge the fertilizability of ova produced by female house mice from experimental populations that evolved either with or without sperm competition. Our analysis revealed that after 24 generations of experimental evolution, females that evolved under a polygamous regime produced more defensive ova than females that evolved under a monogamous regime. We therefore provide the first direct line of evidence that sperm competition can generate sexual conflict at the gametic level and lead to asymmetries in fertilization rates among populations. Our results show that females respond to sperm competition via fertilization barriers that have the potential to mediate sperm entry.
Asunto(s)
Evolución Biológica , Óvulo/fisiología , Selección Genética , Espermatozoides/fisiología , Animales , Femenino , Fertilización , Fertilización In Vitro , Masculino , RatonesRESUMEN
When females mate with multiple males both pre- and post-copulatory sexual selections occur. It has been suggested that females benefit from polyandry when better-quality males are successful in sperm competition and sire high-quality offspring. Indeed, studies of experimental evolution have confirmed that sperm competition selects for both increased ejaculate quality and elevated offspring viability. Fewer investigations have explored whether these fitness benefits are evident beyond early life-history stages. Here, I used house mice (Mus domesticus) from selection lines that had been evolving for 25 generations under either polygamy or monogamy to test whether females preferred males from lines that had evolved with sperm competition. Males from the polygamous lines had previously been shown to achieve a fitness advantage under semi-natural conditions, deeming them to be of high genetic quality and leading to the a priori expectation that females would prefer males that had evolved with sperm competition compared with males that had not. Contrary to expectation, the data showed that sexually receptive females spent more time associating with males from the monogamous lines. This unexpected but interesting result is discussed in relation to sperm competition theory that predicts a trade-off between male investment in pre- and post-copulatory sexually selected traits.
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Conducta Animal/fisiología , Evolución Biológica , Preferencia en el Apareamiento Animal , Conducta Sexual Animal , Animales , Femenino , Masculino , RatonesRESUMEN
Theory predicts that sperm competition will generate sexual conflict that favours increased ovum defences against polyspermy. A recent study on house mice has shown that ovum resistance to fertilization coevolves in response to increased sperm fertilizing capacity. However, the capacity for the female gamete to adjust its fertilizability as a strategic response to sperm competition risk has never, to our knowledge, been studied. We sourced house mice (Mus domesticus) from natural populations that differ in the level of sperm competition and sperm fertilizing capacity, and manipulated the social experience of females during their sexual development to simulate conditions of either a future 'risk' or 'no risk' of sperm competition. Consistent with coevolutionary predictions, we found lower fertilization rates in ova produced by females from a high sperm competition population compared with ova from a low sperm competition population, indicating that these populations are divergent in the fertilizability of their ova. More importantly, females exposed to a 'risk' of sperm competition produced ova that had greater resistance to fertilization than ova produced by females reared in an environment with 'no risk'. Consequently, we show that variation in sperm competition risk during development generates phenotypic plasticity in ova fertilizability, which allows females to prepare for prevailing conditions during their reproductive life.
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Fertilización , Ratones/fisiología , Óvulo/fisiología , Fenotipo , Espermatozoides/fisiología , Animales , Femenino , Fertilización In Vitro , Masculino , Preferencia en el Apareamiento Animal , Olfato , Australia OccidentalRESUMEN
Sex allocation theories predict that under different ecological conditions the production of sons and daughters will affect parental fitness differently. Skewed offspring sex ratios often occur under captive conditions where individuals are exposed to nutritional and social conditions that differ from nature. Here, we analyzed 29 years of offspring sex ratio data from a captive population of an endangered marsupial, the Numbat (Myrmecobius fasciatus). We partitioned variation in offspring sex ratio based on parental origin (captive- vs. wild-bred), parental weight, maternal age, and maternal reproductive history. Our analyses revealed no effect of parental weight or maternal origin on offspring sex ratio-however, there was a significant effect of paternal origin. Data visualization indicated that captive-bred males tended to produce male-biased litters. We discuss the result in relation to recent studies that have shown that male mammals have the capacity to be arbiters of sex allocation and highlight candidate mechanisms, but consider it with caution due to the small sample size from which the result was derived. We performed a population viability analysis (PVA) to explore the potential impact of a sex ratio skew on the sustainability of the captive Numbat population under hypothetical scenarios. Our PVA revealed that supplementation with wild individuals is critical to the persistence of the captive Numbat population and that a biased sex ratio will lead to extinction of the captive colony under certain conditions. Overall, our study demonstrates that covert sex ratio skews can persist undetected in captive populations, which have the potential to become impactful and compromise population sustainability under changed management processes.
RESUMEN
Although mating is costly, multiple mating by females is a taxonomically widespread phenomenon. Theory has suggested that polyandry may allow females to gain genetic benefits for their offspring, and thus offset the costs associated with this mating strategy. For example, the good sperm hypothesis posits that females benefit from mating multiply when genetically superior males have increased success in sperm competition and produce high quality offspring. We applied the powerful approach of experimental evolution to explore the potential for polyandry to drive evolutionary increases in female fitness in house mice, Mus domesticus. We maintained polygamously mated and monogamously mated selection lines of house mice for 14 generations, before determining whether selection history could account for divergence in embryo viability. We found that males from lineages evolving with post-copulatory sexual selection sire offspring with increased viability, suggesting that polyandry results in the production of higher quality offspring and thus provides long-term fitness benefits to females.
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Embrión de Mamíferos/fisiología , Preferencia en el Apareamiento Animal , Animales , Evolución Biológica , Femenino , Masculino , Ratones , Espermatozoides/fisiologíaRESUMEN
BACKGROUND: 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. RESULTS: 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. CONCLUSION: 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.
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Evolución Biológica , Ratones/fisiología , Motilidad Espermática , Espermatozoides/citología , Animales , Femenino , Genotipo , Masculino , Ratones/genética , Repeticiones de Microsatélite , Fenotipo , Recuento de EspermatozoidesRESUMEN
Females of many taxa often copulate with multiple males and incite sperm competition. On the premise that males of high genetic quality are more successful in sperm competition, it has been suggested that females may benefit from polyandry by accruing 'good genes' for their offspring. Laboratory studies have shown that multiple mating can increase female fitness through enhanced embryo viability, and have exposed how polyandry influences the evolution of the ejaculate. However, such studies often do not allow for both female mate choice and male-male competition to operate simultaneously. Here, I took house mice (Mus domesticus) from selection lines that had been evolving with (polygamous) and without (monogamous) sperm competition for 16 generations and, by placing them in free-ranging enclosures for 11 weeks, forced them to compete for access to resources and mates. Parentage analyses revealed that female reproductive success was not influenced by selection history, but there was a significant paternity bias towards males from the polygamous selection lines. Therefore, I show that female house mice benefit from polyandry by producing sons that achieve increased fitness in a semi-natural environment.
Asunto(s)
Evolución Biológica , Conducta Competitiva , Matrimonio , Reproducción , Conducta Sexual Animal , Espermatozoides , Animales , Femenino , Masculino , Preferencia en el Apareamiento Animal , Ratones , Reproducción/genética , Espermatozoides/fisiologíaRESUMEN
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.
Asunto(s)
Evolución Biológica , Tamaño de la Célula , Pieza Intermedia del Espermatozoide/ultraestructura , Motilidad Espermática/fisiología , Espermatozoides/citología , Análisis de Varianza , Animales , Cruzamientos Genéticos , Masculino , RatonesRESUMEN
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'.