Polyandrous females benefit by producing sons that achieve high reproductive success in a competitive environment

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.     

The evolution of polyandry: an examination of the genetic incompatibility and good‐sperm hypotheses

I have examined the adaptive significance of polyandry using the Australian field cricket Teleogryllus oceanicus. Previous studies of polyandry have examined differences in offspring production by females mated multiply to a single male or females mated multiply to different males. Here I combine this approach with a study of parentage of offspring produced in the later group. Females mated to two different males had a higher proportion of their eggs hatching than did females mating twice with a single male. Offspring fitness parameters were not effected. There was little evidence to suggest that females elevate their hatching success via fertilizing their eggs with sperm from genetically compatible males. Although the average paternity points towards random sperm mixing, there was considerable individual variation in sperm competition success. Patterns of parentage were consistent across females mating twice or four times. Sperm competition success was not related to offspring viability or performance. Thus, the notion that competitively superior sperm produce competitively superior offspring is not supported either. The mechanism underlying increased hatching success with polyandry requires further study.     

Female social preference for males that have evolved via monogamy: evidence of a trade-off between pre- and post-copulatory sexually selected traits?

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.     

The influence of maternal effects on indirect benefits associated with polyandry

Despite numerous and diverse theoretical models for the indirect benefits of polyandry, empirical support is mixed. One reason for the difficulty in detecting indirect benefits of polyandry may be that these are subtle and are mediated by environmental effects, such as maternal effects. Maternal effects may be especially important if females allocate resources to their offspring depending on the characteristics of their mating partners. We test this hypothesis in the burying beetle Nicrophorus vespilloides, a species that provides extensive and direct parental care to offspring. We used a fully factorial design and mated females to one, two, three, four or five different males and manipulated conditions so that their offspring received reduced (12 h) or full (ca 72 h) maternal care. We found that average offspring fitness increased with full maternal care but there was no significant effect of polyandry or the interaction between the duration of maternal care and the level of polyandry on offspring fitness. Thus, although polyandry could provide a mechanism for biasing paternity towards high quality or compatible males, and variation in parental care matters, we found no evidence that female N. vespilloides gain indirect benefits by using parental care to bias the allocation of resources under different mating conditions.     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

Polyandry produces sexy sons at the cost of daughters in red flour beetles

Female mating with multiple males within a single fertile period is a common phenomenon in the animal kingdom. Female insects are particularly promiscuous. It is not clear why females mate with multiple partners despite several potential costs, such as expenditure of time and energy, reduced lifespan, risk of predation and contracting sexually transmitted diseases. Female red flour beetles (Tribolium castaneum) obtain sufficient sperm from a single insemination to retain fertility for several months. Nonetheless they copulate repeatedly within minutes with different males despite no direct fitness benefits from this behaviour. One hypothesis is that females mate with multiple partners to provide indirect benefits via enhanced offspring fitness. To test this hypothesis, we compared the relative fitness of F(1) offspring from females mated with single males and multiple males (2, 4, 8, or 16 partners), under the condition of relatively high intraspecific competition. We found that a female mating with 16 males enhanced the relative fitness of F(1) males (in two out of three trials) but reduced F(1) females' fitness (in two independent trials) in comparison with singly mated females. We also determined whether several important fitness correlates were affected by polyandry. We found that F(1) males from mothers with 16 partners inseminated more females than F(1) males from mothers with a single partner. The viability of the eggs sired or produced by F(1) males and females from highly polyandrous mothers was also increased under conditions of low intra-specific competition. Thus, the effects of polyandry on F(1) offspring fitness depend on environmental conditions. Our results demonstrated a fitness trade-off between male and female offspring from polyandrous mothers in a competitive environment. The mechanisms and biological significance of this unique phenomenon are discussed.     

Polyandrous females acquire indirect benefits in a nuptial feeding species

The relative force of direct and indirect selection underlying the evolution of polyandry is contentious. When females acquire direct benefits during mating, indirect benefits are often considered negligible. Although direct benefits are likely to play a prominent role in the evolution of polyandry, post‐mating selection for indirect benefits may subsequently evolve. We examined whether polyandrous females acquire indirect benefits and quantified direct and indirect effects of multiple mating on female fitness in a nuptial gift‐giving spider (Pisaura mirabilis). In this system, the food item donated by males during mating predicts direct benefits of polyandry. We compared fecundity, fertility and survival of singly mated females to that of females mated three times with the same (monogamy) or different (polyandry) males in a two‐factorial design where females were kept under high and low feeding conditions. Greater access to nutrients and sperm had surprisingly little positive effect on fitness, apart from shortening the time until oviposition. In contrast, polyandry increased female reproductive success by increasing the probability of oviposition, and egg hatching success indicating that indirect benefits arise from mating with several different mating partners rather than resources transferred by males. The evolution of polyandry in a male‐resource‐based mating system may result from exploitation of the female foraging motivation and that indirect genetic benefits are subsequently derived resulting from co‐evolutionary post‐mating processes to gain a reproductive advantage or to counter costs of mating. Importantly, indirect benefits may represent an additional explanation for the maintenance of polyandry.     

No evidence that polyandry benefits females in Drosophila melanogaster

Understanding the evolution of polyandry (mating with multiple males) is a major issue in the study of animal breeding systems. We examined the adaptive significance of polyandry in Drosophila melanogaster, a species with well-documented costs of mating in which males generally cannot force copulations. We found no direct fitness advantages of polyandry. Females that mated with multiple males had no greater mean fitness and no different variance in fitness than females that mated repeatedly with the same male. Subcomponents of reproductive success, including fecundity, egg hatch rate, larval viability, and larval development time, also did not differ between polyandrous and monogamous females. Polyandry had no affect on progeny sex ratios, suggesting that polyandry does not function against costly sex-ratio distorters. We also found no evidence that polyandry functions to favor the paternity of males successful in precopulatory sexual selection. Experimentally controlled opportunities for precopulatory sexual selection had no effect on postcopulatory sperm precedence. Although these results were generally negative, they are supported with substantial statistical power and they help narrow the list of evolutionary explanations for polyandry in an important model species.     

Variation in polyandry and its fitness consequences among populations of the red flour beetle, <Emphasis Type="Italic">Tribolium castaneum</Emphasis>

Female mating with multiple males in a single reproductive period, or polyandry, is a common phenomenon in animals. In this study we investigated variation in female mating behavior and its fitness consequences among three genetic strains of the red flour beetle, Tribolium castaneum. We found that the extent of polyandry and its fitness consequences varied significantly among the strains. In the first strain PRUZ, females mated multiply but incurred costs of polyandry in the form of reduced offspring production. Females of the second strain, NDG11, mated readily with multiple partners and benefited because polyandry led to higher offspring quality. Finally, TIW1 females were resistant to multiple mating and polyandry resulted in lower offspring production but improved offspring quality. Thus, in the first population we observed only costs of polyandry, in the second strain only benefits of polyandry whereas in the third we detected both costs and benefits of polyandry. Possible explanations for such a pattern are discussed.     

Polyandry enhances offspring survival in an infanticidal species

The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus. Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing but sperm, but commit infanticide, can gain non-genetic fitness benefits from polyandry.     

Polyandry and fitness of offspring reared under varying nutritional stress in decorated crickets

Abstract.— Females, by mating with more than one male in their lifetime, may reduce their risk of receiving sperm from genetically incompatible sires or increase their prospects of obtaining sperm from genetically superior sires. Although there is evidence of both kinds of genetic benefits in crickets, their relative importance remains unclear, and the extent to which experimentally manipulated levels of polyandry in the laboratory correspond to those that occur in nature remain unknown. We measured lifetime polyandry of free-living female decorated crickets, Gryllodes sigillatus , and conducted an experiment to determine whether polyandry leads to an increase in offspring viability. We experimentally manipulated both the levels of polyandry and opportunities for females to select among males, randomly allocating the offspring of experimental females to high-food-stress or low-food-stress regimes to complete their development. Females exhibited a high degree of polyandry, mating on average with more than seven different males during their lifetime and up to as many as 15. Polyandry had no effect on either the developmental time or survival of offspring. However, polyandrous females produced significantly heavier sons than those of monandrous females, although there was no difference in the adult mass of daughters. There was no significant interaction between mating treatment and offspring nutritional regimen in their effects on offspring mass, suggesting that benefits accruing to female polyandry are independent of the environment in which offspring develop. The sex difference in the extent to which male and female offspring benefit via their mother's polyandry may reflect possible differences in the fitness returns from sons and daughters. The larger mass gain shown by sons of polyandrous females probably leads to their increased reproductive success, either because of their increased success in sperm competition or because of their increased life span.     

EXPERIMENTAL EVOLUTION OF SPERM QUALITY VIA POSTCOPULATORY SEXUAL SELECTION IN HOUSE MICE

Individuals of many species copulate with multiple mates (polygamy). Multiple mating by females (polyandry) promotes sperm competition, which has broad implications for the evolution of the ejaculate. Multigenerational studies of polygamous insects have shown that the removal of sexual selection has profound fitness consequences for females, and can lead to an evolutionary divergence in ejaculate traits. However, the evolutionary implications of polygamous mating across successive generations have not before been demonstrated in a vertebrate. By manipulating the mating system we were able to reinstate postcopulatory sexual selection in a house mouse population that had a long history of enforced monogamy. Following eight generations of selection, we performed sperm quality assays on males from both the polygamous and monogamous selection lines. We applied a principal component analysis to summarize the variation among 12 correlated sperm traits, and found that males evolving under sperm competition had significantly larger scores on the first axis of variation, reflecting greater numbers of epididymal sperm and increased sperm motility, compared to males from lines under relaxed selection. Moreover, we found a correlated response in the size of litters born to females in lines subject to sperm competition. Thus, we present significant evidence that sperm competition has profound fitness consequences for both male and female house mice.     

BENEFITS OF MULTIPLE MATES IN THE CRICKET GRYLLUS BIMACULATUS

Despite the importance of polyandry for sexual selection, the reasons why females frequently mate with several males remain poorly understood. A number of genetic benefits have been proposed, based on the idea that by taking multiple mates, females increase the likelihood that their offspring will be sired by genetically more compatible or superior males. If certain males have intrinsically “good genes,” any female mating with them will produce superior offspring. Alternatively, if some males have genetic elements that are incompatible with a particular female, then she may benefit from polyandry if the sperm of such males are less likely to fertilize her eggs. We examined these hypotheses in the field cricket Gryllus bimaculatus (Orthoptera: Gryllidae). By allocating females identical numbers of matings but different numbers of mates we investigated the influence of number of mates on female fecundity, and both short- and long-term offspring fitness. This revealed no effect of number of mates on number of eggs laid. However, hatching success of eggs increased with number of mates. This effect could not be attributed to nongenetic effects such as the possibility that polyandry reduces variance in the quantity or fertilizing ability of sperm females receive, because a control group receiving half the number of copulations showed no drop in hatching success. Offspring did not differ in survival, adult mass, size, or development time with treatment. When males were mated to several different females there were no repeatable differences between individual males in the hatching success of their mate's eggs. This suggests that improved hatching success of polyandrous females is not due to certain males having genes that improve egg viability regardless of their mate. Instead, our results support the hypothesis that certain males are genetically more compatible with certain females, and that this drives polyandry through differential fertilization success of sperm from more compatible males.     

Paternity costs from polyandry compensated by increased fecundity in the hide beetle

Polyandry-induced sperm competition is assumed to impose costson males through reduced per capita paternity success. In contrast,studies focusing on the consequences of polyandry for femalesreport increased oviposition rates and fertility. For thesespecies, there is potential for the increased female fecundityassociated with polyandry to offset the costs to males of sharedpaternity. We tested this hypothesis by comparing the proportionand number of offspring sired by males mated with monandrousand polyandrous females in the hide beetle, Dermestes maculates,both for males mating with different females and for males rematingwith the same female. In 4 mating treatments, monandrous femalesmated either once or twice with the same male and polyandrousfemales mated either twice with 2 different males or thricewith 2 males (where 1 male mated twice). Polyandrous and twice-matingmonandrous females displayed greater fecundity and fertilitythan singly mating monandrous females. Moreover, males rematedto the same female had greater paternity regardless of whetherthat female mated with another male. In both polyandrous treatments,male mating order did not affect paternity success. Finally,although the proportion of eggs sired decreased if a male matedwith a polyandrous female, multiply mating females or femalesthat remated with a previous mate laid significantly more eggsand thus the actual number of eggs sired was comparable. Thus,males do not necessarily accrue a net fitness loss when matingwith polyandrous females. This may explain the absence of anyobvious defensive paternity-protection traits in hide beetlesand other species.     

Male house mice produce fewer offspring with lower viability and poorer performance when mated with females they do not prefer

We report experimental results consistent with the hypothesis that constraints on the expression of male mating preferences affect breeder fitness, offspring viability and performance. If constraints on the expression of mating preferences are common, tests of fitness variation associated with mate preferences must eliminate as many constraints on mate preferences as possible. We tested whether male mate preferences influenced breeder fitness, offspring performance and viability in typically polygynous house mice, Mus domesticus, from a feral source population. Our ‘free mate choice’ trials not only eliminated female preferences, male-male and female-female competition, but also our best guesses of the traits mediating choosers' preferences. Males mated with their preferred (P) females sired more litters than males mated with their nonpreferred (NP) females. Offspring viability was significantly lower when males' reproduced with females they did not prefer compared with females they did prefer. Adult sons of males that mated with their P females were socially dominant to sons of males that mated with their NP females. Adult offspring from P pairings built better nests than offspring from NP pairings. The slope of the survivorship curve for P offspring was significantly higher than for NP offspring. These results showed (1) males' mate preferences affected their fitness, (2) males that mated with females they preferred produced more litters than males that mated with females they did not prefer, and (3) their offspring were significantly more viable and performed significantly better on standardized performance tests. This is the first demonstration of fitness benefits of male choice behaviour in a mammal species with typical paternal investment. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

POLYANDRY INCREASES OFFSPRING FECUNDITY IN THE BULB MITE

Abstract The common occurrence of polyandry continues to puzzle evolutionary biologists, as female reproductive success is thought to be limited mostly by her fecundity. Here we test whether females of the bulb mite, a species in which the females are highly promiscuous, benefit from polyandry in terms of increased fitness of their progeny. Females were given opportunity to mate with either one or six males, but the experiment was designed to allow the same number of matings per female in both groups, that is, irrespective of the number of males. We found that daughters of females mated to six males had significantly higher fecundity than daughters of females mated to one male, whereas other fitness components of progeny (male virility and longevity of both sexes) were not affected. These findings appear to support hypotheses proposing that multi-male mating enables females to exercise postcopulatory mate-choice (direct or indirect, via sperm competition) and thus accrue genetic benefits.     

Can paternal effects via seminal fluid contribute to the evolution of polyandry?

Genetic benefits from mating with multiple males are thought to favour the evolution of polyandry. However, recent evidence suggests that non-genetic paternal effects via seminal fluid might contribute to the observed effects of polyandry on offspring performance. Here, we test this hypothesis using the field cricket Teleogryllus oceanicus. Using interference RNA, we first show that at least one seminal fluid protein is essential for embryo survival. We then show that polyandrous females mated to three different males produced embryos with higher pre-hatching viability than did monandrous females mated with the same male three times. Pseudo-polyandrous females that obtained sperm and seminal fluid from a single male and seminal fluid from two additional males had embryos with viabilities intermediate between monandrous and polyandrous females. Our results suggest either that ejaculate mediated paternal effects on embryo viability have both genetic and non-genetic components, or that seminal fluids transferred by castrated males provide only a subset of proteins contained within the normal ejaculate, and are unable to exert their full effect on embryo viability.     

同时而非先后一雌多雄交配增加不同温度下食蚜瓢虫的适合度（英文）

【目的】尽管一雌多雄在瓢虫科中常见,但各研究中获得的数据不足以解释雌虫多次交配和一雌多雄的一般适应性意义或适合度后果。本研究以温度为胁迫因子,旨在评价一雌多雄的某些益处（如增加的适合度）是否可传递给后代。【方法】本研究检测了黄斑盘瓢虫Coelophora saucia (Mulsant) 3种交配处理中的适合度：一雌一雄（与同一雄虫交配5次,1次/d）,先后一雌多雄（与5头不同的雄虫依次交配5次,即每天与新的雄虫交配1次）,以及同时一雌多雄（放进5头雄虫,任由雌虫选择雄虫,交配5次,1次/d）。观察了各交配处理不同温度下（25, 27和 30℃）繁殖力、卵的育性、后代发育和存活。【结果】结果表明,经历一雌多雄然后进行交配选择或竞争的雌性的繁殖能力最强,后代能在更广温度范围内最好地适应发育和存活。但先后一雌多雄交配的雌性与一雌一雄交配的雌性的繁殖能力相似。【结论】结果说明,在无交配选择或雄性竞争的条件下,一雌多雄的益处不明显。这可能是由于在依次射精的雄性间存在精子竞争,或由于雌性的隐性选择。据我们所知,本研究中观察发现的无交配选择时不表现一雌多雄的益处的现象,之前在昆虫中未观察到过。     

Fitness benefits of polyandry for experienced females

Females often mate with several different males, which may promote sperm competition and increase offspring viability. However, the potential benefits of polyandry remain controversial, particularly in birds where recent reviews have suggested that females gain few genetic benefits from extra‐pair mating. In tree swallows (Tachycineta bicolor), we found that females with prior breeding experience had more sires per brood when paired to genetically similar social mates, and, among experienced females, broods with more sires had higher hatching success. Individual females breeding in two consecutive years also produced broods with more sires when they were more genetically similar to their mate. Thus, experienced females were able to avoid the costs of mating with a genetically similar social mate and realize fitness benefits from mating with a relatively large number of males. This is one of the first studies to show that female breeding experience influences polyandry and female fitness in a natural population of vertebrates. Our results suggest that the benefits of polyandry may only be clear when considering both the number of mates females acquire and their ability to modify the outcome of sexual conflict.     

Measuring polyandry in wild populations: a case study using promiscuous crickets

Mating rate has important implications for patterns of sexual selection and sexual conflict and hence for issues such as speciation and the maintenance of genetic diversity. Knowledge of natural mating rates can provide insights into the factors driving female mating behaviour. We investigated the level of polyandry in a Spanish population of the field cricket Gryllus bimaculatus using microsatellite markers. Two approaches were employed: (i) genotyping the offspring of wild-caught gravid females to determine the number of males siring the brood and (ii) genotyping sperm stored in the spermathecae of females mated in the wild to estimate the number of mating partners. We compared existing methods for inferring the minimum and probable number of fathers and described a novel probabilistic technique estimating the number of mates by genotyping stored sperm. Using the most conservative allele-counting method, 71% of females produced offspring sired by at least two males (a minimum mean of 2.4 fathers per clutch), and all females had mated to at least two males with minimum mean estimates of 2.7-5.1 mates per female. Our study reveals high levels of polyandry in the wild and suggests that females mate with more males than sire their offspring.