Polyandrous females provide sons with more competitive sperm: Support for the sexy‐sperm hypothesis in the rattlebox moth (Utetheisa ornatrix)

Given the costs of multiple mating, why has female polyandry evolved? Utetheisa ornatrix moths are well suited for studying multiple mating in females because females are highly polyandrous over their life span, with each male mate transferring a substantial spermatophore with both genetic and nongenetic material. The accumulation of resources might explain the prevalence of polyandry in this species, but another, not mutually exclusive, possibility is that females mate multiply to increase the probability that their sons will inherit more‐competitive sperm. This latter “sexy‐sperm” hypothesis posits that female multiple mating and male sperm competitiveness coevolve via a Fisherian runaway process. We tested the sexy‐sperm hypothesis by using competitive double matings to compare the sperm competition success of sons of polyandrous versus monandrous females. In accordance with sexy‐sperm theory, we found that in 511 offspring across 17 families, the male whose polyandrous mother mated once with each of three different males sired significantly more of all total offspring (81%) than did the male whose monandrous mother was mated thrice to a single male. Interestingly, sons of polyandrous mothers had a significantly biased sex ratio of their brood toward sons, also in support of the hypothesis.     

Can females gain extra paternal investment by mating with multiple males? A game theoretic approach

Although females may require only one mating to become inseminated, many female animals engage in costly mating with multiple males. One potential benefit of polyandrous mating is gaining parental investment from multiple males. We developed two game theoretic models to explore this possibility. Our first model showed that male care of multiple females' offspring evolves when male help substantially increases offspring fitness, future mating opportunity is limited, and group size is small. In our second model, we assumed that males invest in the offspring of former mates and evaluated the fitness consequences of female monogamous and polyandrous mating strategies. Females benefit only from limited polyandry, that is, mating with several males. Polyandry is discouraged because females must share male investment with other polyandrous females, and paternal care is likely to experience diminishing returns. Females may enhance their access to male investment by competing with rival females and monopolizing investment, however. The results support the argument that females can gain paternal investment by mating with several males in small social groups (e.g., dunnocks Prunella modularis). The results do not support the argument that females can gain paternal investment from pronounced multiple mating in large social groups, however, as observed in many primate species.     

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.     

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.     

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.     

Male house mice evolving with post-copulatory sexual selection sire embryos with increased viability

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.     

Costs and benefits of polyandry in the egg parasitoid Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae)

Polyandry implies costs (i.e., time, energy, predation risk, etc.) especially in short-lived parasitoid species but females of several hymenopteran parasitoid species, mostly gregarious, do mate with multiple males. Several hypotheses have been proposed to explain the benefits of polyandry but controversy remains, especially in facultative gregarious species that bridge the gap between solitary and gregarious development. In this study, we investigated the possibility that polyandry may bring material benefits to Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) females, a short-lived and facultative gregarious egg parasitoid. Females mated several times with different males both at emergence and throughout their life. No significant difference was found in the offspring sex ratio and the fecundity of multiple mated and single mated females and pre-mating duration increased with the female’s age. The longevity of females did vary significantly with the number of matings but only in the presence of hosts. Female T. evanescens received enough sperm from one mating to allocate an optimal offspring sex ratio and we found no evidence of either nutritional resources or convenience polyandry in this species. Polyandry in facultative gregarious parasitoids might be an adaptive strategy to minimize the risk of mating with males that have already emptied their sperm bank or to accumulate sperm from several partially sperm-depleted males. Polyandry may also increase the probability of non-sib mating in patches exploited by several females.     

The effect of mating frequency and mating pattern on female reproductive fitness in cabbage beetle,Colaphellus bowringi

It is generally thought that females can receive more of the material benefits from males by increasing mating frequency and polyandry can lead to greater reproductive success. The cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae), is a highly promiscuous species, in which females or males can readily mate repeatedly with a given partner or multiple partners at a very high frequency. In the present study, the effect of mating frequency (number of matings) and mating pattern (polyandry vs. monogamy) on female reproductive fitness was investigated by measuring fecundity, fertility, and female longevity. The results indicated that increased female mating frequency with the same male did not result in variation in lifetime fecundity, but significantly increased fertility and decreased female longevity. Moreover, five copulations were sufficient to acquire maximal reproductive potential. Female lifetime fecundity also did not differ between polyandrous and monogamous treatments. However, monogamous females exhibited a significant increase in fertility and significant prolongation of longevity compared with polyandrous females, further demonstrating that monogamy is superior to polyandry in this beetle.     

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.     

A theoretical study on the evolution of male parental care and female multiple mating: effects of female mate choice and male care bias

Male parental care and female multiple mating are seen in many species in spite of the cost they entail. Moreover, they even coexist in some species though polyandry, by reducing paternity confidence of caregiving males, seems to hinder the evolution of paternal care. Previous studies have investigated the coevolutionary process of paternal care and polyandry under various simplifying assumptions, including random mating and random provision of male care. We extend these models to examine possible effects of female mate choice and male care bias, assuming that (a) monandrous females mate preferentially with caregiving males while polyandrous females compromise their preference in order to mate with multiple males and (b) caregiving males tend to direct their care to offspring of monandrous females. Our models suggest that both the female preference and the male bias always favor caregiving males while they may not always facilitate the evolution of monandry.     

Copulation reduces male but not female longevity in Saltella sphondylli (Diptera: Sepsidae)

Mating more than once is extremely costly for females in many species, making the near ubiquity of polyandry difficult to understand. However, evidence of mating costs for males is much rarer. We investigated the effects of copulation on longevity of male and female flies (Saltella sphondylli). We also scrutinized potential fecundity and fertility benefits to females with differing mating history. Copulation per se was found to decrease the longevity of males but not that of females. However, when females were allowed to lay eggs, females that mated died earlier than virgin females, indicating costs of egg production and/or oviposition. Thus, although longevity costs of copulation are higher for males, reproduction is nevertheless costly for females. We also found no differences in fecundity or fertility relative to female mating history. Results suggest that polyandry may be driven by minor costs rather than by major benefits in this species.     

The more the better – polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra)

Although classically thought to be rare, female polyandry is widespread and may entail significant fitness benefits. If females store sperm over extended periods of time, the consequences of polyandry will depend on the pattern of sperm storage, and some of the potential benefits of polyandry can only be realized if sperm from different males is mixed. Our study aimed to determine patterns and consequences of polyandry in an amphibian species, the fire salamander, under fully natural conditions. Fire salamanders are ideal study objects, because mating, fertilization and larval deposition are temporally decoupled, females store sperm for several months, and larvae are deposited in the order of fertilization. Based on 18 microsatellite loci, we conducted paternity analysis of 24 female‐offspring arrays with, in total, over 600 larvae fertilized under complete natural conditions. More than one‐third of females were polyandrous and up to four males were found as sires. Our data clearly show that sperm from multiple males is mixed in the female's spermatheca. Nevertheless, paternity is biased, and the most successful male sires on average 70% of the larvae, suggesting a ‘topping off’ mechanism with first‐male precedence. Female reproductive success increased with the number of sires, most probably because multiple mating ensured high fertilization success. In contrast, offspring number was unaffected by female condition and genetic characteristics, but surprisingly, it increased with the degree of genetic relatedness between females and their sires. Sires of polyandrous females tended to be genetically similar to each other, indicating a role for active female choice.     

Relatedness Does not Affect Competitive Behavior of Rival Males or Offspring Growth in Multiply Sired Litters of Bank Voles (Myodes glareolus)

Kin selection operates through the fitness of an organism's relatives. In the polyandry context, kin selection may be observable on the one hand in competition between rival males and, on the other hand, in competition between litter mates. Sperm competition theory predicts that males should invest less into mating when competing for fertilizations against a close relative as compared to an unrelated male. We tested this hypothesis with bank voles (Myodes glareolus) by mating each focal male to two females: one of which had previously mated with a full sibling of the focal male and the other one with a male unrelated to the focal male. However, we found no effect of rival male relatedness on mating behavior or proportion of offspring sired by the 2nd male to mate. Possibly, the probability of successive mating of related males with the same female is too low in natural bank vole populations for selection to have fine‐tuned mating behavior in relation to rival male relatedness. Further, polyandry often results in litters sired by multiple males. Litter mates of such litters have a reduced relatedness and are thus expected to be less cooperative during gestation and lactation, which may impair growth. Following double matings with either two full‐sibling males or two unrelated males, we compared offspring growth at birth and during lactation. Against our prediction, there was no difference in growth between litters sired either by two full‐sibling males or by two unrelated males. Either the conflict was not severe enough to be visible with our sample size (N = 16) or it may have been resolved by maternal control of offspring provisioning.     

Repeated mating with the same male increases female longevity and fecundity in a polyandrous leaf beetle Galerucella birmanica (Coleoptera: Chrysomelidae)

Female multiple mating (polyandry) is widespread across Insecta, even if mating can be costly to females. To explain the evolution and maintenance of polyandry, several hypotheses, mainly focusing on the material (direct) and/or the genetic (indirect) benefits, have been proposed and empirically tested in many species. Considering only the direct benefits, repeatedly‐mated females are expected to exhibit the same fitness as multiply‐mated females under the same mating frequency. In the present study, we compare the fitness of females received monandrous repeated mating (MM) and polyandrous multiple mating (PM) in a polyandrous leaf beetle Galerucella birmanica and assess female mate preference with regard to polyandry or monandry. Our data indicate that the longevity and the egg‐laying duration of MM females are significantly longer than that of PM females. MM females produce significantly more hatched eggs than PM females over their lifetime under the same mating frequency, which results from the high hatching rate of eggs produced by MM females. PM females mated with novel virgin males in the second mating suffer decreased longevity and lifetime fecundity compared with PM females mated with novel mated males in the second mating. Once‐mated females are more likely to re‐mate with familiar males than novel males. By contrast to expectations, the results of the present study suggest that repeated mating provides females with more direct benefits than multiple mating in G. birmanica, and females prefer to re‐mate with familiar males. The possible causes of this finding are discussed.     

Ejaculate size, second male size, and moderate polyandry increase female fecundity in a seed beetle

Several hypotheses have been proposed to explain the evolutionof polyandry in species that provide nuptial gifts. When nuptialgifts are in the form of nutritional elements in the ejaculateand ejaculate size is correlated with male body size, femalescan accrue both direct (nutritional) and indirect (genetic)benefits from multiple mating. We examined remating decisionsin females of the seed beetle Stator limbatus and, using pathanalysis, examined the effects of male body size on the sizeof his ejaculate, the amount of ejaculate that was successfullytransferred to females, and the overall effect of these variableson female fecundity. Larger males produced larger ejaculatesand consequently transferred a larger ejaculate to females,but the effects on female fecundity differed between the females'first and second mates. Both larger first and second males wereable to transfer more of their ejaculate to females than weresmaller males. Both the total amount of ejaculate transferredby these males and polyandry (number of matings) were positivelycorrelated to female fecundity independently of each other.However, larger second males were more successful at stimulatingfemale fecundity independently of how much ejaculate they transferred.We also provide evidence that females are choosy during theirsecond mating opportunity. Both female choosiness and higherfemale investment after mating with larger second males suggestthat females may benefit from both direct and indirect effectsfrom multiple mating. We also conclude that male body size isunder both directional fecundity selection and directional sexualselection.     

Polyandry enhances offspring viability with survival costs to mothers only when mating exclusively with virgin males in Drosophila melanogaster

A prominent hypothesis for polyandry says that male–male competitive drivers induce males to coerce already‐mated females to copulate, suggesting that females are more likely to be harassed in the presence of multiple males. This early sociobiological idea of male competitive drive seemed to explain why sperm‐storing females mate multiply. Here, we describe an experiment eliminating all opportunities for male–male behavioral competition, while varying females’ opportunities to mate or not with the same male many times, or with many other males only one time each. We limited each female subject's exposure to no more than one male per day over her entire lifespan starting at the age at which copulations usually commence. We tested a priori predictions about relative lifespan and daily components of RS of female Drosophila melanogaster in experimental social situations producing lifelong virgins, once‐mated females, lifelong monogamous, and lifelong polyandrous females, using a matched‐treatments design. Results included that (1) a single copulation enhanced female survival compared to survival of lifelong virgins, (2) multiple copulations enhanced the number of offspring for both monogamous and polyandrous females, (3) compared to females in lifelong monogamy, polyandrous females paired daily with a novel, age‐matched experienced male produced offspring of enhanced viability, and (4) female survival was unchallenged when monogamous and polyandrous females could re‐mate with age‐ and experienced‐matched males. (5) Polyandrous females daily paired with novel virgin males had significantly reduced lifespans compared to polyandrous females with novel, age‐matched, and experienced males. (6) Polyandrous mating enhanced offspring viability and thereby weakened support for the random mating hypothesis for female multiple mating. Analyzes of nonequivalence of variances revealed opportunities for within‐sex selection among females. Results support the idea that females able to avoid constraints on their behavior from simultaneous exposure to multiple males can affect both RS and survival of females and offspring.     

Males Benefit from Mating with Outbred Females in Drosophila littoralis: Male Choice for Female Genetic Quality?

The evolution and expression of mate choice behaviour in either sex depends on the sex‐specific combination of mating costs, benefits of choice and constraints on choice. If the benefits of choice are larger for one sex, we would expect that sex to be choosier, assuming that the mating costs and constraints on choice are equal between sexes. Because deliberate inbreeding is a powerful genetic method for experimental manipulation of the quality of study organisms, we tested the effects of both male and female inbreeding on egg and offspring production in Drosophila littoralis. Female inbreeding significantly reduced offspring production (mostly due to lower egg‐to‐adult viability), whereas male inbreeding did not affect offspring production (despite a slight effect of paternal inbreeding on egg‐to‐adult viability). As inbreeding depressed female quality more than male quality, the benefits of mate choice were larger for males than for females. In mate choice experiments, inbreeding did not affect male mating success (measured as a probability to be accepted as a mate in a large group), suggesting that females did not discriminate among inbred and outbred males. In contrast, female mating success was affected by inbreeding, with outbred females having higher mating success than inbred females. This result was not explained by lower activity of inbred females. Our results show that D. littoralis males benefit from mating with outbred females of high genetic quality and suggest adaptive male mate choice for female genetic quality in this species. Thus, patterns of mating success in mate choice trials mirrored the benefits of choice: the sex that benefited more from choice (i.e. males) was more choosy.     

鸟类婚配制度的生态学分类

在Ｅmlen和Ｏring鸟类婚配制度生态学分类系统的基础上,根据近年来鸟类行为生态学研究的成果,对鸟类的婚配制度进行了补充分类,并强调了应以进化稳定策略的观念来认识乌类的婚配制度。补充的鸟类婚配制度生态型包括：合作型一雄一雌制（cooperative monogamy)、临界型一雄一雌制（critical monogamy)、保卫雌性型一雄一雌制（female defense mognogamy)、从领域型一雄多雌制（poly-terri-tory polygyny)和社群繁殖制。合作型一雄一雌制的鸟 类雌雄个体爱力合作才保证繁殖的成功;临界型一悲欢离合一雌制鸟类雌雄个体都有多配倾向,但迫于生态压力必须共同抚育后代才能繁殖成功;保卫雌性型一雄一雌制的鸟 类通过保卫一个雌鸟不被其它雄鸟占有而保证繁殖成功,多领域型一雄多雌制的雄鸟通过占有多个领域而多个雌鸟交配;社群繁殖制的鸟 类由三个以上个体参与工部分参与繁殖,所有个体共同抚育一批后代,现有的鸟类婚配制度可以归为一雄一雌制（monogamy)、一雄多雌繁殖,所有个体共同抚育一批后代。现有的鸟类婚配制度可以归为一雄一雌制(polygyny)、一雌多雄制（polyandry)快速多窝型多配制（rapid-multiple-clutch polygamy)和社群繁殖制（social breeing systen）五大类型。     

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.     

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.