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.     

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.     

Polyandrous females found fitter populations

Multiple mating by females (polyandry) requires an evolutionary explanation, because it carries fitness costs in many species. When mated females disperse alone to a new habitat, their offspring may have no option but to mate with their siblings and incur inbreeding depression. However, some of the offspring of polyandrous females may only be half siblings, reducing inbreeding depression when isolated groups of siblings only have each other as mates. We investigated this putative benefit of polyandry over monandry by initiating multiple genetically isolated populations of Callosobruchus maculatus beetles, each founded by a single female, who received a complete ejaculate from either one or two males. The early generations had comparable fitness, but the F4 and F5 descendants of doubly inseminated females were more numerous and had higher egg‐to‐adult survival than the descendants of singly inseminated females. This fitness benefit was of similar magnitude whether beetles were reared on their standard food plant, or on a less favourable food source. Our results suggest that polyandrous females produce fitter descendants in inbred founder populations and therefore that polyandry may affect movement ecology and invasion biology.     

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.     

Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus

Polyandry, i.e. mating with multiple males within one reproductive event, is a common female mating strategy but its adaptive function is often unclear. We tested whether polyandrous females gain genetic benefits by comparing fitness traits of monandrous (mated twice with a single male) and polyandrous (mated twice with two different males) female bank voles Clethrionomys glareolus. We raised the offspring in the laboratory until adulthood and measured their body size, before releasing them to outdoor enclosures to overwinter. At the onset of the breeding season in the following spring, we found that offspring of polyandrous females performed significantly better at reproduction than those of monandrous females. This was mainly due to sons of polyandrous females producing significantly more offspring than those of monandrous females. No significant differences were found for offspring body mass or winter survival between the two treatments. Our results appear to provide evidence that bank vole females gain long-term benefits from polyandry.     

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.     

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.     

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.     

Females of the Cellar Spider Discriminate Against Previous Mates

Mate choice for novel partners should evolve when remating with males of varying genetic quality provides females with fitness‐enhancing benefits. We investigated sequential mate choice for same or novel mating partners in females of the cellar spider Pholcus phalangioides (Pholcidae) to understand what drives female remating in this system. Pholcus phalangioides females are moderately polyandrous and show reluctance to remating, but double‐mated females benefit from a higher oviposition probability compared to single‐mated females. We exposed mated females to either their former (same male) or a novel mating partner and assessed mating success together with courtship and copulatory behaviours in both sexes. We found clear evidence for mate discrimination: females experienced three‐fold higher remating probabilities with novel males, being more often aggressive towards former males and accepting novel males faster in the second than in the first mating trial. The preference for novel males suggests that remating is driven by benefits derived from multiple partners. The low remating rates and the strong last male sperm precedence in this system suggest that mating with novel partners that represent alternative genotypes may be a means for selecting against a former mate of lower quality.     

Sexual conflict over mating in a spider: increased fecundity does not compensate for the costs of polyandry

Female multiple mating (polyandry) is a widespread but costly behavior that remains poorly understood. Polyandry may arise when whatever benefits females accrue from multiple mating outweigh the costs, or males manipulate females against the females' best interests. In a polyandrous spider Stegodyphus lineatus females may mate with up to five males, but behave aggressively toward additional males after the first mating. Female aggressiveness may act to select for better quality males. Alternatively, females may try to avoid superfluous matings. To test these alternatives, we allocated females into single-mating (SM) and double-mating treatments. Double-mated females either accepted (DM) or rejected (RE) the second male. DM females laid more eggs, but did not produce more offspring than SM and RE females. Offspring of DM females were smaller at dispersal than offspring of SM and RE females. Also, nest failure was significantly more common in DM females. Paternal variables did not influence female reproductive success, whereas maternal body condition explained much of the variation. We show that polyandry is costly for females despite the production of larger clutches and suggest that multiple mating results from male manipulation of female remating behavior.     

Post-copulatory sexual selection and female fitness in Scathophaga stercoraria

Whether sexual selection increases or decreases female fitness is determined by the occurrence and relative importance of sexual-conflict processes and the ability of females to choose high-quality males. Experimentally enforced polyandry and monogamy have previously been shown to cause rapid evolution in the yellow dung fly Scathophaga stercoraria. Flies from polyandrous lines invested more in reproductive tissue, and this investment influenced paternity in sperm competition, but came at a cost to immune function. While some fitness consequences of enforced polyandry or monogamy have been examined when flies mate multiply, the consequences for female fitness when singly copulated remain unexplored. Under a good-genes scenario females from polyandrous lines should be of higher general quality and should outperform females from monogamous lines even with a single copulation. Under sexual conflict, costly adaptations will afford no advantages when females are allowed to mate only once. We investigate the lifetime reproductive success and longevity of females evolving under enforced monogamy or polyandry when mating once with males from these selection regimes. Females from polyandrous lines were found to have lower fitness than their monogamous counterparts when mating once. They died earlier and produced significantly fewer eggs and offspring. These results suggest that sexual conflict probably drove evolution under enforced polyandry as female fitness did not increase overall as expected with purely good-genes effects.     

Bet‐hedging as a mechanism for the evolution of polyandry,revisited

Females that mate with multiple males (polyandry) may reduce the risk that their eggs are fertilized by a single unsuitable male. About 25 years ago it was hypothesized that bet‐hedging could function as a mechanism favoring the evolution of polyandry, but this idea is controversial because theory indicates that bet‐hedging via polyandry can compensate the costs of mating only in small populations. Nevertheless, populations are often spatially structured, and even in the absence of spatial structure, mate‐choice opportunity can be limited to a few potential partners. We examined the effectiveness of bet‐hedging in such situations with simulations carried out under two scenarios: (1) intrinsic male quality, with offspring survival determined by male phenotype (male's ability to generate viable offspring), and (2) genetic incompatibility (offspring fitness determined nonadditively by parental genotypes). We find higher fixation probabilities for a polyandrous strategy compared to a monandrous strategy if complete reproductive failure due to male effects or parental incompatibility is pervasive in the population. Our results also indicate that bet‐hedging polyandry can delay the extinction of small demes. Our results underscore the potential for bet‐hedging to provide benefits to polyandrous females and have valuable implications for conservation biology.     

Conflict over multiple-partner mating between males and females of the polygynandrous common lizards

The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple-partner mating. This suggests that the population sex ratio may affect multiple-partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male-biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male-biased populations females suffered from reduced reproductive success compared to female-biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male-biased populations showed disproportionately more mating scars, indicating that polyandrous females of male-biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.     

Polyandry promotes enhanced offspring survival in decorated crickets

Although female multiple mating is ubiquitous in insects, its adaptive significance remains poorly understood. Benefits to multiple mating can accrue via direct material benefits, indirect genetic benefits, or both. We investigated the effects of multiple mating in the decorated cricket, Gryllodes sigillatus, by simultaneously varying the number of times that females mated and the number of different males with which they mated, measuring aspects of female fecundity and elements of offspring performance and viability. Multiple matings resulted in enhanced female fitness relative to single matings when females mated with different partners, but not when females mated repeatedly with the same male. Specifically, polyandrous females produced significantly more offspring surviving to reproductive maturity than did monogamous females mating once or mating repeatedly with the same male. These results suggest that the benefit females gain from multiple mating is influenced primarily by genetic and not material benefits.     

Bet hedging via multiple mating: A meta‐analysis

Polyandry has been hypothesized to allow females to “bet hedge” against mating only with unsuitable mates, reducing variance in offspring fitness between members of a polyandrous lineage relative to a single‐mating one. Theoretically, this reduction in fitness variance could select for polyandrous genotypes even when polyandry carries a direct cost, especially in small populations. However, this hypothesis is controversial and difficult to test empirically. Here, I apply a novel simulation model to 49 published empirical datasets, and quantify the potential selective advantage of multiple mating via reduced offspring fitness variance. For a wide range of assumptions, including those that most favor the evolution of bet hedging, I show that any fitness gains are meager. The variance in offspring quality caused by mate identity does not appear to be high enough for bet hedging to drive the evolution of polyandry.     

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。     

Age-specific mating strategies and reproductive senescence

While males gain obvious direct advantages from multiple mating, the reproductive capacity of females is more constrained. The reason why polyandry evolved in females is therefore open to many conjectures. One hypothesis postulates that females gain indirect benefits by increasing the probability of siring young from high quality males. To explore this hypothesis, we used the natural variation of the reproductive value that males and females undergo through age. The age-related variation of phenotypic performance might then induce variations in mating strategies in males and females. Using the common lizard (Lacerta vivipara) as our model system, we showed that reproductive immaturity and senescence created variability in both male and female reproductive success (including survival of offspring). Consistent with theory, males at their best-performing phenotype adopted a polygynous strategy. These males were of an intermediate age and they produced offspring of higher viability than younger and older males. In contrast, females at their best performing phenotype, also of an intermediate age, were less polyandrous than other less-performing females. Middle-aged females tended to mate with males of an intermediate age and produced litters with higher viability independently from their reproductive strategy. Males of an intermediate age enhanced their fitness by additional matings with young or old females. Young and old females increased their fitness by being more polyandrous. Polyandry therefore appears as means to seek for good males. A positive correlation between males and their partners' fitness disagree with the idea that polyandry is the result of a sexual conflict in this species.     

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.     

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.     

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.