The significance of multiple mating in the social wasp Vespula maculifrons

The evolution of the complex societies displayed by social insects depended partly on high relatedness among interacting group members. Therefore, behaviors that depress group relatedness, such as multiple mating by reproductive females (polyandry), are unexpected in social insects. Nevertheless, the queens of several social insect species mate multiply, suggesting that polyandry provides some benefits that counteract the costs. However, few studies have obtained evidence for links between rates of polyandry and fitness in naturally occurring social insect populations. We investigated if polyandry was beneficial in the social wasp Vespula maculifrons. We used genetic markers to estimate queen mate number in V. maculifrons colonies and assessed colony fitness by counting the number of cells that colonies produced. Our results indicated that queen mate number was directly, strongly, and significantly correlated with the number of queen cells produced by colonies. Because V. maculifrons queens are necessarily reared in queen cells, our results demonstrate that high levels of polyandry are associated with colonies capable of producing many new queens. These data are consistent with the explanation that polyandry is adaptive in V. maculifrons because it provides a fitness advantage to queens. Our research may provide a rare example of an association between polyandry and fitness in a natural social insect population and help explain why queens in this taxon mate multiply.     

Varying Ecological Quality Influences the Probability of Polyandry in White-handed Gibbons (Hylobates lar) in Thailand

Although members of the family Hylobatidae are known to be monogamous, adult white-handed gibbons ( Hylobates lar ) at Khao Yai National Park, Thailand, also show multimale groups and polyandry. A need for more than one male to successfully raise offspring cannot explain the occurrence of polyandry in these territorial primates, because direct paternal care is absent in this species. We hypothesize that polyandry is primarily related to costs/benefits for males of cooperatively defending a female and/or resources; our prediction was that polyandry would become more frequent with increasing costs of female/resource defense. We measured the ecological quality of seven gibbon home ranges over a 3-yr period (2001–2003) to investigate how resource availability affected the probability of polyandry, and found a significant negative relationship between home range quality and home range size. Larger home ranges were of lower quality. As predicted, groups living on larger, poorer home ranges also experienced longer periods of polyandry. In forest areas of comparatively low quality, acquiring and maintaining a large home range that includes enough resources for a female to reproduce steadily may surpass a single male's capacity. Our model of cooperative male polyandry was supported by preliminary data of shared territorial defense and access to the female. However, interaction proportions were strongly skewed, and female's primary male partners monopolized grooming and mating. Nevertheless, a primary male on a large territory may benefit from the presence of a secondary male with aid in territorial/female defense, whereas a secondary male may gain by avoiding high dispersal costs.     

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.     

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.     

Mating frequency and reproductive success in an income breeding moth,Mnesampela privata

The frequency of mating in insects is often an important determinant of female reproductive output and male sperm competition. In Lepidoptera that provide male nutrients to the female when mating, it is hypothesized that polyandry may be more prevalent. This is thought to be especially so among species described as income breeders; that is, in species who do not derive all their nutrients for reproductive output entirely from the resources obtained during the larval stage. We selected the geometrid moth, Mnesampela privata (Guenée) (Lepidoptera: Geometridae), to examine this hypothesis further. We found this species was best characterized as an income breeder with female weight on emergence positively correlated with total egg load but not with the number of eggs laid. Further, in accord with income breeders, females emerged with a partially developed egg load and lifetime fecundity was positively correlated with the number of oviposition days. However, in the laboratory we found that incidence of repeated matings or polyandry was rare. When moths were paired singly over their lifetime, only 4% of mated females multiple mated. When females were paired with three males concurrently, female mating success increased from 60 to 81% with multiple mating among mated females increasing to just 15%. Dissection of wild caught M. privata found that polyandry levels were also low with a maximum of 16.4% of females collected at any one time being multiple mated. In accord with theory, mating significantly increased the longevity of females, but not of males, suggesting that females acquire essential resources from male ejaculates. Despite this, multiple mated females showed a trend toward decreasing rather than increasing female reproductive output. Spermatophore size, measured on death of the female, was not correlated with male or female forewing length but was negatively correlated with the number of fertile eggs laid and female longevity. Smaller spermatophore width may be related to uptake of more nutrients by the female from a spermatophore. We discuss our findings in relation to income breeding and its relationship to polyandry in Lepidoptera.     

Polyandry in Bicyclus anynana Butterflies Results from Sexual Conflict over Mating

Although only one or just a few matings are considered sufficient to maximise a female's reproductive success, polyandry is a common mating system in insects and other animals. Female polyandry may either result from direct or indirect benefits of mating multiply, or from male harassment and thus sexual conflict over mating. Here, we test whether the latter is involved in determining female mating frequency in the butterfly Bicyclus anynana. We used a full‐factorial design with three different sex ratios and densities each, resulting in a total of nine treatment groups. Sex ratio but not density affected female mating frequency, which increased with an increasingly male‐biased sex ratio. Our results thus suggest that female polyandry in B. anynana results from sexual conflict, although females seem to be able to reject courting males at least to some extent. Therefore, polyandry in this species may occur in the first place from convenience, as the costs of resisting male harassment may be higher than mating repeatedly.     

Female polyandry and size‐assortative mating in isolated local populations of the Japanese common toad Bufo japonicus

In anurans, female polyandry under male harassment is distributed across taxa because of external aquatic fertilization. According to the sexual selection theory, male–male competition for access to females is affected by the operational sex ratio (OSR) and population density. The Japanese common toad, Bufo japonicus, is widespread in mainland Japan, and like the European common toad, B. bufo, it engages in explosive breeding. In this study, we observed the breeding behaviour of B. japonicus in isolated local populations for over four years in two breeding ponds with different population sizes and densities: large‐low (L‐pond) and small‐high (S‐pond). We analysed the relative polyandry ratio in egg clutches laid by females and estimated the size‐assortative mating pattern to be an indicator of male–male competition in the two ponds. Both ponds tended to exhibit a size‐assortative mating pattern; however, the frequency of polyandry was different in the two ponds (L‐pond = 20% and S‐pond = 90%). Our results showed that polyandry could occur without multiple amplexus with a high population density, i.e. eggs were often fertilized by free‐swimming sperm in the small shallow pond. We propose that high female polyandry ratios without continuous male harassment are generated because of a male‐biased OSR and a high population density in the small pond. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 236–242.     

Demographic factor affecting the fitness of polyandry for human males: A mathematical model and computer simulation

Polyandry has occurred rarely among humans; and has almost always consisted of brothers sharing a wife. The reduced opportunity for fertilization of females that occurs in polyandry would appear to make it a maladaptive mating system for human males. Previous evolutionary studies of human polyandry have suggested that kin selection may play a role in maintaining polyandry in some populations. A mathematical model for determining the fitness of polyandry for males is presented, and a simple deterministic analytic solution is derived. The model indicates that for polyandry to be an adaptive alternative to monogamy, the number of surviving offspring must be greater than the number of surviving offspring under monogamy times the number of males sharing a wife. This model exists in the literature. The unrealistic assumptions made in deriving this simple equation are revealed. An alternative stochastic computer simulation model is presented. The reproductive life history of a set of brothers is simulated under different demographic conditions, using data from polyandrous societies to estimate probabilities of fitness-related events. Under the assumption of equality of values of demographic variables for polyandry and monogamy, polyandry achieved or exceeded fitness parity with monogamy one third of the time. This contrasts with the prediction of the deterministic model stating that polyandry will never be an adaptive alternative to monogamy when fitness-related parameters are equal. The conditions improving fitness expectations for polyandry are conditions where genetic replication is decreased, i.e., with fewer brothers, high female sterility, decreased offspring survival, and decreased female fertility. Also, increased age difference between brothers enhances the fitness of polyandry. Genetic relatedness between brothers did not significantly affect the fitness of polyandry; therefore the kin selection hypothesis does not receive support. To a certain degree, these conditions exist for polyandrous populations in the Himalayas. Multivariate statistical analyses of simulation results revealed that most of the effects of these demographic factors could be accounted for by their association with increased probability of household extinction under monogamy and increased number of years of reproductive monogamy within polyandry. Although conditions favoring polyandry could be specified, analysis of the correlation between adaptiveness of polyandry and amount of genetic replication revealed that the demographic conditions favoring polyandry also lead to family extinction. Deficiencies in the model are discussed. It is suggested that future studies identify the advantages polyandry may have over monogamy in the values of demographic variables (e.g., increased offspring survival, increased extramarital reproduction), and take a multigenerational approach.     

Selfish genetic elements and sexual selection: their impact on male fertility

Females of many species mate with more than one male (polyandry), yet the adaptive significance of polyandry is poorly understood. One hypothesis to explain the widespread occurrence of multiple mating is that it may allow females to utilize post-copulatory mechanisms to reduce the risk of fertilizing their eggs with sperm from incompatible males. Selfish genetic elements (SGEs) are ubiquitous in eukaryotes, frequent sources of reproductive incompatibilities, and associated with fitness costs. However, their impact on sexual selection is largely unexplored. In this review we examine the link between SGEs, male fertility and sperm competitive ability. We show there is widespread evidence that SGEs are associated with reduced fertility in both animals and plants, and present some recent data showing that males carrying SGEs have reduced paternity in sperm competition. We also discuss possible reasons why male gametes are particularly vulnerable to the selfish actions of SGEs. The widespread reduction in male fertility caused by SGEs implies polyandry may be a successful female strategy to bias paternity against SGE-carrying males.     

Selfish genetic elements and sexual selection: their impact on male fertility

Females of many species mate with more than one male (polyandry), yet the adaptive significance of polyandry is poorly understood. One hypothesis to explain the widespread occurrence of multiple mating is that it may allow females to utilize post-copulatory mechanisms to reduce the risk of fertilizing their eggs with sperm from incompatible males. Selfish genetic elements (SGEs) are ubiquitous in eukaryotes, frequent sources of reproductive incompatibilities, and associated with fitness costs. However, their impact on sexual selection is largely unexplored. In this review we examine the link between SGEs, male fertility and sperm competitive ability. We show there is widespread evidence that SGEs are associated with reduced fertility in both animals and plants, and present some recent data showing that males carrying SGEs have reduced paternity in sperm competition. We also discuss possible reasons why male gametes are particularly vulnerable to the selfish actions of SGEs. The widespread reduction in male fertility caused by SGEs implies polyandry may be a successful female strategy to bias paternity against SGE-carrying males.     

Monandry and polyandry as alternative lifestyles in a butterfly

Butterflies show considerable variability in female mating frequency, ranging from monandrous species to females mating several timesin their lifetime. Degree of polyandry also varies within species,with some females only mating once and others mating multiply.Previous studies have shown that one reason for female multiplemating is to obtain nutritious male donations that both increasethe longevity of females and result in higher lifetime fecundity.Despite the presence of male nutrient donations, some femalesof the green-veined white butterfly (Pieridae: Pieris napi)never mate more than once. In this study, we examined thisapparent paradox. We assessed to what degree polyandry is undergenetic control by a full-sib analysis, and we also estimatedthe broad sense heritability of female lifetime fecundity in singly mated females. Both polyandry and lifetime fecundityhave a genetic component. However, degree of polyandry appearsto be traded off against reduced longevity when denied theopportunity to mate more than once. It is possible that femaleP. napi display different reproductive strategies, with somefemales relying on male donations to realize their potentialfecundity and others relying on their own resources for egg production. In nature, polyandrous females may be preventedfrom mating multiply due to unfavorable weather. We discussthe possibility that the trade-off between degree of polyandryand life span when singly mated may affect the maintenanceof genetic variability in female mating frequency in this species.Possible reasons for these different reproductive strategiesare discussed.     

The unexpected genetic mating system of the red‐backed toadlet (Pseudophryne coriacea): A species with prolonged terrestrial breeding and cryptic reproductive behaviour

Molecular technologies have revolutionized our classification of animal mating systems, yet we still know very little about the genetic mating systems of many vertebrate groups. It is widely believed that anuran amphibians have the highest reproductive diversity of all vertebrates, yet genetic mating systems have been studied in <1% of all described species. Here, we use single nucleotide polymorphisms to quantify the genetic mating system of the terrestrial breeding red‐backed toadlet Pseudophryne coriacea. In this species, breeding is prolonged (approximately 5 months), and males construct subterranean nests in which females deposit eggs. We predicted that females would display extreme sequential polyandry because this mating system has been reported in a closely related species (P. bibronii). Parentage analysis revealed that mating success was heavily skewed towards a subset of males (30.6% of potential sires) and that nearly all females (92.6%) mated with one male. In a high percentage of occupied nests (37.1%), the resident male was not the genetic sire, and very few nests (4.3%) contained clutches with multiple paternity. Unexpectedly, these results show that sequential polyandry is rare. They also show that there is a high frequency of nest takeover and extreme competition between males for nest sites, but that males rarely sneak matings. Genetic analysis also revealed introgressive hybridization between P. coriacea and the red‐crowned toadlet (Pseudophryne australis). Our study demonstrates a high level of mating system complexity, and it shows that closely related anurans can vary dramatically in their genetic mating system.     

Is polyandry a common event among wild populations of the pest Ceratitis capitata?

In many insect species, females can mate more than once and store sperm from more than one male. An assessment and understanding of polyandry in the field can be important for pest species with a high colonization potential, such as the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), which is also highly polyphagous and among the most destructive agricultural insects. The use of polymorphic microsatellite markers, combined with different statistical approaches, provides evidence that polyandry occurs in two C. capitata natural populations, one population from the Greek island of Chios and one population from Rehovot, in Israel. The observed different level of polyandry is discussed in relation to the genetic diversity, seasonality, and demography of the two populations. When polyandry is present, paternity analysis also indicates that one male, presumably the last, tends to sire most of the progeny. Polyandry and paternity skew may have important implications for the evolution of the species, in terms of maintenance of the genetic variability. Moreover, these aspects of the mating behavior, i.e., remating frequency and paternity skew, may locally affect the sterile insect technique, the most commonly applied control strategy against C. capitata.     

The incidence and selection of multiple mating in plants

Mating with more than one pollen donor, or polyandry, is common in land plants. In flowering plants, polyandry occurs when the pollen from different potential sires is distributed among the fruits of a single individual, or when pollen from more than one donor is deposited on the same stigma. Because polyandry typically leads to multiple paternity among or within fruits, it can be indirectly inferred on the basis of paternity analysis using molecular markers. A review of the literature indicates that polyandry is probably ubiquitous in plants except those that habitually self-fertilize, or that disperse their pollen in pollen packages, such as polyads or pollinia. Multiple mating may increase plants'' female component by alleviating pollen limitation or by promoting competition among pollen grains from different potential sires. Accordingly, a number of traits have evolved that should promote polyandry at the flower level from the female''s point of view, e.g. the prolongation of stigma receptivity or increases in stigma size. However, many floral traits, such as attractiveness, the physical manipulation of pollinators and pollen-dispensing mechanisms that lead to polyandrous pollination, have probably evolved in response to selection to promote male siring success in general, so that polyandry might often best be seen as a by-product of selection to enhance outcross siring success. In this sense, polyandry in plants is similar to geitonogamy (selfing caused by pollen transfer among flowers of the same plant), because both polyandry and geitonogamy probably result from selection to promote outcross siring success, although geitonogamy is almost always deleterious while polyandry in plants will seldom be so.     

Status and Reproduction in Humans: New Evidence for the Validity of Evolutionary Explanations on Basis of a University Sample

A strong positive relationship between reproductive success (offspring count) and status (position in the institutional hierarchy) is demonstrated in a contemporary sample of male university employees (n = 2693). Male academics in leading positions have more children than do other male employees. In female university employees (n = 2073), a negative relationship between status and reproductive success was found, but only if childless women were included in the analysis. Although a positive relationship between male status and offspring count has been predicted by evolutionary theory and was found in animal species and ‘traditional’ human societies, in modern societies most of the studies found no or even a negative relationship between status and reproductive success in males. We suggest that status may be a more important dimension for particular subsamples of modern society than for samples representing entire societies, so that associations might actually differ among subsamples. We suggest that analyses on a small and rather uniform level using modern large‐scale hierarchical organizations (such as universities) are candidates for the investigation of appropriate ‘society subsets’. Our results may stress the importance of evolutionary predictions and may be of relevance for theoretical and empirical considerations at the levels of economics and administration.     

The consequences of polyandry for population viability,extinction risk and conservation

Polyandry, by elevating sexual conflict and selecting for reduced male care relative to monandry, may exacerbate the cost of sex and thereby seriously impact population fitness. On the other hand, polyandry has a number of possible population-level benefits over monandry, such as increased sexual selection leading to faster adaptation and a reduced mutation load. Here, we review existing information on how female fitness evolves under polyandry and how this influences population dynamics. In balance, it is far from clear whether polyandry has a net positive or negative effect on female fitness, but we also stress that its effects on individuals may not have visible demographic consequences. In populations that produce many more offspring than can possibly survive and breed, offspring gained or lost as a result of polyandry may not affect population size. Such ecological ‘masking’ of changes in population fitness could hide a response that only manifests under adverse environmental conditions (e.g. anthropogenic change). Surprisingly few studies have attempted to link mating system variation to population dynamics, and in general we urge researchers to consider the ecological consequences of evolutionary processes.     

Honey Bee Colonies Headed by Hyperpolyandrous Queens Have Improved Brood Rearing Efficiency and Lower Infestation Rates of Parasitic Varroa Mites

A honey bee queen mates on wing with an average of 12 males and stores their sperm to produce progeny of mixed paternity. The degree of a queen’s polyandry is positively associated with measures of her colony’s fitness, and observed distributions of mating number are evolutionary optima balancing risks of mating flights against benefits to the colony. Effective mating numbers as high as 40 have been documented, begging the question of the upper bounds of this behavior that can be expected to confer colony benefit. In this study we used instrumental insemination to create three classes of queens with exaggerated range of polyandry– 15, 30, or 60 drones. Colonies headed by queens inseminated with 30 or 60 drones produced more brood per bee and had a lower proportion of samples positive for Varroa destructor mites than colonies whose queens were inseminated with 15 drones, suggesting benefits of polyandry at rates higher than those normally obtaining in nature. Our results are consistent with two hypotheses that posit conditions that reward such high expressions of polyandry: (1) a queen may mate with many males in order to promote beneficial non-additive genetic interactions among subfamilies, and (2) a queen may mate with many males in order to capture a large number of rare alleles that regulate resistance to pathogens and parasites in a breeding population. Our results are unique for identifying the highest levels of polyandry yet detected that confer colony-level benefit and for showing a benefit of polyandry in particular toward the parasitic mite V. destructor.     

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.     

DO WOLBACHIA‐ASSOCIATED INCOMPATIBILITIES PROMOTE POLYANDRY?

The genetic incompatibility avoidance hypothesis as an explanation for the polyandrous mating strategies (mating with more than one male) of females of many species has received significant attention in recent years. It has received support from both empirical studies and a meta-analysis, which concludes that polyandrous females enjoy increased reproductive success through improved offspring viability relative to monandrous females. In this study we investigate whether polyandrous female Drosophila simulans improve their fitness relative to monandrous females in the face of severe Wolbachia-associated reproductive incompatibilities. We use the results of this study to develop models that test the predictions that Wolbachia should promote polyandry, and that polyandry itself may constrain the spread of Wolbachia. Uniquely, our models allow biologically relevant rates of incompatibility to coevolve with a polyandry modifier allele, which allows us to evaluate the fate of the modifier and that of Wolbachia. Our empirical results reveal that polyandrous females significantly reduce the reproductive costs of Wolbachia, owing to infected males being poor sperm competitors. The models show that this disadvantage in sperm competition can inhibit or prevent the invasion of Wolbachia. However, despite the increased reproductive success obtained by polyandrous females, the spread of a polyandry modifier allele is constrained by any costs that might be associated with polyandry and the low frequency of incompatible matings when Wolbachia has reached a stable equilibrium. Therefore, although incompatibility avoidance may be a benefit of polyandry, our findings do not support the hypothesis that genetic incompatibilities caused by Wolbachia promote the evolution of polyandry.     

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.