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.     

Material and genetic benefits of female multiple mating and polyandry

The maintenance of female polyandry has traditionally been attributed to the material (direct) benefits derived from male mating resources (e.g. nuptial gifts) accrued by multiple mating. However, genetic (indirect) benefits offer a more robust explanation since only polyandrous, not monandrous, females may gain both material benefits from multiple mating and genetic benefits from multiple sires. Discriminating between material and genetic benefits is essential when addressing the mechanism by which polyandry is adaptively maintained, but are difficult to disentangle because they affect fitness in similar ways. To test the hypothesis that genetic benefits maintain polyandry, we compared four components of fitness (longevity, fecundity, hatching success and survivorship) between monandrous and polyandrous females in the ground cricket, Allonemobius socius. We discovered that females derived nongenetic benefits from mating multiply, in that the magnitude of the nuptial gift was positively associated with the number of eggs produced. However, polyandrous females had over a two-fold greater hatching success and a 43% greater offspring survivorship, leading to a significantly higher relative fitness than the monandrous strategy. These results were independent of the confounding effects of material benefits, implying that genetic contributions play a large role in the maintenance of polyandry and potentially in the antagonistic coevolutionary relationship between polyandry and male nuptial gifts. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

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

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

Male age affects female mating preference but not fitness in the monandrous moth Dendrolimus punctatus Walker (Lepidoptera: Lasiocampidae)

It is widely accepted that male age can influence female mating preference and subsequent fitness consequences in many polyandrous species, yet this is seldom investigated in monandrous species. In the present study, we use the monandrous pine moth Dendrolimus punctatus to examine the effects of male age on female mating preference and future reproductive potential. In multiple male trials, when permitted free mating from an aggregation consisting of virgin males aged 0 (young), 2 (middle-aged) and 4 (old) days, virgin females preferentially mate with young and middle-aged males, although mating latency and mating duration are independent of male age. In single male trials, when virgin females are randomly assigned single virgin males of known age, a negative correlation is found between mating success and male age in this species. However, we find that male age also has no effect on mating latency and mating duration. Further fitness analysis reveals that females do not receive benefits in terms of oviposition period, total egg production, average daily egg production, percentage of egg hatching, longevity, expected reproduction and relative expected reproduction from mating with young and middle-aged males compared with mating with old males. The results of the present study are the first demonstrate that females mated preferentially with younger males but gain no apparent fitness benefits in a monandrous moth species.     

Sperm competition,but not major histocompatibility divergence,drives differential fertilization success between alternative reproductive tactics in Chinook salmon

Post‐copulatory sexual selection processes, including sperm competition and cryptic female choice (CFC), can operate based on major histocompatibility (MH) genes. We investigated sperm competition between male alternative reproductive tactics [jack (sneaker) and hooknose (guard)] of Chinook salmon (Oncorhynchus tshawytscha). Using a full factorial design, we examined in vitro competitive fertilization success of paired jack and hooknose males at three time points after sperm activation (0, 15 and 60 s) to test for male competition, CFC and time effects on male fertilization success. We also examined egg‐mediated CFC at two MH genes by examining both the relationship between competitive fertilization success and MH divergence as well as inheritance patterns of MH alleles in resulting offspring. We found that jacks sired more offspring than hooknose males at 0 s post‐activation; however, jack fertilization success declined over time post‐activation, suggesting a trade‐off between sperm speed and longevity. Enhanced fertilization success of jacks (presumably via higher sperm quality) may serve to increase sneaker tactic competitiveness relative to dominant hooknose males. We also found evidence of egg‐mediated CFC (i.e. female × male interaction) influencing competitive fertilization success; however, CFC was not acting on the MH genes as we found no relationship between fertilization success and MH II β₁ or MH I α₁ divergence and we found no deviations from Mendelian inheritance of MH alleles in the offspring. Our study provides insight into evolutionary mechanisms influencing variation in male mating success within alternative reproductive tactics, thus underscoring different strategies that males can adopt to attain success.     

Large Numbers of Matings Give Female Field Crickets a Direct Benefit but not a Genetic Benefit

Female crickets can potentially gain both direct and indirect benefits from mating multiple times with different males. Most studies have only examined the effects of small numbers of matings, although female crickets are capable of mating many times. The goal of this paper is to examine the direct and indirect benefits of mating large numbers of times for female reproductive success. In a previous experiment, female Gryllus vocalis were found to gain diminishing direct benefits from mating large numbers of times. In this study I attempt to determine whether mating large numbers of times yields similar diminishing returns on female indirect benefits. Virgin female Gryllus vocalis crickets were assigned to mate five, ten or 15 times with either the same or different males. Females that mated more times gained direct benefits in terms of laying more eggs and more fertilized eggs. Females that mated with different males rather than mating repeatedly with the same male did not have higher offspring hatching success, a result that is contrary to other published results comparing female reproductive success with repeated versus different partners. These results suggest that females that mate large numbers of times fail to gain additional genetic benefits from doing so.     

Testing the viviparity-driven-conflict hypothesis: parent-offspring conflict and the evolution of reproductive isolation in a poeciliid fish

The evolution of viviparity increases the potential for genomic conflicts between mothers and offspring over the level of maternal investment. The viviparity-driven-conflict hypothesis predicts that such conflicts will drive the evolution of asymmetrical reproductive isolation between populations with divergent mating systems. We tested this hypothesis using crosses between populations of a poeciliid fish that differ in their level of polyandry. Our results support the prediction of an asymmetry in the rate of spontaneous abortion in reciprocal crosses, with the highest rate occurring in crosses between females from a relatively monandrous population and males from a relatively polyandrous population. The patterns of offspring size were not consistent with the pattern predicted by the viviparity-driven-conflict hypothesis: crosses between a monandrous female and a polyandrous male did not produce larger offspring than the reciprocal cross. This discrepancy was due to the presence of an effect of the maternal population on offspring size: polyandrous females produced larger offspring than monandrous females. In addition, offspring size was positively correlated with maternal size in crosses involving a polyandrous male. We discuss these results in light of models for intra- and intergenomic epistasis and the rapid origin of asymmetric reproductive isolation in viviparous taxa.     

Good genes and the maternal effects of polyandry on offspring reproductive success in the bulb mite

Genetic benefits are potentially the most robust explanation of the controversial issue of evolutionary maintenance of polyandry, but the unambiguous demonstration of such benefits has been hindered by the possibility of their confusion with maternal effects. Previous research has shown that polyandrous bulb mite females produce daughters with higher fecundity than monandrous females. Here, we investigate whether this effect arises because polyandrous females invest more in their offspring, or because their offspring inherit 'good genes' from their fathers. Females were mated with either one or four (different) males. However, by sterilizing three of the four males with ionizing radiation, we eliminated any chance of sexual selection (in the polyandrous treatment) so that any differences in the female mating regimes must have been owing to maternal effects. Polyandry had no significant effect on daughter fecundity, thus indicating that any previously documented effects must have been genetic. This was further supported by a significant association between fathers' offensive sperm-competitive ability and the fecundity of their daughters. The association with fathers' sperm defensive ability was not significant, and neither was the association between fathers' sperm competitiveness and sons' reproductive success. However, sons of polyandrous females had lower reproductive success than sons of monandrous females. This shows that the maternal effects of polyandry should be taken into account whenever its costs and benefits are being considered.     

Paternal body size affects reproductive success in laboratory-held zebrafish (<Emphasis Type="Italic">Danio rerio</Emphasis>)

Across many fish species, large females tend to exhibit higher individual reproductive success due to elevated fecundity and the provisioning of better conditioned eggs and offspring compared to small females. By contrast, effects of paternal body size on reproductive success are less well understood. We disentangled the maternal- and paternal-size dependent effects on reproductive output and early life history in zebrafish (Danio rerio). In the laboratory, females and males from four size categories (small, medium-sized, large and very large) were allowed to spawn freely in a full factorial design with 10 replicates per size combination. As expected, larger females produced more eggs and better conditioned offspring compared to smaller females. Male body size further contributed to zebrafish reproductive success: offspring sired by large males exhibited higher hatching probability and these offspring also hatched earlier and larger than offspring fertilized by small males. However, the largest males experienced lower mating success and received fewer eggs than males of the smaller size classes. While male body size substantially affected reproductive success in zebrafish, it remained unclear whether and to what degree direct paternal effects (e.g., related to sperm quality) or indirect paternal effects stemming from differential allocation patterns by females were the mechanism behind our findings. Answering this question constitutes an important future research topic.     

Effects of ovarian fluid and genetic differences on sperm performance and fertilization success of alternative reproductive tactics in Chinook salmon

In many species, sperm velocity affects variation in the outcome of male competitive fertilization success. In fishes, ovarian fluid (OF) released with the eggs can increase male sperm velocity and potentially facilitate cryptic female choice for males of specific phenotypes and/or genotypes. Therefore, to investigate the effect of OF on fertilization success, we measured sperm velocity and conducted in vitro competitive fertilizations with paired Chinook salmon (Oncorhynchus tshawytscha) males representing two alternative reproductive tactics, jacks (small sneaker males) and hooknoses (large guarding males), in the presence of river water alone and OF mixed with river water. To determine the effect of genetic differences on fertilization success, we genotyped fish at neutral (microsatellites) and functional [major histocompatibility complex (MHC) II ß1] markers. We found that when sperm were competed in river water, jacks sired significantly more offspring than hooknoses; however, in OF, there was no difference in paternity between the tactics. Sperm velocity was significantly correlated with paternity success in river water, but not in ovarian fluid. Paternity success in OF, but not in river water alone, was correlated with genetic relatedness between male and female, where males that were less related to the female attained greater paternity. We found no relationship between MHC II ß1 divergence between mates and paternity success in water or OF. Our results indicate that OF can influence the outcome of sperm competition in Chinook salmon, where OF provides both male tactics with fertilization opportunities, which may in part explain what maintains both tactics in nature.     

Benefits of polyandry in Parthenium beetle,Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae)

The influence of polyandry on the reproductive performance of females and on offspring fitness in Zygogramma bicolorata Pallister was investigated using four experimental treatments, viz. (A) monandrous, limited mating, (B) monandrous, unlimited mating, (C) polyandrous, no-choice limited mating, and (D) polyandrous, mate choice unlimited mating. Polyandrous females had higher reproductive performance than monandrous ones. Monandrous females subjected to unlimited matings had higher egg viability than those subjected to limited matings, but fecundity did not differ significantly. In polyandrous females, the freedom to choose mates did not affect reproductive performance. However, offspring of polyandrous females allowed mate choice developed fastest and had the highest survival at 25, 27, and 30 °C. Thus, polyandry in Z. bicolorata appears to provide both direct (material) and indirect (genetic) benefits resulting in better reproductive performance and increased adaptability of the offspring to counter environmental stresses. The present study not only adds to the knowledge of reproductive biology of Z. bicolorata but it could also be of economic value as it may help in the mass rearing of Z. bicolorata and in the management of Parthenium hysterophorus.     

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.     

Life history tradeoffs in relation to the degree of polyandry and developmental pathway in Pieris napi (Lepidoptera, Pieridae)

Pieris napi females have different heritable reproductive tactics. Polyandrous females have higher lifetime fecundity, whereas monandrous ones start to reproduce at a faster rate. Butterfly larvae are time‐constrained in seasonal environments. Thus, polyandry is expected to be associated with fast juvenile development, which may result in biased mortality due to physiological costs. We compared how females with varying degrees of polyandry allocate between duration of larval period and achievable size in directly developing and over‐wintering generations. Offspring survival and growth were monitored under a high density and low quality diet. Polyandrous females developed at a faster rate than monandrous ones, regardless of developmental pathway. The growth rate of female offspring correlated with their mothers’ degree of polyandry, which underpins polyandry and monandry as distinct strategies with life history differences reaching beyond mating frequency. The high growth rate of polyandrous females resulted in a short larval period among directly developing females, and in large size within an over‐wintering cohort. A change in either the duration of the larval period or pupal mass had no significant effect on the other, emphasising that growth rate is not necessarily a simple outcome of the tradeoff between development time and size at maturity. The correlation between the degree of polyandry and juvenile growth rate diminished when larvae were exposed to environmental stress, which offers an explanation why juvenile mortality was decoupled from mating tactic. We conclude that polyandry is a strategy that allows larvae to utilise optimal conditions in a more effective way than monandry. As a consequence, polyandrous females either achieve larger size or they mature faster. This gives them a double advantage over monandrous ones within an over‐wintering generation or diminishes the effects of asynchronous hatching of offspring within a directly developing generation. Possible costs of high growth rate are discussed.     

Do female black field crickets Teleogryllus commodus benefit from polyandry?

Female insects that mate multiply tend to have increased lifetime fitness, apparently because of greater access to male-derived resources (e.g. sperm, nuptial gifts) that elevate fertility/fecundity. Experiments that standardize the number of matings per female also show that polyandry can improve aspects of offspring performance, most notably early embryo survival (egg hatching success). This improvement is widely attributed to genetic benefits which would arise if polyandrous females skew paternity to produce fitter offspring. In two separate experiments with field crickets (Teleogryllus commodus) polyandrous females (two, three or four mates) did not have higher egg hatching success than monandrous females (effect sizes: r = 0.03 and 0.08 for the respective experiments), which is consistent with our finding of no sire effect on hatching success. Polyandry also had no effect on post-hatching offspring survival. Polyandrous females' offspring took significantly longer to mature but their sons were not heavier and their daughters were actually significantly smaller than those of monandrous females. Finally, after controlling for relative male size, monandrous females' sons were more successful when directly competing for a mate.     

The mating systems of three species of minute pirate bug,Orius sauteri,O. minutus,and O. strigicollis

We compared the mating systems and genital morphology of three Orius species dominant in Japan: Orius sauteri (Poppius), Orius minutus (L.), and Orius strigicollis (Poppius) (Heteroptera: Anthocoridae). In all three species, the males were polygamous and could inseminate at least three females at a rate of one female per day. Compared to the other two species, the O. minutus males had a lower rate of success in three consecutive mating orders. The mated females laid the same number of eggs irrespective of mating sequence. Orius minutus and O. strigicollis females were found to be monandrous, and they re‐mated with another male only when the 1st mating failed. In contrast, O. sauteri females were polyandrous and accepted a 2nd male even when the 1st mating was successful. Multiple mating with a single male did not increase their fecundity, and it decreased the hatching success of eggs. Mating with multiple males did not affect the fecundity or hatching success. Our scanning electron microscopy observation suggested that the genitalia of O. minutus and O. strigicollis were more similar in shape. The similarities in mating system and morphology between O. minutus and O. strigicollis support a close phylogenetic relationship.     

Alternative tactics and individual reproductive success in natural associations of the burying beetle, Nicrophorus vespilloides

Alternative reproductive tactics can be maintained through differentevolutionary avenues. They can be genetically or stochasticallydetermined, in which case they must yield equal fitness, ortheir use can be conditional, in which case the fitness payoffof alternatives may differ. We attempted to assess the reproductivesuccess of alternative reproductive tactics employed by wildmale and female burying beetles in natural associations on carcassesplaced in the field. A beetle's reproductive tactic was definedby its potential involvement in care of larvae, and parentagewas assessed using oligolocus DNA fingerprinting of offspringand potential parents. Both in males and in females, alternativetactics yielded significantly different reproductive benefits:subordinate females (brood parasites) and males (satellite males)had considerably lower reproductive success than dominant oruncontested individuals. Joint breeding was too infrequent forstatistical inferences, generating intermediate offspring numbers.About 15% of offspring were sired by males not present on thecarcass, suggesting that mating away from reproductive resourcescan produce reproductive benefits to males. Our results, inconcert with the observation that beetles using one tactic canbe manipulated into employing the alternative, support the notionthat Nicrophorus vespilloides uses alternatives conditionally,opportunistically employing lower-benefit tactics when moreprofitable tactics are not available, or as additional "on-the-side"tactics to bolster reproductive success.     

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.     

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.     

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.     

Seasonal variation in male alternative reproductive tactics

Genetic parentage analyses reveal considerable diversity in alternative reproductive behaviours (e.g. sneaking) in many taxa. However, little is known about whether these behaviours vary seasonally and between populations. Here, we investigate seasonal variation in male reproductive behaviours in a population of two‐spotted gobies (Gobiusculus flavescens) in Norway. Male two‐spotted gobies guard nests, attract females and care for fertilized eggs. We collected clutches and nest‐guarding males early and late in the breeding season in artificial nests and used microsatellite markers to reconstruct parentage from a subset of offspring from each nest. We hypothesized that mating, reproductive success and sneaking should be more prevalent early in the breeding season when competition for mates among males is predicted to be higher. However, parentage analyses revealed similar values of mating, reproductive success and high frequencies of successful sneaking early (30% of nests) and late (27% of nests) in the season. We also found that multiple females with eggs in the same nest were fertilized by one or more sneaker males, indicating that some males in this population engage in a satellite strategy. We contrast our results to previous work that demonstrates low levels of cuckoldry in a population in Sweden. Our results demonstrate marked stability in both the genetic mating system and male alternative reproductive tactics over the breeding season. However, sneaking rates may vary geographically within a species, likely due to local selection influencing ecological factors encountered at different locations.