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.     

Mating Frequency, Fecundity and Fertilization Success in the Hide Beetle, Dermestes Maculatus

While the immediate benefits accrued to females through multiple mating are well documented, the effect of sperm depletion for multiply mating males is rarely considered. We show that, in small mixed-sex laboratory aggregations, both male and female hide beetles, Dermestes maculatus (De Geer) mated multiply. There was considerable variation in the mating frequency of both sexes; however the skew in mating success was comparable for males and females. Several individuals that mated multiply also re-mated with a previous partner, but in a competitive environment no male copulated more than seven times. Mating success was unrelated to an individual's size, but males that had the most inter-sexual matings also engaged in the most intra-sexual mating attempts. In a second experiment, we show that, even in the absence of rivals, only a small number of males mated with all available virgin females. Moreover, even though males were mated twice to each female, males that copulated more than eight times failed to fertilize any eggs. We suggest that under natural conditions male hide beetles may refrain from mating either prior to, or at the point of, sperm depletion thereby reducing the selection pressure for females to discriminate against sperm depleted males. However, fecundity and fertilization success varied considerably across females and even those mating with sperm-replete males were unable to fertilize 100% of their egg batch. Thus, direct fertilization benefits accrued by females through mating more than once with the same male may play a key role in the maintenance of polyandry in this species.     

Increased hatching success as a direct benefit of polyandry in birds

Multiple mating by females is difficult to explain in primarily socially monogamous taxa such as birds because mating outside the pair bond often provides no obvious benefit to females. Although indirect selection is often invoked to explain the evolution of polyandry, current evidence suggests that selection on indirect benefits of mating is weak. Here, I consider a direct benefit of remating in birds: increased fertilization success. I test whether increased hatching success of a female's eggs is related to rates of extra-pair paternity (EPP), a proxy of polyandry, across 113 bird species. I use two statistical approaches, control for phylogenetic uncertainty, and assess the fit of competing evolutionary models. Results show there is indeed a positive relationship between rates of EPP and hatching success in birds. I propose that by mating with many males, females may increase their fertility. I end by discussing the biological rationale for this explanation, alternative interpretations of the results, and how this study furthers our understanding of polyandry and mating system evolution.     

What is driving male mate preference evolution in Jamaican field crickets?

Male mating preferences are often a neglected aspect of studies on sexual selection. Male mating preferences may evolve if they provide males with direct‐fitness benefits such as increased opportunity to fertilize more eggs or indirect‐fitness benefits such as enhanced offspring survival. We tested these ideas using Jamaican field crickets, Gryllus assimilis, previously shown to exhibit male mating preferences. We randomly mated males to either their preferred or non‐preferred potential mates and then asked whether mating treatment influenced egg oviposition or offspring viability. Preferred females were not significantly more fecund and did not produce more viable eggs or offspring than non‐preferred females. Male mate preferences were therefore inconsistent with both the direct‐ and indirect‐fitness benefits hypotheses under the conditions of our experiment. Our null results leave us with an open question about what is driving the evolution of mating preferences in male crickets. Future research should explore the whether the offspring of preferred females are more attractive, have stronger immune systems, and/or experience higher adult longevity.     

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.     

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.     

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

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

The evolution of repeated mating in the burying beetle, Nicrophorus vespilloides

Animals of many species accept or solicit recurring copulations with the same partner; i.e., show repeated mating. An evolutionary explanation for this excess requires that the advantages of repeated mating outweigh the costs, and that behavioral components of repeated mating are genetically influenced. There can be benefits of repeated mating for males when there is competition for fertilizations or where the opportunities for inseminating additional mates are rare or unpredictable. The benefits to females are less obvious and, depending on underlying genetic architecture, repeated mating may have evolved as a correlated response to selection on males. We investigated the evolution of repeated mating with the same partner in the burying beetle Nicrophorus vespilloides by estimating the direct and indirect fitness benefits for females and the genetics of behavior underlying repeated mating. The number of times a female mated had minimal direct and no indirect fitness benefits for females. The behavioral components of repeated mating (mating frequency and mating speed) were moderately negatively genetically correlated in males and uncorrelated in females. However, mating frequency and mating speed were strongly positively genetically correlated between males and females. Our data suggest that repeated mating by female N. vespilloides may have evolved as a correlated response to selection on male behavior rather than in response to benefits of repeated mating for females.     

Fitness benefits of polyandry for experienced females

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

No evidence that polyandry benefits females in Drosophila melanogaster

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

REMATING IN DROSOPHILA MELANOGASTER: ARE INDIRECT BENEFITS CONDITION DEPENDENT?

By measuring the direct and indirect fitness costs and benefits of sexual interactions, the feasibility of alternate explanations for polyandry can be experimentally assessed. This approach becomes more complicated when the relative magnitude of the costs and/or benefits associated with multiple mating (i.e., remating with different males) vary with female condition, as this may influence the strength and direction of sexual selection. Here, using the model organism Drosophila melanogaster, we test whether the indirect benefits that a nonvirgin female gains by remating (“trading‐up”) are influenced by her condition (body size). We found that remating by small‐bodied, low‐fecundity females resulted in the production of daughters of relatively higher fecundity, whereas the opposite pattern was observed for large‐bodied females. In contrast, remating had no measurable effect on the relative reproductive success of sons from dams of either body size. These results are consistent with a hypothesis based on sexually antagonistic genetic variation. The implications of these results to our understanding of the evolution and consequences of polyandry are discussed.     

Strong material benefits and no longevity costs of multiple mating in an extremely polyandrous leaf beetle, Chrysochus cobaltinus (Coleoptera: Chrysomelidae)

It is well established that females of many species exhibitpolyandry. Although such behavior often increases female fitnessby augmenting fecundity or enhancing the genetic diversity andvigor of their offspring, it often reduces female longevity.It has been argued that trade-offs between these costs and benefitsshould limit the degree to which females remate. However, theexistence of highly polyandrous species suggests substantialpolyandry benefits and/or minimal costs in some systems. Femalesof the leaf beetle, Chrysochus cobaltinus, are extremely polyandrous,providing an opportunity to examine the factors influencingthe evolution of such behaviors. We compared the fecundity andlongevity of singly mated females, females that mated multipletimes with the same male, and females that mated multiple timeswith different males. Compared with females in the single matingtreatment, females in both multiple mating treatments exhibiteda significant reduction in latency to oviposition and, due toan increase in daily egg production, significant increases inlifetime fecundity. This difference diminished as the time sincelast mating increased. There were no differences in fecunditybetween the 2 multiple mating treatments, indicating that mateidentity does not influence the material benefits of multiplemating. Surprisingly, female longevity did not differ amongtreatments. The pronounced fecundity benefits that females gainfrom multiple mating, coupled with a lack of longevity costs,apparently explains the extreme polyandry in this species. Inaddition, the existence of material fitness benefits via conspecificmatings raises the intriguing possibility that in a C. cobaltinus–Chrysochusauratus hybrid zone, heterospecific matings may confer similarbenefits to Chrysochus females.     

FEMALES RECEIVE A LIFE-SPAN BENEFIT FROM MALE EJACULATES IN A FIELD CRICKET

Abstract.— Mating has been found to be costly for females of some species because of toxic products that males transfer to females in their seminal fluid. Such mating costs seem paradoxical, particularly for species in which females mate more frequently than is necessary to fertilize their eggs. Indeed, some studies suggest that females may benefit from mating more frequently. The effect of male ejaculates on female life span and lifetime fecundity was experimentally tested in the variable field cricket, Gryllus lineaticeps. In field crickets, females will mate repeatedly with a given male and mate with multiple males. Females that were experimentally mated either repeatedly or multiply lived more than 32% longer than singly mated females. In addition, multiply mated females produced 98% more eggs than singly mated females. Because females received only sperm and seminal fluid from males in the experimental matings, these life‐span and fecundity benefits may result from beneficial seminal fluid products that males transfer to females during mating. Mating benefits rather than mating costs may be common in many animals, particularly in species where female mate choice has a larger effect on male reproductive success than does the outcome of sperm competition.     

Polyandry as a mediator of sexual selection before and after mating

The Darwin–Bateman paradigm recognizes competition among males for access to multiple mates as the main driver of sexual selection. Increasingly, however, females are also being found to benefit from multiple mating so that polyandry can generate competition among females for access to multiple males, and impose sexual selection on female traits that influence their mating success. Polyandry can reduce a male''s ability to monopolize females, and thus weaken male focused sexual selection. Perhaps the most important effect of polyandry on males arises because of sperm competition and cryptic female choice. Polyandry favours increased male ejaculate expenditure that can affect sexual selection on males by reducing their potential reproductive rate. Moreover, sexual selection after mating can ameliorate or exaggerate sexual selection before mating. Currently, estimates of sexual selection intensity rely heavily on measures of male mating success, but polyandry now raises serious questions over the validity of such approaches. Future work must take into account both pre- and post-copulatory episodes of selection. A change in focus from the products of sexual selection expected in males, to less obvious traits in females, such as sensory perception, is likely to reveal a greater role of sexual selection in female evolution.     

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.     

Female Remating Behavior in a Lekking Moth

In polyandrous species, male reproductive success will at least partly be determined by males' success in sperm competition. To understand the potential for post‐mating sexual selection, it is therefore important to assess the extent of female remating. In the lekking moth Achroia grisella, male mating success is strongly determined by female choice based on the attractiveness of male ultrasonic songs. Although observations have indicated that some females will remate, only little is known about the level of sperm competition. In many species, females are more likely to remate if their first mating involved an already mated male than if the first male was virgin. Potentially, this is because mated males are less well able to provide an adequate sperm supply, nutrients, or substances inhibiting female remating. This phenomenon will effectively reduce the strength of pre‐copulatory sexual selection because attractive males with high mating success will be more susceptible to sperm competition. We therefore performed an experiment designed both to provide a more precise estimate of female remating probability and simultaneously to test the hypothesis that female remating is influenced by male mating history. Overall, approximately one of five females remated with a second male. Yet, although females mated to non‐virgin males were somewhat more prone to remate, the effect of male mating history was not significant. The results revealed, however, that heavier females were more likely to remate. Furthermore, we found that females' second copulations were longer, suggesting that, in accordance with theory, males may invest more sperm in situations with an elevated risk of sperm competition.     

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

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

POLYANDRY INCREASES OFFSPRING FECUNDITY IN THE BULB MITE

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

The costs and benefits of multiple mating in a mostly monandrous wasp

The taxonomically widespread nature of polyandry remains a puzzle. Much of the empirical work regarding the costs and benefits of multiple mating to females has, for obvious reasons, relied on species that are already highly polyandrous. However, this makes it difficult to separate the processes that maintain the current level of polyandry from the processes that facilitate its expression and initiated its evolution. Here we consider the costs and benefits of polyandry in Nasonia vitripennis, a species of parasitoid wasp that is “mostly monandrous” in the wild, but which evolves polyandry under laboratory culture conditions. In a series of six experiments, we show that females gain a direct fecundity and longevity benefit from mating multiply with virgin males. Conversely, mating multiply with previously mated males actually results in a fecundity cost. Sexual harassment may also represent a significant cost of reproduction. Harassment was, however, only costly during oviposition, resulting in reduced fecundity, longevity, and disrupted sex allocation. Our results show that ecological changes, in our case associated with differences in the local mating structure in the laboratory can alter the costs and benefits of mating and harassment and potentially lead to shifts in mating patterns.     

Mating strategy in Aleochara bilineata: sperm storage and allocation

Abstract By contrast to females that can maximize reproductive success with only one or a few copulations, males generally increase their fitness with frequency of mating. Sperm storage and allocation is therefore crucial for both male and female fitness. Sperm storage in Aleochara bilineata (Coleoptera; Staphylinidae) is investigated by measuring the number of spermatozoa stored in the female spermatheca after single, double or triple successive copulations with different males. The potential advantages of polyandry are studied in terms of the number of sperm stored by females mated twice with the same male (i.e. repeated copulation), compared with females mated twice with two different virgin males (i.e. polyandry). Level of polygyny is also estimated by measuring sperm allocation when ten successive mates are offered to a virgin male. Aleochara bilineata females store the sperm of the same or different males additively, suggesting no advantage for polyandry in terms of the number of sperm stored. A virgin male is able to inseminate ten different females but the number of sperm transferred decreases linearly. Finally, the latencies and durations of copulations are measured in all experiments to estimate changes according to the male or female status (i.e. virgin or mated). The latency before mating is higher when females are virgin than when females have already mated.