Impact of male mating history on the postmating resumption of sexual receptivity and lifetime reproductive success in Choristoneura rosaceana females

Abstract.  The first objective of the present study is to test the hypothesis that the decrease in the number of eupyrene spermatozoa in the spermatheca is directly associated with the resumption of sexual receptivity in female moths, an aspect that has not been examined in previous studies. The obliquebanded leafroller, Choristoneura rosaceana , is used and females mated with previously mated males have a shorter refractory period than those mated with virgins. This difference is associated with a faster rate of movement of sperm from the spermatheca. Overall, the length of the female refractory period coincides with the mean time required for the number of eupyrene sperm in the spermatheca to drop to approximately 3000, regardless of male mating history. Although such a decline in sperm numbers may be a factor responsible for the resumption of sexual receptivity, this is clearly not the only one because more than 40% of females remate even though sperm numbers in the spermatheca are well above this threshold. Virgin males do not vary the mass or the content of their ejaculate as a function of the female's reproductive status and this may increase the risk of sperm competition if the female is previously mated. The second objective of this study is to examine the effect of previous male mating history on female reproductive potential. Females mated with previously mated males have a significantly lower fecundity than those mated with virgin males. However, in all treatments, remating increases both female longevity and lifetime fecundity. There is also a significant effect of female mass on the length of the refractory period and on lifetime fecundity, with large females resuming sexual receptivity sooner and laying more eggs than small ones, regardless of male mating history.     

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.     

Male and female condition influence mating performance and sexual receptivity in two tropical fruit flies (Diptera: Tephritidae) with contrasting life histories

Recent recognition of widespread polyandry in insects has generated considerable interest in understanding why females mate multiple times and in identifying factors that affect mating rate and inhibit female remating. However, little attention has been paid to understanding the question from both a female and male perspective, particularly with respect to factors that may simultaneously influence female remating rates. Here, we report on a study aimed at ascertaining the possible interactive effects that male and female size and diet, and female access to a host could have on mating latency, probability, and duration and female refractory period using two tropical fruit fly species with contrasting life histories. Of all factors tested, adult diet played the most significant role. Both Anastrepha ludens and Anastrepha obliqua males which had constant access to protein and sucrose mated more often, had shorter copulations and induced longer refractory periods in females than males fed a low quality diet (sucrose offered every third day). Female size and the interaction with male diet determined how quickly female A. ludens mated for the first time. Smaller females mated sooner with low quality fed males than with high quality fed males while there was no difference for large females, suggesting that male choice may be at play if high quality fed males discriminate against smaller females. Copulation duration also depended on both male and female nutritional condition, and the interaction between male diet and female size and diet. Large and high quality fed females had shorter copulations regardless of male condition. Importantly, for A. ludens, female refractory period depended on male size and the nutritional condition of both males and females, which could indicate that for this species, female receptivity does not depend only on the condition of the male ejaculate. For A. obliqua refractory period was associated with the interaction between male size and diet and male diet and host presence. We discuss our results in terms of male ability to inhibit female remating and the relative contribution of female condition to this behavior. We also address the importance of studying effects simultaneously on species with contrasting life histories.     

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.     

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.     

Males of the seed bug Togo hemipterus (Heteroptera: Lygaeidae) use accessory gland substances to inhibit remating by females

In species in which females mate repeatedly, males can adopt several strategies to reduce the risk of sperm competition with future males. The refractory period of females significantly increased as the mating duration increased in the seed bug Togo hemipterus (Heteroptera: Lygaeidae). To elucidate the mechanisms by which mated females are inhibited from remating, we investigated the effects of male-derived substances on the inhibition of mating receptivity of virgin females by injecting the substances into their abdomens. The length of time from injection to mating in virgin females was significantly longer for females injected with accessory gland B solution than for those injected with seminal vesicle, accessory gland A, or control solutions. This is the first report showing that heteropteran males inhibit female remating by using substances from an accessory gland. We discuss and consider the adoption and evolution of this strategy by T. hemipterus males by focusing on female genitalia structures, oviposition habit, and paternity and comparing these traits with those of other heteropterids.     

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.     

Reproductive costs of mating with a sibling male: sperm depletion and multiple mating in Cephalonomia hyalinipennis

Polygynous parasitoid males may be limited by the amount of sperm they can transmit to females, which in turn may become sperm limited. In this study, I tested the effect of male mating history on copula duration, female fecundity, and offspring sex ratio, and the likelihood that females will have multiple mates, in the gregarious parasitoid Cephalonomia hyalinipennis Ashmead (Hymenoptera: Bethylidae: Epyrinae), a likely candidate for sperm depletion due to its local mate competition system. Males were eager to mate with the seven females presented in rapid succession. Copula duration did not differ with male mating history, but latency before a first mating was significantly longer than before consecutive matings. Male mating history had no bearing on female fecundity (number of offspring), but significantly influenced offspring sex ratio. The last female to mate with a given male produced significantly more male offspring than the first one, and eventually became sperm depleted. In contrast, the offspring sex ratio of first‐mated females was female biased, denoting a high degree of sex allocation control. Once‐mated females, whether sperm‐depleted or not, accepted a second mating after a period of oviposition. Sperm‐depleted females resumed production of fertilized eggs after a second mating. Young, recently mated females also accepted a second mating, but extended in‐copula courtship was observed. Carrying out multiple matings in this species thus seems to reduce the cost of being constrained to produce only haploid males after accepting copulation with a sperm‐depleted male. I discuss the reproductive fitness costs that females experience when mating solely with their sibling males and the reproductive fitness gain of males that persist in mating, even when almost sperm‐depleted. Behavioural observations support the hypothesis that females monitor their sperm stock. It is concluded that C. hyalinipennis is a species with a partial local mating system.     

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.     

Butterflies tailor their ejaculate in response to sperm competition risk and intensity

Males of many insects eclose with their entire lifetime sperm supply and have to allocate their ejaculates at mating prudently. In polyandrous species, ejaculates of rival males overlap, creating sperm competition. Recent models suggest that males should increase their ejaculate expenditure when experiencing a high risk of sperm competition. Ejaculate expenditure is also predicted to vary in relation to sperm competition intensity. During high intensity, where several ejaculates compete for fertilization of the female''s eggs, ejaculate expenditure is expected to be reduced. This is because there are diminishing returns of providing more sperm. Additionally, sperm numbers will depend on males'' ability to assess female mating status. We investigate ejaculate allocation in the polyandrous small white butterfly Pieris rapae (Lepidoptera). Males have previously been found to ejaculate more sperm on their second mating when experiencing increased risk of sperm competition. Here we show that males also adjust the number of sperm ejaculated in relation to direct sperm competition. Mated males provide more sperm to females previously mated with mated males (i.e. when competing with many sperm) than to females previously mated to virgin males (competing with few sperm). Virgin males, on the other hand, do not adjust their ejaculate in relation to female mating history, but provide heavier females with more sperm. Although virgin males induce longer non-receptive periods in females than mated males, heavier females remate sooner. Virgin males may be responding to the higher risk of sperm competition by providing more sperm to heavier females. It is clear from this study that males are sensitive to factors affecting sperm competition risk, tailoring their ejaculates as predicted by recent theoretical models.     

The evolution of polyandry: an examination of the genetic incompatibility and good‐sperm hypotheses

I have examined the adaptive significance of polyandry using the Australian field cricket Teleogryllus oceanicus. Previous studies of polyandry have examined differences in offspring production by females mated multiply to a single male or females mated multiply to different males. Here I combine this approach with a study of parentage of offspring produced in the later group. Females mated to two different males had a higher proportion of their eggs hatching than did females mating twice with a single male. Offspring fitness parameters were not effected. There was little evidence to suggest that females elevate their hatching success via fertilizing their eggs with sperm from genetically compatible males. Although the average paternity points towards random sperm mixing, there was considerable individual variation in sperm competition success. Patterns of parentage were consistent across females mating twice or four times. Sperm competition success was not related to offspring viability or performance. Thus, the notion that competitively superior sperm produce competitively superior offspring is not supported either. The mechanism underlying increased hatching success with polyandry requires further study.     

三突伊氏蛛雌蛛不同交配史对雄蛛交配行为的影响

近年来越来越多研究表明,雄性产生精子(精液)也需付出代价。在多次交配的动物中,雄性为获得最大生殖潜力,必须依据配偶的质量策略性地调整每次交配的生殖投入。雄性策略性的生殖投入主要体现在两个方面,一是精子竞争(sperm competition),二是柯立芝效应(Coolidge effect)。目前精子竞争研究主要集中于昆虫类群,而柯立芝效应研究集中于高等脊椎动物,同时验证结果也时常与假说不一致。以多次交配的三突伊氏蛛为材料,以雄蛛交配行为为指标,在蜘蛛类群中探讨和验证雄性精子竞争强度假说和柯立芝效应。设定3个交配组合:2只雄蛛依次与1只雌蛛各交配1次(A组)、2只雄蛛依次与2只雌蛛各交配1次(B组)和1只雄蛛与1只雌蛛交配2次(C组),分析比较3个交配组合的三突伊氏蛛第1次交配和第2次交配在交配潜伏期、交配持续时间和交配回合数方面的差异,比较三突伊氏蛛雌蛛不同交配史对雄蛛交配行为的影响,以此验证雄性精子竞争强度假说和柯立芝效应。研究结果表明A和B组的三突伊氏蛛第2次交配的交配潜伏期和交配持续时间显著长于第1次交配。同时,C组的三突伊氏蛛第1次交配的交配潜伏期和交配持续时间与第2次交配都没有显著差异。同时,A、B和C组的三突伊氏蛛第1次交配的交配回合数与第2次交配都没有显著差异。研究结果支持精子竞争强度假说,而不支持柯立芝效应。     

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.     

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.     

Why Do Female Callosobruchus maculatus Kick Their Mates?

Sexual conflict is now recognised as an important driver of sexual trait evolution. However, due to their variable outcomes and effects on other fitness components, the detection of sexual conflicts on individual traits can be complicated. This difficulty is exemplified in the beetle Callosobruchus maculatus, where longer matings increase the size of nutritious ejaculates but simultaneously reduce female future receptivity. While previous studies show that females gain direct benefits from extended mating duration, females show conspicuous copulatory kicking behaviour, apparently to dislodge mating males prematurely. We explore the potential for sexual conflict by comparing several fitness components and remating propensity in pairs of full sibling females where each female mated with a male from an unrelated pair of full sibling males. For one female, matings were terminated at the onset of kicking, whereas the other’s matings remained uninterrupted. While fecundity (number of eggs) was similar between treatments, uninterrupted matings enhanced adult offspring numbers and fractionally also longevity. However, females whose matings were interrupted at the onset of kicking exhibited an increased propensity to remate. Since polyandry can benefit female fitness in this species, we argue that kicking, rather than being maladaptive, may indicate that females prefer remating over increased ejaculate size. It may thus be difficult to assess the presence of sexual conflict over contested traits such as mating duration when females face a trade off between direct benefits gained from one mating and indirect benefits from additional matings.     

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

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

Sexual conflict and cooperation under naturally occurring male enforced monogamy

An evolutionary conflict often exists between the sexes in regard to female mating patterns. Females can benefit from polyandry, whereas males mating with polyandrous females lose reproductive opportunities because of sperm competition. Where this conflict occurs, the evolution of mechanisms whereby males can control female remating, often at a fitness cost to the female, are expected to evolve. The fitness cost to the female will be increased in systems where a few high status males monopolise mating opportunities and thus have limited sperm supplies. Here we show that in the cockroach Nauphoeta cinerea, a species where males enforce female monogamy in the first reproductive cycle, males that have become sperm depleted continue to be able to manipulate female remating behaviour. Although the manipulation severely decreases fecundity in females mated to sperm-depleted males, males benefit, increasing their relative fitness by preventing other males from reproducing. Our results suggest that there is selection on maintaining the mechanism of manipulation rather than maintaining sperm numbers. Taken with previous research on sexual conflict in N. cinerea, this study suggests that the causes and consequences of sexual conflict are complex and can change across the life history of an individual.     

Factors influencing the onset of egglaying in a cecidomyiid fly

Abstract The timing of the onset of egglaying in the Hessian fly, Mayetiola destructor (Say), is influenced by several exogenous and endogenous factors. Mated females initiated egglaying 48 h earlier than virgins and laid 3–4 times more eggs before dying. The effects of mating on the onset of egglaying were further modified by several other factors whose effects were measured in hours rather than days. Increases in ambient temperatures experienced by mated females shortened the post-mating pre-ovipositional transition phase; however, the effects of temperature were not linear throughout the temperature range. Age of females at the time of mating also influenced the onset of egglaying. Females that mated 1 , 2 and 3 h after eclosion spent 190 , 160 and 120 min in the post-mating transition phase, respectively. Effects of age were also observed when females were mated over the three calling periods that comprise the 3-day lifespan of the adult female. Linear regressions of transition times on time of mating had similar slopes for first and second day post-eclosion females but were offset such that first-day females mated late in the morning had similar transition times to second-day females mated early in the morning. By the third day post-eclosion, transition times showed no significant changes when females were mated throughout the calling period. Possible mechanisms underlying the effects of mating, temperature, and female age on post-mating pre-oviposition transition times are discussed.     

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.     

Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina

Understanding why females mate multiply is a major issue in evolutionary ecology. We investigated the consequences of an asynchronous arrival pattern on male competition and multiple paternity in the apparently monoandrous agile frog ( Rana dalmatina ). The largest frogs arrived first and both males and females lost weight significantly during the spawning period. Asynchronous arrival at breeding sites resulted in a male-biased operational sex ratio (OSR). The OSR was more strongly male-biased at the beginning and at the end of the breeding period when the number of satellite males increased. All females mated only once, but multiple paternity within clutches occurred at the beginning and the end of the breeding period. The influence of asynchronous arrival and biased sex ratio suggests that reduced variance or bet-hedging promoting female fitness had only a reduced role in the evolution of polyandry, and polyandry is likely to be associated with male benefits. Polyandry in frogs can be explained either by forced mating as a result of sexual conflict or by clutch piracy. By modifying intrasexual competition, asynchronous arrival and changes in OSR may have a decisive influence upon the evolution of mating systems and favour both polyandry and stable coexistence of alternative mating behaviour.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 191–200.