Experimental evidence for female-driven monandry in the wolf spider, <Emphasis Type="Italic">Pardosa astrigera</Emphasis>

Females of many species mate multiply, yet some taxon females mate with only one male, also known as monandry. Although the underlying mechanism behind female monandry is poorly understood relative to female polyandry, there are two contrasting hypotheses, male control and female control, for the maintenance of monandry. Since females generally benefit from multiple mating for material and/or genetic benefits, cases of monandry may reflect male manipulation on female remating at the expense of female fitness (male control). Alternatively, monandry may be favored by females, if females maximize their fitness by mating once (female control). Here, we tested two hypotheses by manipulating the number of mating (repeated mating and polyandry) on female fitness in a largely monandrous wolf spider, Pardosa astrigera. We allowed females to be inseminated once, twice with the same males (repeated mating) or with two males (polyandry) and determined female fitness consequences. The number of female mating, regardless of a single mating, repeated mating, or polyandry, had no significant effects on female fecundity, fertility, and survival and size of their spiderlings. However, the fitness cost of female multiple mating may to some extent be underestimated under laboratory conditions. In addition, female survival was adversely affected by induced multiple mating. Therefore, our results suggest that monandry of the wolf spider (P. astrigera) may be under the control of females, rather than under the control of males.     

A female preference for experienced males in the almond moth, Cadra cautella

Male mating status can affect female reproductive output if male ejaculate investment declines over consecutive matings. Accordingly, females are predicted to mate preferentially with virgin males. In mildly polyandrous lepidopterans, female fitness is less affected by reduced male investment than in more polyandrous species, and so the predictions for female mating preferences are less clear. We examined female mating preferences in the mildly polyandrous almond moth, Cadra cautella, in which ejaculate size does not affect female reproductive output. First, we allowed females to mate with virgin or once-mated males, in which the males were presented individually or simultaneously. We recorded the latency to mating and, in the case of the simultaneously presented trials, the identity of the successful, copulating male. We found that females mated more frequently with mated males (when simultaneously presented with both males), yet females did not differ in the time taken to initiate copulation with any male. We further examined if this mated male advantage was due to differential mate detection or locomotory behaviour of the male treatments. We tested the ability of virgin and mated males to locate a receptive female within a wind tunnel using long-distance pheromone cues and recorded their activity budget. We found no difference in the ability of mated or virgin males to locate or approach a receptive female, or in their activity levels. These data suggest a female preference for mated males in this species, a preference that may minimise other potential costs of mating.     

Protein content of spermatophores in relation to monandry/polyandry in butterflies

The evolution of a mating system, and specifically mating frequency, is dependent on the costs and benefits to both sexes of mating once or several times. In butterflies, males transfer a spermatophore that contains both sperm and accessory gland products. Accessory gland substances contain nutrients which, in some species, females use to increase their reproductive output and longevity. Nutrients contained in these packaged ejaculates represent investment by males in reproduction. Consequently, the nutritional composition of spermatophores may vary depending on the mating system. There are two lines of arguments concerning the evolution of the nutrient content of ejaculates. One hypothesis argues that male nuptial gifts evolved in the context of certainty of paternity and ease of finding mates; thus spermatophores of polyandrous males (with lower certainty of paternity and greater ease of finding mates) should contain less protein than those of monandrous males, since more spermatophores are produced on average. The other hypothesis argues that polyandry evolved in the context of maximization of male transfer of nutrients to females, and hence spermatophores of polyandrous males should contain more protein than those of monandrous males. In an attempt to distinguish between these two hypotheses, we determined how protein content of ejaculates varied with the degree of polyandry in nine species of pierid and two species of satyrid butterflies. We found that both relative ejaculate mass and protein content increased with the degree of polyandry. Hence our results are consistent with the view that polyandry has evolved in the context of male transfer of nutrients to females, and provides another example of a male adaptation to multiple mating in butterflies.     

Temporal patterns in reproduction may explain variationin mating frequencies in the green-veined white butterfly Pieris napi

There is genetic variation in the female mating rate in the green-veined white butterfly (Pieris napi), and females benefit from male ejaculates that contain both sperm and accessory gland substances. Although polyandry corresponds to higher lifetime fecundity than monandry, some females abstain from remating irrespective of the number of available mates. Explaining genetic variation in mating rates requires that monandrous females perform better than polyandrous ones under some conditions. We experimentally explored the reproductive performance of females either with a low or high intrinsic mating rate by allowing them to mate, feed, and lay eggs freely in a laboratory. Individual females followed different life histories: during the early days of reproduction, females with a low mating rate produced more eggs than females with a high mating rate. Hence, refraining from the benefits of multiple mating may be beneficial, if the time for reproduction is limited, or other female traits associated with polyandry are traded off against longevity. Given the day length of 10 h, a model shows that even if polyandrous females enjoy higher lifetime reproductive success, changeable and unpredictable weather will favor monandry if each period of suitable weather lasts, on average, less than 5 days. Thus, a combination of life history cost and unpredictability of fitness may explain the maintenance of monandry in the wild. Our results are also consistent with the observation that frequency of monandry increases with latitude.     

Male remating and female fitness in the wolf spider Pardosa astrigera: the role of male mating history

Although the effects of male mating history on female reproductive output and longevity have been studied in insects, few such studies have been carried out in spiders. In a mating system in which females are monandrous while males are polygynous, females may incur the risk by mating with successful males that have experienced consecutive matings and suffer from the possible depletion of sperm and/or associated ejaculates. Here, we examine the effects of male mating history on male courtship and copulation duration, female reproductive fitness, and female adult longevity of the wolf spider, Pardosa astrigera. Results indicated that male mating frequency had little effect on their subsequent copulation success, and of 35 males tested, about half of the males were able to copulate with five virgin females successively at an interval of 24 h. Male mating history had little effect on their courtship duration. However, male mating history significantly affected male copulation duration, female adult longevity, and reproductive output. Males that mated more frequently copulated longer and more likely failed to cause their mates to produce a clutch, although there was no significant difference in the number of eggs laid and the number of eggs hatched regardless of the first clutch or the second one. Multiple mating of male P. astrigera resulted in significant reduction in female adult longevity. Our results indicate that monandrous females mating with multiple-mated males may incur substantial fitness costs.     

The benefits of multiple mating to female seaweed flies, Coelopa frigida (Diptera: Coelpidae)

Female seaweed flies, Coelopa frigida, have the potential to benefit from mating more than once. Single matings result in low fertility so females may benefit directly from multiple copulations by sperm replenishment. A chromosomal inversion associated with larval fitness, with heterokaryotypic larvae having higher viability than homokaryotypes, means that polyandrous homokaryotypic females have a higher probability of producing genetically fit offspring than monandrous homokaryotypic females. We allowed females to mate only once, repeatedly four times to the same male, or polyandrously four times to four different males. Multiply mated and polyandrous females laid more eggs and produced more offspring than singly mated and monandrous females, respectively. Polyandrous females laid more eggs, had higher egg-to-adult survival rates and produced more offspring than repeatedly mated females. Fertility rates did not differ between treatments. The observed fitness patterns therefore resulted from increased oviposition through multiple mating per se, and a further increase in oviposition coupled with higher egg-to-adult offspring survival benefits to polyandry. Daily monitoring of individual females over their entire life spans showed that multiple copulations induced early oviposition, with polyandrous females ovipositing earlier than repeatedly mated females. Singly mated and polyandrous females incurred a longevity cost independent of egg production, whereas repeatedly mated females did not. This suggests that repeatedly mating with the same male may counteract a general cost of mating. Longevity, however, was not correlated with overall female fitness. Our data are discussed in the overall context of the seaweed fly mating system.Communicated by G. Wilkinson     

Fecundity,egg weight and longevity in relation to multiple matings in females of the monarch butterfly

Summary In many insects nutrients transferred by the male at mating are later incorporated into both the eggs and soma of the mated females. Accordingly, it has been suggested that insect females can use these male-derived nutrients for somatic maintenance and enhancement of their fecundity and fitness of their offspring. I this paper we tested the validity of these predictions by studying the longevity and reproductive output of 1, 2, 3, 4 or 5 times mated female monarchs Danaus plexippus, a nectar-feeding butterfly that is long-lived and strongly polyandrous and emerges as an adult without mature eggs. Females mated five times received ejaculates that corresponded to an average of 38% of their body weight at eclosion. However, we found that the number of times females had mated had no effect on their longevity, life-time fecundity, or egg weight. Although negative evidence should always be interpreted with caution, our study suggests that male-derived nutrients are less important for female longevity and reproductive output than are larval and adult food.     

No cost of male mating experience on female reproductive success in the almond moth, <Emphasis Type="BoldItalic">Cadra cautella</Emphasis> (Lepidoptera; Pyralidae)

Male copulation experience may have a profound impact on female reproductive success if male reproductive investment declines over consecutive copulations and if females are unlikely to re-mate. Male reproductive investment is particularly interesting in lepidopterans because males produce dimorphic sperm: a fertilizing (eupyrene) and a non-fertilising (apyrene) sperm. In two experiments, we explored the lifetime reproductive investment of male almond moths, Cadra cautella (also known as Ephestia cautella) and examined its influence on female reproductive success. In the almond moth, females re-mate infrequently and males transfer sperm in a spermatophore. Attached to the spermatophore is a large chitinous process, the function of which is unknown. One group of males were permitted consecutive copulations with virgin females and the amount of sperm and size of the spermatophore transferred were compared for all females. We found that the number of both eupyrene and apyrene sperm per ejaculate decreased with his increased mating frequency, while the size of the spermatophore process decreased dramatically after the male’s first copulation. In a second experiment, we allowed males to mate with females throughout their lives and then compared female fecundity and fertilisation success. We found no obvious decrease in female fecundity and fertilisation success with increased male copulation experience, despite the likely reduction in male gametic investment. We discuss potential explanations for the development of this enlarged and elaborate first spermatophore of male almond moths given that it confers no clear fitness advantage to females.     

Female seed beetles, <Emphasis Type="Italic">Callosobruchus maculatus,</Emphasis> remate for male-supplied water rather than ejaculate nutrition

Female seed beetles, Callosobruchus maculatus, mate multiply even though association with males and copulations carry costs, such as injury to the genital tract. Multiple mating (polyandry) may, however, offset these costs through the acquisition of food and water, two material benefits hypothesized to be obtained from the large ejaculates produced by males. The material benefits hypothesis can be tested by increasing female access to nutrients and water, with the prediction that female mating frequency will decrease as copulation is no longer required to derive these materials. Females were given water, 5% sugar–water or baker’s yeast, and were compared with females deprived of these. We presented females with virgin males daily for 8 days and recorded female mating frequency, survivorship, and fecundity. Females provided with water and sugar–water decreased mating frequency. Thus, water, rather than nutrients in the ejaculate, appears to be important to females of this species. In addition, both life span and fecundity were extended for females in the sugar–water and water treatments. Since water is scarce in the arid environment in which this species is found, we conclude that polyandry provides material benefits to females that may offset some of the costs of associating with males.     

Effects of size and nuptial gifts on butterfly reproduction: can females compensate for a smaller size through male-derived nutrients?

In butterflies and other insects, fecundity generally increases with female adult weight. Hence, most butterflies are essentially "capital breeders", because nutrients acquired during the larval stage are stored and subsequently used for egg production during the adult stage. However, in some species, males transfer a large nutritious ejaculate to the female at mating. These females can partly be characterized as "income breeders", and female mass can potentially be decoupled from fecundity to some extent. In the gift-giving green-veined white butterfly Pieris napi, it has been shown that female fecundity and longevity increase with number of matings and also that females mature at smaller size under poor food conditions compared to males. So it has been suggested that females can compensate for their smaller size through nuptial feeding. Here we test this hypothesis in P. napi by assessing female fecundity and longevity in relation to female mass and polyandry. The results showed no support for the hypothesis. Smaller females were not capable of increasing their mating rate to compensate for a low weight at eclosion. Instead, larger females remated sooner. Also, smaller females suffered from both a reduced daily and total fecundity compared to larger females and this decrease in fecundity was independent of female mating status, i.e. females allowed to mate only once and multiply mated females suffered to the same extent from their smaller size.     

Polyandry, multiple mating, and female fitness in a water strider Aquarius paludum

Contrary to Bateman’s principle, polyandry appears to be a common female mating strategy. Several hypotheses have been proposed to explain the evolution of polyandry. It is assumed that females gain either material or genetic benefits from multiple matings, or that they are coerced into mating by males. In water striders, mating is generally assumed to be costly to females, and they are thought to mate for reasons of convenience, adjusting their resistance to mating according to male harassment. Here, we tested the effect of number of matings (with the same male) and number of partners on female fitness in a water strider Aquarius paludum. In the first experiment, we regulated the time females spent with a male and found that females’ egg production increased with multiple matings up to a point. The result supports the existence of an optimal female mating frequency. In the second experiment, we tested how polyandry affects the number of eggs laid and egg hatching success. We conducted three different trials: females mated four times with either a single male, two different males, or with four different males. Females that mated with four different males laid the lowest number of eggs and had the lowest egg hatching success, suggesting that polyandry reduces females’ egg production and egg hatching success in A. paludum. We conclude that A. paludum females probably gain material benefits from mating but no genetic benefits were found in this study.     

Female benefit,male risk: Polyandry in the true armyworm Pseudaletia unipuncta

In Lepidoptera polyandry is common and females may increase their lifetime reproductive output through repeated matings if they acquire essential resources from male ejaculates. However, the paternity of males mating with previously-mated females is far from assured unless sperm precedence is absolute. In this study on the polyandrous armyworm, Pseudaletia unipuncta, we used two strains of male (the black-eyed wild type and a red-eyed homozygous, recessive mutant), mated with red-eyed females, to determine (i) whether male investment has any impact on female reproductive output, and (ii) if females do benefit from multiple matings, to what extent males fertilize the eggs to which they contributed. Multiple mating resulted in a significant increase in both the fecundity and longevity of females. However, the degree of sperm precedence (those eggs fertilized by the second male) varied from 0–100%, but was not affected by either male size or age, or by the duration of copulation. In cases where sperm precedence was <50% (x = 12%) females produced significantly more eggs (1384 versus 940) prior to the second mating than females where sperm precedence was >50% (x = 89%), indicating that the quality of the first mating influenced the fertilization success of the female's second mate.     

Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua

In lekking species, females may become sperm-limited when mating with sexually successful males, and this may be exacerbated by a poor male diet. Polygynous males may also be limited by the amount of accessory gland products (AGPs) they can transmit to females, which in turn may influence the females’ refractory period and longevity. Here, we tested the effect of male mating history, larval and adult diet on copula duration, mating intervals, female fecundity, fertilisation success, life span and likelihood to remate using sexually successful males of the lekking tephritid fly Anastrepha obliqua. Flies originated from either a native or exotic host fruit and were protein-fed or deprived. Male diet and larval host influenced copula duration, while the time elapsed between matings was affected by the interaction of mating order and male adult diet. Female fecundity was not influenced by female position in mating order or protein inclusion into the male diet. However, mating order and male larval diet influenced female fertilisation success. Importantly, as males mated successively they were less able to induce a refractory period on females, as the last females to mate with a male were more likely to remate and had slightly longer life spans than the first females to mate with males. These results might be attributed to a decrease in male AGPs with increasing male mating frequency. We discuss the role of conditional expression of male mating frequency with respect to A. obliqua’s life history, the trade-off that females face when mating with a successful male, the effect of larval diet on adult sexual performance and the possibility for sexual conflict to occur due to high male mating rates and fitness costs to females.     

The effect of mating frequency on female lifetime fecundity in the bulb mite, <Emphasis Type="Italic">Rhizoglyphus robini </Emphasis>(Acari: Acaridae)

We investigated the influence of mating frequency on lifetime reproductive success in females of the bulb mite, Rhizoglyphus robini. This species is highly promiscuous, and its colonial lifestyle promotes mating frequencies of at least several times a day. We manipulated mating frequencies either by keeping females continuously in the presence of a male, with males replaced every second day, or by exposing females to a new male for 4 h every second day (4 h is enough for a male to complete at least one copulation). We used males that were isolated from females either for 2 days, and thus had large reserves of sperm and seminal fluid, or for 2 h. We found that females with continuous access to a male had lower lifetime egg output than those exposed to males intermittently. This effect was mediated through decreased fecundity and not longevity. Male mating history had no significant effect on female fecundity or longevity. These results confirm that mating frequencies observed in bulb mite colonies exceed those necessary for sperm replenishment, and suggests that frequent mating is costly to females. We discuss possible explanations for the maintenance of mating frequencies that are detrimental to females.     

Fallow deer polyandry is related to fertilization insurance

Polyandry is widespread, but its adaptive significance is not fully understood. The hypotheses used to explain its persistence have rarely been tested in the wild and particularly for large, long-lived mammals. We investigated polyandry in fallow deer, using female mating and reproduction data gathered over 10 years. Females of this species produce a single offspring (monotocous) and can live to 23 years old. Overall, polyandry was evident in 12 % of females and the long-term, consistent proportion of polyandrous females observed, suggests that monandry and polyandry represent alternative mating strategies. Females were more likely to be polyandrous when their first mate had previously achieved high numbers of matings during the rut or was relatively old. However, polyandry was not related to the following factors: female age, the stage of the rut, the dominance ranks of mates, or the number of daily matings achieved by males. Polyandrous and monandrous multiple-mating females were not more likely than single-mating females to be observed with an offspring during the following year, and there were no significant differences in offspring size between these females. These results provide support for a fertility insurance hypothesis, with females remating if fertilization from the first mating was uncertain due to possible sperm depletion. The potential for different female mating strategies among large, polygynous mammals has generally been overlooked. Our findings highlight the complexity of female reproductive strategies and the possible trade-offs between fertilization success, preferences for high-quality males, and potential costs of polyandry, particularly for monotocous species.     

Indirect genetic benefits of polyandry in a spider with direct costs of mating

The search for the evolutionary explanation of polyandry is increasingly focused on direct and indirect selection on female resistance. In a polyandrous spider Stegodyphus lineatus, males do not provide material benefits and females are resistant to remating. Nevertheless, polyandrous females may obtain indirect genetic benefits that offset the costs associated with multiple mating. We manipulated the opportunity for females to select between different partners and examined the effect of female mating history (mated once, mated twice, or rejected the second male) on offspring body mass, size, condition, and survival under high- and low-food rearing regimens. We found that multiple mating, not female choice, results in increased female offspring body mass and condition. However, these effects were present only in low-food regimen. We did not find any effects of female mating history on male offspring variables. Thus, the benefits of polyandry depend not only on sex, but also on offspring environment. Furthermore, the observed patterns suggest that indirect genetic benefits cannot explain the evolution of female resistance in this system.     

Male mating bias and its potential reproductive consequence in the butterfly <Emphasis Type="Italic">Colias eurytheme</Emphasis>

Male mating biases may be a widespread feature of animal mating systems but the phenotypic consequences of these biases are often unclear, especially in species for which the operational sex ratio is strongly male-biased. In Colias butterflies, male choice is thought to be one of the factors responsible for maintaining a female-limited genetic color polymorphism, in which female wings appear either yellowish-orange or white (the “alba” variant). Previous studies have indicated that alba females of two montane Colias species mate fewer times during their lifetime, possibly as a partial consequence of this bias. Here we report the results of a field study of male mating behavior and female mating biology in Colias eurytheme, conducted under conditions of high (summer) and low (spring) population densities. Our data show that despite a substantial male bias in approaching alba vs yellowish-orange phenotypes [ratios of 0.08:1 (spring) and 0.28:1 (summer)], alba females did not contain, on average, fewer or smaller spermatophores. Not one of the 308 sampled females was virgin, but females of both phenotypes accumulated spermatophores with age, and tended to carry fewer, larger spermatophores in spring. These data suggest that significantly fewer (or lighter) spermatophores need not be an obligatory or simple consequence of a strong male bias in butterflies. We discuss these findings in light of the known, thermally and density-dependent complexities of alba reproductive biology and of the Colias mating system.     

Polyandrous female butterflies forage for matings

Butterfly mating systems exhibit great variation and range from strict monandry to strong polyandry. During mating males transfer ejaculates containing both sperm and accessory substances to females. In the polyandrous green-veined white butterfly, Pieris napi (Lepidoptera, Pieridae) these ejaculates average 15% of male body mass, but can represent up to 23% of body mass for individual males. Hence, mating is costly to males, and recently mated males increase copula duration but decrease ejaculate mass transferred to females. Substances transferred to females during mating are later incorporated into female soma and reproductive tissues, and multiply mated female butterflies have higher lifetime fecundity, lay proportionately larger eggs, and live longer compared to once mated females. Here we report that females of P. napi allowed to mate at liberty with recently mated males only (i.e. males that delivered a small ejaculate) increased their lifetime number of matings compared to females allowed to mate with virgin males only (i.e. males that delivered large ejaculates), the former group mating on average 5.1 times (range 2–10) and the latter group mating on average 2.8 times (range 1–4). The lifetime fecundity of the two groups of females did not differ significantly. Because nutrient donation from males is essential for females to realize their potential fecundity, we conclude that females of the polyandrous green-veined white actively forage for matings.     

Sexual selection and female fitness in <Emphasis Type="Italic">Drosophila simulans</Emphasis>

There is a current debate over the net fitness consequences of sexual selection. Do preferred males increase female fitness or are these males manipulating females for their own benefit? The evidence is mixed. Some studies find that mating with attractive males increases female fitness components, while others show that preferred males decrease measures of female fitness. In this study, we examined some of the fitness consequences of pre-copulatory sexual selection in Drosophila simulans. Virgin females were either paired with one male and given an opportunity for one copulation or were exposed simultaneously to two males. This allowed us to compare female preference (copulation latency) and fitness (longevity, lifetime productivity and rate of offspring production) both with and without the influence of male–male competition. When females had access to a single male, neither female longevity, productivity, nor short-term rate of productivity were associated with female preference, and although females mated more quickly with larger males, male size was also not associated with any female fitness measure. Inclusion of male–male competition showed that female longevity was negatively affected by preference, while productivity and rate of productivity was unaffected. This latter experiment also indicated that females preferred larger males, but again, male size was not associated with female fitness. These results indicate that females may not benefit from mating with preferred males, but they may incur survival costs.     

Experienced males have higher mating success than virgin males despite fitness costs to females

It is generally assumed that mating history has potentially important effects on the mating biology of insects, and differences in mating success of males, in relation to their mating history, have been commonly documented in Lepidoptera. Mating success of male European corn borer Ostrinia nubilalis, in relation to their mating history, and consequent fitness parameters for their female mates, were investigated. Mating experience significantly increased mating success for O. nubilalis males. Mating with experienced males significantly reduced lifetime fecundity and longevity of females. Sperm depletion, transfer of less nutritive substances or more toxic substances may explain the female response to mating with experienced males. Male persistence or some other compensatory mechanism may account for female acceptance of experienced males.