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     

Mating behavior and sperm competition in the fly,Dryomyza anilis

Summary Mating behavior in D. andis was studied both in nature and in the laboratory. Each mating in nature consisted of several repeated copulation and oviposition bouts during which the male stayed mounted. One copulation bout included an intromission in the beginning followed by several tapping sequences. During one tapping sequence the male touched the external genitalia of the female with his claspers several times. The experimental matings with irradiated sterile males contained one copulation bout after which the female laid her eggs. In these matings the percentage fertilization for the last male to mate with the female increased with increasing number of tapping sequences. The percentage fertilization was affected positively also by the time between the end of the copulation bout and the start of oviposition, but the time spent in the copulation bout was not important. Furthermore, there was a negative correlation between the length of intromission and the percentage fertilization. After the copulation bout, the percentage fertilization was higher among the first eggs laid. This difference between the first and later eggs laid increased with the increasing number of tapping sequences, suggesting that copulating and ovipositing in several bouts further increase the male percentage fertilization. In matings recorded in nature, both the number of tapping sequences and the number of copulation and oviposition bouts varied greatly. Of the variables recorded during these matings, individual size and the number of eggs the female contained in the beginning of a mating affected the number of copulation bouts and the number of tapping sequences. Males also mated differently with females containing immature or mature eggs. The male behavior resulting in sperm precedence and the variability of matings in nature in relation to male sperm competition is discussed.     

Female butterflies mated with recently mated males show reduced reproductive output

Summary During copulation, males of the alfalfa butterfly, Colias eurytheme, transfer nutrients and sperm to the female. Recently mated males produce only about 40% of the quantity of material produced by males that have not recently mated (Rutowski and Gilchrist 1986). In this study, females that mated with recently mated males died sooner, had a lower lifetime egg output, and laid fewer eggs per day overall, but especially during the first 2 days after mating. We conclude that the effect of the materials (nutrients and sperm) passed by males at copulation on female oviposition and receptivity is such that the male's genetic return from nutrients passed is maximized.     

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.     

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 effect of female mating status on male offspring traits

In haplodiploid insects, males develop from unfertilized eggs; consequently, unmated females can reproduce. In a patchy, highly structured population, where brothers compete for mates and the reproductive return through sons is lower, females should minimize the number of male offspring. Consequently, unmated females are likely to have a reduced fitness compared to mated females. Here, we tested the oviposition behaviour of the haplodiploid beetle Coccotrypes dactyliperda. In this species, the unmated female can mate with her son to produce daughters. We predicted that unmated females could increase their fitness by (1) producing only few and small sons sufficient for mother–son mating and (2) dispersing to a patch occupied by conspecific females in order to increase their or their sons’ chance of mating. We demonstrate that (1) unmated females are common (23 % of all females), (2) they oviposit more frequently than mated females in occupied patches, (3) unmated females oviposit more eggs than mated females—this is in spite of the trade-offs, evident in this study, between the number of sons and the number of the mother’s future offspring after mating, (4) unmated females have a higher proportion of dispersing sons, and (5) sons of unmated females are smaller than sons of mated females. We conclude that the incidence of unmated females in the structured populations of C. dactyliperda is explained by plasticity in their oviposition behaviour. We discuss conditions where a high incidence of unmated females can persist as a successful strategy in structured populations.     

The wartbiter spermatophore and its effect on female reproductive output (Orthoptera: Tettigoniidae,Decticus verrucivorus)

Summary Male wartbiters Decticus verrucivorus transfer elaborate spermatophores to females during copulation. The spermatophore is attached externally to the female's genitalia and consists of two parts: a large, gelatinous, sperm-free portion, the spermatophylax, eaten by the female after mating; and a sperm-containing ampulla, eaten after the spermatophylax has been consumed. Since females take longer to eat larger spermatophylaxes, the duration of ampulla attachment is positively correlated with spermatophylax size. Two series of experiments were carried out, one in which the size of the spermatophylax consumed by females and the duration of ampulla attachment were manipulated in concert and another in which they were manipulated independently. Some females were also maintained on a protein-free diet and either supplied with or deprived of spermatophylax material. The amount of protein in the diet, but not the amount of spermatophylax material consumed, influenced female longevity, lifetime fecundity, and egg weight. When females were deprived of the spermatophylax, an experimental increase in the duration of ampulla attachment induced longer periods of unreceptivity in females after mating, a more rapid onset of oviposition, and an increased oviposition rate. Consequently, the number of eggs laid by females during their nonreceptive refractory periods increased significantly with increasing duration of ampulla attachment up to 180 min; however, there was no significant increase in the number of eggs laid beyond 180 min of ampulla attachment. This closely corresponds to an ampulla attachment duration of 188 min expected when a male transfers a natural spermatophylax of mean size to the female. These results suggest that the amount of ejaculate transferred to the female, and not the amount of spermatophylax material per se, is the factor controlling female receptivity and oviposition behavior. Since we did not detect any effect of spermatophylax consumption on female fecundity or egg weight, we conclude that the spermatophylax of D. verrucivorus functions primarily as a sperm protection device rather than as a form of male parental investment.     

Intraspecific hyperparasitism in a primary hymenopteran parasitoid

In solitary parasitoids, in which only one individual can emerge per host, the adaptive value of conspecific superparasitism is a function of the survival probability of the egg laid by the superparasitizing female. In the few cases which these probabilities are compared, the oldest immature has an advantage over the other individuals. We measured the acceptance rate of parasitized hosts and survival rate of supernumerary larvae in Anaphes victus (Hymenoptera: Mymaridae) in relation to the interval between ovipositions. When this interval was 5–7 days, the first immature was at the prepupa and pupa stage respectively, and female Anaphes victus changed their oviposition behavior markedly. They killed the developing parasitoid of their own species before ovipositing in it. The progeny of these females, which are normally primary parasitoids, developed thereafter as hyperparasitoids. Indeed, in contrast with other species, the survival of the second female's progeny increased with the time interval between ovipositions. This type of facultative intraspecific hyperparasitism is different from autoparasitism in Aphelinidae and has never been mentioned in other parasitoids; it would be adaptive if females of this short-lived species encounter low-quality patches.     

Reproductive activities in the sesarmid crab Sesarma intermedia in the coastal and estuarine habitats of Hakata,Japan

Aspects of activity pattern, mating, breeding behaviour and reproductive organs were studied in Sesarma intermedia (de Hann) along the Tatara river estuary, Hakata Bay, western Japan. Activity started from early May after a six-month hibernation period. The daily activity pattern was bimodal with one peak after sunset and another before sunrise. Mating started after emerging from hibernation and was ended by July. Practically no mating was seen in August and thereafter, by which time most of the females were carrying eggs. Larger males mated more frequently with any sized adult female. Copulation seemed to take place both in the burrow and on the surface of natural shelter. Females began to carry eggs from mid June on the estuarine habitat, whereas on the coastal habitat ovigerous females could be seen from mid-May. Multiple ovipositions of eggs were realized. Females were able to oviposit three times without any repeated mating. It took about 30 d to incubate one egg mass and less than one week to spawn again. The release of larvae was not sporadic but rather took place within a limited time interval. Sunset seemed to have a great influence on larvae release along the seashore. Energy allocation for reproductive purposes seemed to start before crabs awoke from the hibernation period. Towards the end of the breeding period there was a drastic decline in ovarian development with a remarkable gain in hepatopancreas, a reservoir for energy.     

Oviposition site selection and oviposition stimulation by conspecifics in the golden egg bug (<Emphasis Type="Italic">Phyllomorpha laciniata</Emphasis>): implications for female fitness

Phyllomorpha laciniata Vill. (Heteroptera, Coreidae) females lay eggs on the host plant and on the backs of conspecifics. Since egg survival is greater when eggs develop on the backs of conspecifics than when laid on plants, we predict that females should prefer to lay eggs on conspecifics. In addition, because conspecifics are a high-quality site that represents a limiting resource, females should experience oviposition stimulation upon an encounter with a conspecific. Our results reveal that, when both the host plant and conspecifics are available simultaneously, females lay eggs preferentially on conspecifics. The results also support the second prediction, since females housed with conspecifics lay more than twice the number of eggs than isolated females. Isolated females do not seem to retain eggs, suggesting that oviposition stimulation is the result of an acceleration of egg-maturation rates. Other studies have found oviposition stimulation by mating and have suggested that it is the result of male strategies to increase short-term male reproductive success at some cost to females. The evolutionary scenario of our model organism seems to be quite different since females benefit greatly from increasing egg laying when there are conspecifics, because the advantages in terms of offspring survival are likely to translate into substantial increases in female reproductive success.     

The effect of maternal body size on embryo survivorship in the broods of pregnant male pipefish

The occurrence of male pregnancy in the family Syngnathidae (seahorses, pipefishes, and sea dragons) provides an exceptionally fertile system in which to investigate issues related to the evolution of parental care. Here, we take advantage of this unique reproductive system to study the influence of maternal body size on embryo survivorship in the brood pouches of pregnant males of the broad-nosed pipefish, Syngnathus typhle. Males were mated with either two large females, two small females, a large then a small female, or a small then a large female. Our results show that offspring survivorship depends on an interaction between female body size and the number of eggs transferred by the female. Eggs of larger females deposited in large numbers are more likely to result in viable offspring than eggs of smaller females laid in large numbers. However, when females deposited smaller numbers of eggs, the eggs from smaller females were more likely to produce viable offspring compared to those from larger females. We found no evidence that this result was based on mating order, the relative sizes of competing females, or egg characteristics such as dry weight of eggs. Additionally, male body size did not significantly influence the survivorship of offspring during brooding. Our results suggest that the factors underlying offspring survivorship in pipefish may be more complex than previously believed, with multiple factors interacting to determine the fitness of individual offspring within the broods of pregnant males.     

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.     

Costs of courtship and mating in a sexually cannibalistic orb-web spider: female mating strategies and their consequences for males

The costs of courtship and mating may include increased risks of predation, the transmission of pathogens, and a loss of foraging opportunities. Thus, a female's decision to tolerate a courting male will depend upon how these costs offset the benefits of mating, which will depend on her reproductive and nutritional status. While these costs may be similar for mated and unmated females, the benefits of mating will be less for mated than virgin females. However, the cost of lost foraging opportunities may be higher for females with fewer nutritional reserves necessary for forming eggs. We examined how these costs and benefits influence the courtship and mating behaviour of male and female orb-web spiders, Argiope keyserlingi. In the field, females on webs that also contained a courting male intercepted fewer prey items per hour than females on webs without a male. In the laboratory, the presence of a courting male at the hub also attracted mantid predators to the web, increasing the risk of predation for both male and female. Staged mating experiments in the laboratory revealed that the frequency of female attacks and pre-copulatory cannibalism was greater among mated than virgin females. Feeding history did not affect aggression in virgin females but, among mated females, food-deprived spiders attacked and cannibalized males more frequently than sated females and only the latter ever remated. These differences in female behaviour influenced male mating strategies. Choice experiments demonstrated that males preferred to venture onto the silk threads of virgin rather than those of mated females. Similar patterns of mate selectivity were observed in the field; females with narrow abdomens attracted more males to the webs than females with broad abdomens, and copulations were observed more frequently among females with narrow abdomens. These smaller females are likely to be virgins that have recently molted. Males that preferentially mate with virgin females will not only avoid potentially fatal attacks but also obtain, on average, a higher fertilization success.     

Effects of female mating status on copulation behaviour and sperm expenditure in the freshwater crayfish <Emphasis Type="Italic">Austropotamobius italicus</Emphasis>

Sperm competition models predict that males should adjust their sperm expenditure according to the risk and/or intensity of sperm competition. In this paper, we analysed copulatory behaviour of both sexes and sperm expenditure in relation to female mating status (virgin or mated) in the freshwater crayfish Austropotamobius italicus, a species where males have been reported to feed on and remove sperm laid by other males. The same females were allowed to be inseminated sequentially by two males, and we compared the sexual behaviours of partners between the first (virgin females) and the second mating (mated females). We found that female resistance did not differ between the first and the second mating, nor males refused or took more time to mount a mated female. However, when mating with a mated female, males reached an effective copulation position significantly later. This occurred because second-mating males removed, by eating, all or most spermatophores previously deposited by first males. As removal was often incomplete, this resulted in a larger amount of sperm being deposited on female ventral parts after the second mating, although second males did not allocate more sperm to mated females than first males did. Thus, the peculiar mode of sperm competition, where males remove previously deposited sperm, and the consequent predictable strong last male prevalence in paternity likely led to the observed lack of adjustment of sperm expenditure to female mating status in this species.     

Eggs of cabbage root fly stimulate conspecific oviposition: Evaluation of the activity and determination of an egg-associated compound

Summary. Previous studies indicated the presence of antennally-active compounds in extracts of eggs laid by female cabbage root flies, Delia radicum, that stimulated oviposition by conspecific females. We confirmed that previously laid D. radicum eggs stimulated oviposition by other D. radicum females, in a dose-dependent manner. Methanol extracts of conspecific eggs stimulated oviposition by females D. radicum, whereas egg extracts of D. antiqua and Psila rosae had no effect. Electrophysiological recordings from the tarsal sensilla of D. radicum females indicated that neurones of the C₅ sensillum responded to the egg extracts from both D. radicum and D. antiqua, but not P. rosae. Chemical analysis revealed that the extract of eggs from D. radicum contained the thia-triaza-fluorene compound, 1,2-dihydro-3-thia-4,10,10b-triaza-cyclopenta[.a.]fluorene-1-carboxylic acid (CIF-1), an oviposition stimulant found previously only in cruciferous plants. Another potentially active component has yet to be identified.     

Prolonged copulation: A male ‘postcopulatory’ strategy in a promiscuous species,Lygaeus equestris (Heteroptera: Lygaeidae)

Summary Copulation in Lygaeus equestris L. (Heteroptera, Lygaeidae) is known to last 0.5–24 h. Variations in copula duration of field-collected insects were studied in the laboratory, and different hypotheses concerning the significance of prolonged copulations were tested.Through reciprocal matings with normal and sterile (irradiated) males, sperm displacement was estimated at about 90%. A male could thus increase his fitness by preventing subsequent matings of an inseminated female.Copulations with virgin insects, observed over 15 h, were classified in two categories: short (0.5–8.0 h) and long (> 15 h) duration (Fig. 1). No difference in the number of fertilized eggs was found between long and short copulations, and the insemination rate was highest during the first hour of a couplation (Fig. 2). Long-lasting couplations did not give rise to increased sperm displacement (Table 2). These results indicate that there is no difference in the amount of sperm transferred during short and long copulations and that no insemination takes place during the latter part of a prolonged copulation.Longer lasting copulations occurred when the sex ratio was male-biased than when it was female-biased (Fig. 1). The frequency of prolonged copulations was higher when the female was gravid than when she contained no eggs (virgin) (Figs. 3 and 4). Support is thus given to the hypothesis that prolonged copulation is a male postinsemination strategy to prevent subsequent matings of a female.Females subjected to male competition over a longer period, laid fewer eggs and died earlier than females that were mated but subsequently isolated from males (Fig. 5). Egg batches from females living with males were larger than batches from mated, isolated females (Table 3). This is probably due to a combination of many matings with short intermissions and prolonged copulations, both of which postpone oviposition.Comparisons between copulations of males with either gravid or virgin females during these experiments, led to the conclusion that short copulations with virgin females result from a male decision to terminate copulation after insemination is completed, whereas copula duration with gravid females is more likely to depend on a combination of male and female behavior.     

Copulation duration and sperm competition in white-faced dragonflies (Leucorrhinia intacta; Odonata: Libellulidae)

Summary In many odonates, females mate with more than one male while laying a single clutch of eggs. We studied paternity of eggs laid by remated females of Leucorrhinia intacta, a small libellulid dragonfly, at a pond near Syracuse, NY, USA. The probability of a female remating is a function of male density on the pond. The length of copulations differs considerably among males active on the study pond at the same time. Much of this variation was correlated with differences in mating tactics of the males; copulations by males that stayed on their territories during copulation were shorter than those by other males (Fig. 2). Eggs collected from females mated to irradiated, sterile males and to free-living, fertile males indicated that the average paternity expectation was higher for long than for short copulations, and that the variance in paternity expectation was lower for long than for short copulations. Some possible causes of the high variation in paternity at low copulation durations and possible reasons for differences in copulation duration between male mating tactics are discussed.     

Effects of spermatophores on male and female monarch butterfly reproductive success

Summary I present the results of experiments designed to measure the effects of spermatophores produced by male monarch butterflies on male and female reproductive success. There was wide variation in the number of matings by captive males, suggesting the potential for strong sexual selection on males. Male lifespan was not affected by total number of matings, nor did it differ between males that were allowed to mate and those not exposed to females. Two effects of spermatophores on female behavior or fecundity are reported; (1) Females that received large spermatophores delayed remating longer than those receiving small ones. (2) Females allowed to mate several times laid more eggs than singly-mated females. The relative importance of these effects is discussed in relation to monarch mating patterns.     

Polygyny and male parental care in Savannah sparrows: effects on female fitness

Summary To determine the effects of male mating status on female fitness, we compared the reproductive success, survival, and future fecundity of female Savannah sparrows (Passerculus sandwichensis) mated to monogamous vs. polygynous males in a 5-year study on Kent Island, New Brunswick, Canada. The proportion of males with more than one mate varied from 15 to 43% between years and sites. Polygynous and monogamous males fledged young of equal size in every year of the study. Females who shared paternal care with other females laid as many eggs per clutch and clutches per season as monogamously mated females. In most years polygynously mated females showed no delay in laying a second clutch, and they suffered no reduction in fecundity the following year. Recruitment of a female's offspring into the breeding population was generally independent of her mating status. Fitness costs of being mated to a polygynous male were only apparent in one year of the study, during which females mated to polygynous males had higher over-winter mortality than those mated to monogamous males. That same year, young raised by polygynous males were only one-third as likely to survive to reproductive maturity (as inferred by returns) as those raised by monogamous males. A male's mating status had no effect on his own survivorship. A male's mating status did not necessarily reflect his contributions to raising nestlings, which may partially explain why monogamously and polygynously mated females had equal fitness. At 35 nests the proportion of food deliveries brought by individual males varied from 0 to 75%; on average, males brought fewer than 30% of all food deliveries. Yet parental care by polygynous males was no less than that of monogamous males, at least at the nests of their primary females. Secondary females tended to receive less male assistance during the nestling stage, but their reproductive success was indistinguishable from that of primary females. Females feeding young without male assistance made as many food deliveries/h as did pairs in which males brought at least 30% of all food deliveries. Unassisted females did not suffer diminished fledging success or produce smaller fledglings. The benefits of polygyny for male Savannah sparrows are clear: polygynous males recruit more surviving offspring into the breeding population than monogamous males. The fitness of females, on the other hand, appears to be unaffected by whether their mate was monogamous or polygynous except in occasional years. Polygyny may be maintained in this population by the constraints of a female-biased sex ratio, the inability of females to predict a male's paternal care based on his morphology or behavior, the poor correlation between a male's mating status and his assistance at the nest, and inconsistent natural selection against mating with a polygynous male. Correspondence to: N.T. Wheelwright     

Sperm competition and evidence of sperm fertilization patterns in the carrion ball-roller beetle Canthon cyanellus cyanellus LeConte (Scarabaeidae: Scarabaeinae)

Field observation and laboratory experiments were conducted to investigate sperm competition and patterns of sperm fertilization under different experimental conditions in the carrion ball-roller beetle Canthon cyanellus cyanellus. Males in nature can mate with females whose spermathecae contains fertile sperm from other males. Sperm precedence was investigated using a visible genetic marker. The progeny of red (homozygous recessive) virgin females mated once with a red male and afterward, once with a green beetle (homozygous dominant) and vice versa, revealed that regardless of its color, the last male to mate fertilized c.a. 50% of the eggs, suggesting strong sperm competition. Males were able to achieve higher levels of paternity (more than 80%) when mated ad libitum with previously mated females, although large amount of variance in paternity does not exclude the possibility of first male sperm precedence or female cryptic choice. These results suggest that repeated mating and sperm replacement are the mechanisms by which last males achieve sperm precedence.