Polyandry and its effect on female reproduction in the green-veined white butterfly (Pieris napi L.)

Summary In many insects nutrients transferred by the male to the female at mating are later incorporated into both the eggs and soma of the mated females. Accordingly, it has been suggested that female insects can use these male-derived nutrients both for somatic maintenance and to increase both the number and quality of their offspring. Moreover, much discussion is presently devoted to whether the male nuptial gift represents paternal investment, defined as any increase in given male's total surviving progeny by increasing the reproductive output by a given female, or mating effort which obtains if a male gains by increasing the proportion of eggs he fertilizes from a given female (Parker and Simmons 1989). If the male nuptial gift represents parental investment it should be expected to benefit predominantly the offspring sired by the donor, whereas the physiological fate of the male nuptial gift is somewhat irrelevant under the mating effort explanation. In this paper we test these issues by studying the lifetime fecundity, egg weights and longevity of two groups of females of the polyandrous green-veined white butterfly, Pieris napi, one group of which was allowed to mate only once and the other of which was allowed to mate at liberty, the latter group of females mating on average 2.28 times. Moreover, to test the incorporation rate of male-derived nutrients, we performed a second set of experiments where females were allowed to mate with radioactively labelled males. The results showed that polyandrous females had higher lifetime fecundity compared to monandrous females, laying on average 1.61 as many eggs, and that the difference in cumulative fecundity between the two groups was statistically significant from the 5th day of egg-laying onwards. Polyandrous females also lived longer and maintained egg weight at a high level for longer than monandrous females. Largely concomitant with egg-laying rate, incorporation rate of male-derived nutrients peaked 3–4 days after mating, subsequently tapering off to stabilize at about 40% of the maximum. Given the opportunity, female P. napi remated after 3–5 days, the duration of the refractory period being positively correlated with ejaculate mass. Hence, although the nutrient investment of the first male to mate with a female subsidizes the progeny of later-mating males, the male nuptial gift in P. napi clearly qualifies as both paternal investment and mating effort. Correspondence to: C. Wiklund     

Courtship solicitation by females of the checkered white butterfly,Pieris protodice

Summary The willingness of some females of the checkered white butterfly to approach and chase conspecifies was studied in the field. Both virgin and mated females were observed approaching and chasing conspecifics. Such responses to males result in the solicitation or continuation of male courtship attempts, which in turn may lead to copulation.Mated females that approached conspecifics had significantly smaller spermatophores than females in a random sample from the same population.Females that approached tethered animals spent more time chasing tethered males than tethered females. Females with small spermatophores spent more time chasing tethered males than did females with larger spermatophores.These results confirm the hypothesis that mated females that approach and chase conspecifics are doing so in an effort to solicit male courtship attempts and to potentially receive a fresh spermatophore. The selective forces favoring courtship solicitation by females are discussed.     

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.     

Mating with a kin decreases female remating interval: a possible example of inbreeding avoidance

Inbreeding depression is a relative decline in fitness in offspring of related parents. The magnitude of inbreeding costs varies among taxa and may increase under stressful conditions. Inbreeding tolerance is expected to be low and selection for inbreeding avoidance intense when both sexes invest substantially in shared offspring like in nuptial gift-giving butterflies. This is especially true for increasing mating rate for inbreeding avoidance as nuptial feeding decreases net costs of mating for females. We explored implications of inbreeding in the nuptial gift-giving green-veined white butterfly, Pieris napi. Compared to outbred ones, partially inbred (F = 0.25) eggs and neonate larvae had 25% lower hatching success and 30% lower survival until adult eclosion, respectively. Inbreeding was also associated with small size. Yet, the magnitude of inbreeding depression was independent of larval conditions. A lack of assortative mating and mating durations independent of mating type suggest that neither females nor males discriminate close relatives (r = 0.5) as mates. Indicative of a postcopulatory mechanism to avoid inbreeding, female remating intervals decreased following incestuous matings. Such a plastic response may affect the level of postcopulatory sexual selection as female remating interval (time between successive matings) is necessarily negatively correlated with mating rate (matings per unit time) and mating frequency (lifetime number of matings), and precopulatory mate choice appeared insignificant. Moreover, incest-induced shift in the phenotype towards the adaptive peak may contribute to the evolution of female mating rates, although alternative explanations for polyandry besides material benefits have rarely been invoked when nuptial feeding is involved.     

Mating behaviour of the tiger blue butterfly (Tarucus theophrastus): competitive mate-searching when not all females are captured

Summary Females of the tiger blue butterfly (Tarucus theophrastus) fly upwind in search of the larval hostplant. Males perch or patrol the downwind edges, searching for incoming females or those already on the bush. A model of competitive mate-searching is developed for the case where not all receptive females are contacted by searching males: the model differs from the earlier ones of Parker (1970, 1974), particularly when few males are involved. Observed distributions of males upon bushes of different sizes agree better with the predictions of the game theory model than with a random distribution of males. The described model may be widely applicable to populations where females remate, but frequently evade detection by searching males.     

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.     

Mating and its effect on acoustic signalling behaviour in a primitive orthopteran,Cyphoderris strepitans (Haglidae): the cost of feeding females

Summary Males of the primitive orthopteran, Cyphoderris strepitans, provide their mates with two types of nuptial food gift during mating: 1) females feed while coupled on the fleshy metathoracic wings of the male and the resultant flow of haemolymph and 2) the spermatophore transferred by the male includes a gelatinous spermatophylax which the female eats after mating. During the peak breeding interval, virgin males secure significantly more matings than their numbers relative to non-virgin males would predict. We tested the hypothesis that non-virgin males, having lost a substantial portion of available energy through previous investment in females, call significantly less than virgin males. Reduced calling should result in the attraction of fewer females and/or a greater risk of intrusion from competing males and consequently, a lowered mating success. Calling activity of male C. strepitans of varying mating status was monitored with a sound activated relay apparatus for two consecutive nights following their capture. Males were of three experimental groups, virgin, freshly wounded males (mated on the same night of capture), and old-wound males (mated at least one night prior to capture). Our cata showed a significant short-term reduction in signalling activity as a consequence of mating. Whereas there was no difference in the time spent calling by virgins on the first and second nights following capture, freshly wounded and oldwound males called significantly less on the first night than on the second. Furthermore, the proportion of males calling on both nights was significantly greater for the virgin and old-wound groups than for freshly wounded males. When the duration over which males called on the first night was compared with that of the second, virgin males showed no difference whereas old-wound males called for significantly shorter intervals on the first night. These results indicate that the cost of a large nutrient investment in females lowers the energy level in males below the threshold required for a prolonged signalling period. After a refractory interval during which males feed and replenish their energy reserves, calling levels equivalent to those which occur prior to mating are regained. Active female choice may also contribute to the reduced mating success of non-virgins, but this possibility remains untested.     

Influence of the courtship song of the acridid grasshopper Gomphocerus rufus L. on the female

Summary Males of the acridid species Gomphocerus rufus L. perform unusually long courtship. Following their imaginal molt, the behavior of the females changes in three stages: initial rejection of the males, passive acceptance without singing, and active attraction of a mate by singing. Females in the active state permit copulation after brief courtship or even without it.To understand the function of long courtship, two hypotheses are tested by the present experiments. Hypothesis A assumes that the long courtship of the male affects the female so as to accelerate entry into the active mating state. This is not the case: Females raised in isolation enter the active state at the same time as those that have been exposed to courtship continually. Hypothesis B assumes that the long courtship changes the behavior of a female still in the passive state to enable earlier copulation. This hypothesis is tested by longterm recording of the locomotor and singing activity of the female in the presence of a courting male. The records show that the locomotor activity of a female in the passively acceptant state is significantly reduced during male courtship. Moreover, males in the presence of a passively acceptant female court longer than when the female is in either of the two other states.It appears, therefore, that the unusually long courtship serves to keep the female near the male for a longer period of time, increasing the chance of copulation. The advantages and disadvantages of this courtship strategy are compared with those of searching for a female in the active state.     

Different ejaculate delivery strategies in first versus subsequent matings in the swallowtail butterfly Papilio machaon L.

Summary Evidence suggests that males incur costs in producing ejaculates. Therefore some discrimination should be expected with respect to their pattern of allocating ejaculates. In a laboratory study, males of the European swallowtail butterfly Papilio machaon were mated with conspecific virgin females up to six times. The weight of the spermatophore and of the accessory substances delivered by males, the duration of mating, and the number of sperm in ejaculates were measured. The weight of the first spermatophore was related to male weight but that of accessory substances was not. The weight of the spermatophore delivered by males upon remating was always less than that of the first spermatophore. Second spermatophores Produced by males were smallest when delivered on the day after the first mating and increased asymptotically to about half the initial size with time elapsed since the first mating. Copula duration was highest for males remating on the day after the first mating but decreased to the duration of the first mating for males that were remated on the third day after the first mating or later. The weight of accessory substances delivered by males and the number of sperm in ejaculates were also higher in first matings compared to all subsequent matings. Both of two males that were handpaired on three consecutive days after the first mating produced a cumulative ejaculate mass equalling that transferred at the first mating. Thus the fact that males delivered smaller ejaculates upon remating on the third day after the first mating or later requires explanation, especially in view of the fact that copulations were not prolonged. We argue that the male ejaculate delivery strategy in mildly polyandrous species should be to mate for the first time with virgin females, when a maximum size ejaculate should be delivered, and then to maximize the number of matings. The rationale behind the male shift towards smaller ejaculate sizes delivered at subsequent matings is that: (1) the size of the ejaculate that can be produced is dependent on the time elapsed since the last mating; (2) the abundance of virgin females decreases as the flight season proceeds; and (3) there is an inverse relationship between the size and number of ejaculates that a male can produce in his life-time.     

Chemical basis for differential acceptance of two sympatric rutaceous plants by ovipositing females of a swallowtail butterfly, Papilio polytes (Lepidoptera, Papilionidae)

Summary. In the natural habitat of Papilio polytes, a Rutaceae feeder utilizing Toddalia asiatica as a major host plant, some other rutaceous plants such as Murraya paniculata (abundant) and Glycosmis citrifolia (relatively rare) occur sympatrically as potential hosts. Whereas G. citrifolia is occasionally infested in the field, M. paniculata remains entirely unexploited by the butterfly. We thus examined the phytochemical mechanisms that can explain the differential acceptance of the two plants by ovipositing females of P. polytes. The foliage of G. citrifolia was found to readily induce oviposition and females deposited eggs in response to a methanolic extract of the plant. Stimulatory activity-directed fractionation of the extract revealed the presence of two characteristic compounds, trans-4-hydroxy-N-methylproline and 2-C-methylerythronic acid, known to serve as oviposition stimulants for the butterfly. In addition, larvae performed as well or better onG. citrifolia as on T. asiatica. Similar examination of the inhibitory chemical constituents of M. paniculata led to the isolation of an oviposition deterrent. The compound, identified as trigonelline (N-methylpyridine- 3-carboxylic acid), exhibited moderate oviposition deterrency to females. These results combined with our previous data are in agreement with the observed differential utilization of the two plants by P. polytes in the field.     

Asymmetric costs favor female desertion in the facultatively polyandrous northern flicker (Colaptes auratus): a removal experiment

Previous studies of biparental care in birds have focused on the males contribution and experimental removal of males. Woodpeckers, with a high level of paternal care including nocturnal incubation and brooding by males, offer a meaningful system in which to examine the importance of care by females. I studied the reproductive performance of 17 widowed male and 8 widowed female northern flickers (Colaptes auratus) relative to biparental (control) pairs. Of these single parents all widowed shortly after hatching, only one female abandoned its nest. Single parents boosted their provisioning rates to achieve 83% the provisioning rate of control broods, but reared significantly fewer young and young of poorer quality. However, single males, with 85% of the reproductive success of controls, were more successful than females with 43% the success of controls. Among widowed birds, a not significant lower survival was observed, but the chance of re-pairing with the same partner in a subsequent year was only 16% in the natural population, so long-term costs of desertion may be small. Although females seem to have the incentive and ability to desert, a lack of available males may constrain opportunities. This study demonstrates that when parental care roles are reversed in altricial birds, asymmetric benefits can favor female and not male desertion.     

Frequency and timing of extrapair fertilisation in the polyandrous red phalarope (Phalaropus fulicarius)

In sequentially polyandrous bird species, where females mate with different males in succession during a single breeding season, sperm stored by females can occasionally lead to extrapair fertilisations (EPFs) in clutches cared for by the second and subsequent males. Thus, we predicted that in red phalaropes (Phalaropus fulicarius) – a sex-role-reversed, sequentially polyandrous, arctic breeding shorebird – EPFs would occur more frequently in clutches laid later in the breeding season. We used multilocus DNA profiling to examine the frequency and timing of EPFs in a population of red phalaropes breeding in the Canadian high arctic. Using a technique to determine parentage without maternal DNA, we inferred that 6 of 70 chicks in 18 broods resulted from EPFs – one extrapair chick in each of 6 broods. These results were supported by a further analysis using microsatellite DNA. As predicted, broods containing EPFs hatched from clutches laid significantly later in the season than did broods containing no EPFs. The difference in median hatch dates between broods with and without EPFs was 9.0 days, or 38% of the entire egg-laying period in that season. For the whole breeding season, we estimated that 6.5% of chicks were sired by extrapair males, which is similar to extrapair paternity estimates for other sex-role-reversed birds, but relatively low compared to the majority of socially monogamous species studied so far. Received: 24 August 1998 / Received in revised form: 18 January 1999 / Accepted: 24 January 1999     

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.     

Temporal patterns in the vibratory courtship signals of the wandering spider Cupiennius salei Keys.

Summary The vibratory courtship signal generated by abdominal and leg movements of male Cupiennius salei on plants consists of impulses, which in groups of about ten form syllables. A syllable together with the preceding silent pause is called a sequence. Up to 50 sequences chained together form a series. A series together with the preceding silent period is called an interseries. A complete courtship is built up from a row of successive interseries. An additional signal produced by palpal drumming only occurs between syllables. Females respond to ca. 40% of the male signal series with a single irregular signal produced by leg oscillations and lasting for 113–1790 ms. Their response reduces the duration of the male interseries significantly from an average of 27.9 s to 20.6 s. The female signal follows a male signal series within a narrow time frame of 0.89±0.53 s. Analysis over long periods of time and of complete courtships showed the male signalling to be highly structured in the time domain and to contain many cues potentially usable by the female for both such precise timing and conspecific recognition: (1) On average, the interval between the last two syllables is significantly longer than the preceding ones. (2) During the course of a series, syllable durations increase nearly linearly from 93 ms to 123 ms. (3) The twelfth sequence (T-12) prior to the final one (T) is outstanding since here, roughly 4 s before the end of a series, the duration of sequences and pauses, the signal amplitudes and the occurrence of palpal drumming abruptly start to increase. Also, the frequencies contained in the syllables shift to higher values. (4) Between sequences T-4 and T-6 pause duration and sequence duration reach their minimum whereas the values for signal acceleration and the occurrence of palpal drumming are highest.     

Male care of infants in a siamang (Symphalangus syndactylus) population including socially monogamous and polyandrous groups

While male parental care is uncommon in mammals, siamang (Symphalangus syndactylus) males provide care for infants in the form of infant carrying. I collected behavioral data from a cohort of five wild siamang infants from early infancy until age 15–24 months to identify factors affecting male care and to assess the consequences of male care for males, females, and infants in a population including socially monogamous groups and polyandrous groups. There was substantial variation in male caring behavior. All males in polyandrous groups provided care for infants, but males in socially monogamous groups provided substantially more care than males in polyandrous groups, even when the combined effort of all males in a group was considered. These results suggest that polyandry in siamangs is unlikely to be promoted by the need for “helpers.” Infants receiving more care from males did not receive more care overall because females compensated for increases in male care by reducing their own caring effort. There was no significant relationship between indicators of male–female social bond strength and male time spent carrying infants, and the onset of male care was not associated with a change in copulation rates. Females providing more care for infants had significantly longer interbirth intervals. Male care may reduce the energetic costs of reproduction for females, permitting higher female reproductive rates.     

Seasonal polyphenism in life history traits: time costs of direct development in a butterfly

Insects with two or more generations per year will generally experience different selection regimes depending on the season, and accordingly show seasonal polyphenisms. In butterflies, seasonal polyphenism has been shown with respect to morphology, life history characteristics and behaviour. In temperate bivoltine species, the directly developing generation is more time-constrained than the diapause generation, and this may affect various life history traits such as mating propensity (time from eclosion to mating). Here, we test whether mating propensity differs between generations in Pieris napi, along with several physiological parameters, i.e. male sex pheromone synthesis, and female ovigeny index and fecundity. As predicted, individuals of the directly developing generation—who have shorter time for pupal development—are more immature at eclosion; males take longer to synthesise the male sex pheromone after eclosion and take longer to mate than diapause generation males. Females show the same physiological pattern; the directly developing females lay fewer eggs than diapausing females during the first days of their life. Nevertheless, the directly developing females mate faster after eclosion than diapausing females, indicating substantial adult time stress in this generation and possibly an adaptive value of shortening the pre-reproductive period. Our study highlights how time stress can be predictably different between generations, affecting both life history and behaviour. By analysing several life history traits simultaneously, we adopt a multi-trait approach to examining how adaptations and developmental constraints likely interplay to shape these seasonal polyphenisms.     

Underwater oviposition in a damselfly (Odonata: Coenagrionidae) favors male vigilance,and multiple mating by females

Summary Female Enallagma hageni oviposit underwater where they are inaccessible to males. I demonstrate that males guard submerged females rather than perch sites, and are behaviorally distinct from lone males at the water. In contrast to lone males, which always attempt to copulate with females presented to them, guarding males exhibit a conditional latency to remating which corresponds closely to the time required by females to oviposit a complete clutch of eggs. By ovipositing underwater, females decrease the risk that their eggs become exposed. Risks associated with submerged oviposition favor both mate guarding, and multiple, within-clutch matings by females. Both guarding mates and lone males rescue females that float on the water surface as the result of improper resurfacing. Such behavior reduces the mortality risk to females from 0.06 to 0.02 per oviposition bout. By remating between bouts, females benefit from the additional vigilance of lone males, who rescue floating females 1.4 times as often as original mates. A second consequence of multiple mating is an increase in the selective advantage of vigilance by mates. Because receptive females become scarce by early afternoon, whereas male density remains high, a male has little (3%) chance of encountering a second receptive female that day. However, he incurs a 42% risk of losing fertilizations if he abandons a mate. For male E. hageni mate guarding functions in the context of both natural and sexual selection. It insures that a mate lives to lay a complete egg clutch in addition to protecting a male's sperm investment.     

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.     

Heritability of a male character chosen by females of the field cricket,Gryllus bimaculatus

Summary Body size in the field cricket,Gryllus bimaculatus, contributes to fitness through its effects on competitive male mating success and female fecundity and is a character chosen by females at mating. If females are to benefit from preferentially mating with large males they must be able to pass on the advantages of large size to their offspring. The heritabilities of four aspects of body size were estimated by parent-offspring regression. All aspects were shown to have heritable genetic variation despite the fact that theory predicts characters which contribute to fitness should not be heritable. There may therefore be the potential for female choice in this species to be adaptive. Some possible mechanisms for the maintenance of heritable variation are discussed.