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.     

Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion

The growing molecular evidence that females of many species mate with several males calls for a critical reassessment of the selective forces which act to shape female mating tactics. In natural populations of the harlequin-beetle-riding pseudoscorpion, Cordylochernes scorpioides, females are polyandrous and typically produce mixed-paternity broods. Laboratory behavioral analyses and breeding experiments indicate that polyandry in this pseudoscorpion is an active strategy which increases female reproductive success. Females restricted to mating with a single male experienced a higher rate of embryo failure and produced significantly fewer offspring than either females mated to more than one male in the laboratory or females naturally inseminated in the field. Forced copulation, insufficient sperm from a single mating, male nutrient donations and variation in inherent male genetic quality cannot explain the greater number of nymphs hatched by polyandrous females in this study. Evidence suggests that, by mating with several males, C. scorpioides females may exploit postcopulatory mechanisms for reducing the risk and/or cost of embryo failure resulting from fertilization by genetically incompatible sperm. Received: 5 May 1996 / Accepted after revision: 16 October 1996     

Influence of alternate reproductive tactics and pre- and postcopulatory sexual selection on paternity and offspring performance in a lizard

Sexual selection theory predicts different optima for multiple mating in males and females. We used mating experiments and genetic paternity testing to disentangle pre- and postcopulatory mechanisms of sexual selection and alternate reproductive tactics in the highly promiscuous lizard Eulamprus heatwolei. Both sexes mated multiply: 30–60 % of clutches were sired by two to four fathers, depending on the experiment. Larger males sired more offspring when we allowed male contest competition: 52 % of large males but only 14 % of small males sired at least one offspring. In the absence of male contest competition, females mated promiscuously and there was no large male advantage: 80 % of large males and 90 % of small males sired at least one offspring, and there was no evidence for last-male precedence. Multiple mating did not yield obvious direct or indirect benefits to females. E. heatwolei represents a complex system in which males attempt to improve their fertility success by limiting rivals from access to females and through adopting alternate reproductive tactics. Conversely, females exhibit no obvious precopulatory mate choice but may influence fitness through postcopulatory means by either promoting sperm competition or through cryptic female choice. Our results support the hypothesis that female multiple mating in nonavian reptiles is best explained by the combined effect of mate encounter frequency and high benefits to males but low costs 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.     

Trade-off between pre- and postcopulatory sexual cannibalism in a wolf spider (Araneae,Lycosidae)

Sexual cannibalism can occur before, during or after mating. Relatively few experimental studies have examined why there is variation in the timing of sexual cannibalism. We examined the latency and number of attacks required for female spiders to capture male spiders pre- vs. postcopulation. We also examined the effects of female mating status and hunger level on the occurrence of pre- and postcopulatory cannibalism, which reflects the contribution of both relative capture success and female motivation to cannibalize males. Precopulatory cannibalism occurred after a shorter interval and required fewer chases and physical interactions for the female to successfully capture the male than was the case for postcopulatory cannibalism. Virgin females were more likely to engage in postcopulatory rather than precopulatory cannibalism and mated females vice versa. Those virgin females that did engage in precopulatory cannibalism had significantly lower body condition than virgin females engaging in postcopulatory cannibalism. While precopulatory cannibalism occurred more quickly and required fewer attacks by females, it comes at a potential cost of not mating with males. Hence, females are more likely to engage in precopulatory cannibalism if they have already mated or, if virgins, if they have low body condition. These results indicate that the decision of when to cannibalize males is dynamic and depends upon the relative value of a male as a mate versus a meal.     

Sperm competition as a mechanism of female choice in the field cricket,Gryllus bimaculatus

Summary While traditionally viewed as an extension of intermale competition, mechanisms of sperm competition may be used by multiply mating females for mate choice. In the field cricket G. bimaculatus sperm were shown to mix in the spermatheca. The proportion of offspring sired by the second male increased with spermatophore attachment duration and, therefore, the number of sperm transferred. There was no second male advantage for single matings after an initial double mating. However, the proportion ofoffspring sired by the second male increased in proportion to the number of times he mated such that second males mating three times after an initial double mating had the advantage at fertilization. The data suggested that sperm were utilized in proportion to their numerical representation in the spermatheca. The mechanism of sperm precedence may, therefore, be one of sperm dilution. Female G. bimaculatus may control the degree of sperm competition as a mechanism of mate choice. By accepting large quantities of sperm from chosen males they may determine the paternity of their offspring by diluting out the sperm stored from previous matings.     

Should he stay or should he go: male influence on offspring sex ratio via postcopulatory attendance

In species without nuptial gifts or parental care, postcopulatory attendance of females by males has generally been interpreted as males guarding against sperm competition. Guarding benefits may be concurrent with attendance (the guarding-now hypothesis), or male behavior during attendance may make the female unreceptive (the guarding in absentia hypothesis). However, in addition to guarding functions, attendance may provide the male with an opportunity to influence the female's use of sperm. In haplodiploids such as hymenopterans, doing so may be beneficial because only daughters and not sons are produced sexually and so influence male reproductive success (the sex ratio hypothesis). In the parasitoid wasp Urolepis rufipes, postcopulatory attendance involved the male remaining mounted after copulation and resuming courtship. Support for the guarding-now hypothesis was limited. A male's presence on a female did not reduce the probability, or quickness, of another male mounting, and second-mounted males frequently copulated. The guarding in absentia hypothesis was not supported. Females became unreceptive soon after mating even when copulation and postcopulatory attendance were experimentally prevented. The sex ratio hypothesis was supported. Postcopulatory attendance caused females to produce more daughters. They also produced more total offspring. Thus, a male should stay and should not go even in the absence of other males, at least when opportunities for other matings are absent as in the present study. Although most studies of offspring sex ratios have focused on maternal control, this study provides an example of apparently adaptive male influence on sex ratio.     

Determinants of paternity in the milkweed leaf beetle

Summary Males and females of the milkweed leaf beetle mate for up to 2.5 d in the field; copulation is interspersed with mounted courtship behavior and periods of passive riding on the female's back. In 1985, females mated with up to 10 different males in Bridgeport, New York, and matings averaged 0.75±0.04 (SE) d in duration. Sperm utilization patterns are complex in the milkweed leaf beetle. In the laboratory, mating duration, mating order and the duration of the gap between matings affected paternity. The second male's sperm predominated when a female's two consecutive matings were of equal duration (but were long: 45 h each) or when they were intermediate in duration (15 h each) with a 5 day gap between the two matings. The mechanism of sperm predominance appears to be one of time-dependent sperm removal and replacement. Neither relative nor absolute size of males affected the extent to which they superceded the sperm of rivals. Electrophoretic analysis of paternity at 6 polymorphic loci showed that offspring of at least eight out of 11 mating pairs pairs collected in the field at the end of the 1984 breeding season were sired by more than one male. At least seven of the 11 families produced some offspring that were sired by the female's most recent mate in the field and in no case was the collected male completely excluded from paternity. In a greenhouse plot, males climbed off females' backs a mean of 1.1±0.3 h before oviposition. Females did not oviposit with males on their backs and did not oviposit sooner when males were removed than when males were allowed to remain mounted, indicating that males don't keep females from ovipositing until they can achieve sperm predominance. The close concordance between male disembarkment and oviposition suggests that males remain with females beyond the time when they have superceded the sperm of their prior mates, possibly to guard them from rival males. Although the prolonged mating association of the milkweed leaf beetle cannot be separated into discrete copulatory and guarding phases, the results of this study suggest that prolonged mating enables males both to remove and replace the sperm of the females' prior mates with their own sperm and to prevent females from remating prior to oviposition.     

The effects of age and relatedness on mating patterns in thornbug treehoppers: inbreeding avoidance or inbreeding tolerance?

The social environment of many species includes synchronous maturation of siblings in family groups, followed by limited dispersal of adults from their natal site. Under these conditions, females may experience high encounter rates with same-age siblings during mate searching, increasing their risk of inbreeding. If inbreeding depression occurs, mating with a sibling is often considered maladaptive; however, in some contexts, the inclusive fitness benefits of inbreeding may outweigh the costs, favoring females that tolerate some level of inbreeding depression. We evaluated mating patterns in the treehopper Umbonia crassicornis, a semelparous species in which females encounter same-age siblings during mate searching. A female U. crassicornis that mates with a brother suffers from inbreeding depression. We used a free-choice mating design that offered females simultaneous mating opportunities with three groups of males: siblings, same-age nonsiblings, and older nonsiblings. These groups represent the types of males typically encountered by females during mate searching. Our goal was to assess whether mating patterns were influenced by inbreeding avoidance by evaluating two hypotheses: kin discrimination and age-based mating (older males cannot be siblings in this species). There was no difference in the proportions of females mating with siblings vs nonsiblings, suggesting an absence of kin discrimination. However, females mated with a greater proportion of older vs younger males. Given that females do not avoid siblings as mates despite a cost to inbreeding, our results provide a possible example of inbreeding tolerance. We also discuss some factors that may have contributed to the mating advantage of older males.     

Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (<Emphasis Type="Italic">Microcebus murinus</Emphasis>)

Sex-specific interests over the maximization of reproductive success lead to an inter-sexual conflict over the optimal mating system in a species. Traditionally, the outcome of this inter-sexual conflict has been studied from the male perspective but it also depends on female mating strategies, such as manipulating the temporal distribution of sexual activity, advertisement, and mate choice. We used a small nocturnal primate, the gray mouse lemur (Microcebus murinus) to determine the relative importance of female mating strategies on the outcome of this conflict in a species where females are solitary during their activity period. We studied their mating behavior over three consecutive annual mating seasons and determined the genetic relationships among more than 300 study animals to quantify individual reproductive success. We found that most females were receptive asynchronously. Females did not exhibit any obvious direct mate choice, probably due to a highly male-biased operational sex ratio and the corresponding costs of choosiness. However, females exercised indirect choice for multiple matings. They mated with 1–7 males up to 11 times during their single night of receptivity. As a result, mixed paternity was common but heavier males sired more offspring, meaning that indirect female choice for superior males cannot be excluded. Females exhibited a mixed mating strategy, avoiding costly direct mate choice but still counteracting male efforts to monopolize mating, successfully increasing genetic variability among offspring. Thus, females had a major influence on the outcome of the inter-sexual conflict despite male monopolization attempts.Communicated by J. Setchell     

Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus)

In a wide variety of species, male reproductive success is determined by contest for access to females. Among multi-male primate groups, however, factors in addition to male competitive ability may also influence paternity outcome, although their exact nature and force is still largely unclear. Here, we have investigated in a group of free-ranging Barbary macaques whether paternity is determined on the pre- or postcopulatory level and how male competitive ability and female direct mate choice during the female fertile phase are related to male reproductive success. Behavioural observations were combined with faecal hormone analysis for timing of the fertile phase (13 cycles, 8 females) and genetic paternity analysis (n = 12). During the fertile phase, complete monopolisation of females did not occur. Females were consorted for only 49% of observation time, and all females had ejaculatory copulations with several males. Thus, in all cases, paternity was determined on the postcopulatory level. More than 80% of infants were sired by high-ranking males, and this reproductive skew was related to both, male competitive ability and female direct mate choice as high-ranking males spent more time in consort with females than low-ranking males, and females solicited copulations mainly from dominant males. As most ejaculatory copulations were female-initiated, female direct mate choice appeared to have the highest impact on male reproductive success. However, female preference was not directly translated into paternity, as fathers were not preferred over non-fathers in terms of solicitation, consortship and mating behaviour. Collectively, our data show that in the Barbary macaque, both sexes significantly influence male mating success, but that sperm of several males generally compete within the female reproductive tract and that therefore paternity is determined by mechanisms operating at the postcopulatory level.     

Polyandry and paternity in a wild population of the swordtail Xiphophorus nigrensis

Genetic analyses of parentage provide crucial information about the prevalence of polyandry and the potential for sexual selection to operate in wild populations. In the swordtail Xiphophorus nigrensis, large males are thought to have a competitive advantage due to their superiority in male–male contests and attractiveness to females, who are presumed to mate multiply. I examined the distribution of paternity within broods, the relationship between male body size and paternity and the effect of sire number on fecundity from females collected in the field. Sixty-one percent of females produced offspring from two to four males, with 70% of the offspring typically sired by one of the males represented in the brood. Male body size did not affect paternity share or whether females were multiply mated, as predicted if precopulatory sexual selection has a strong effect on the outcome of postcopulatory sexual selection. Female fecundity increased with the number of sires; however, this relationship was not observed when the smallest broods, where multiple mating is more difficult to detect, were excluded from the analysis. The high levels of multiple paternity and reproductive skew suggest that postcopulatory sexual selection has important evolutionary consequences in X. nigrensis. Traits important in precopulatory sexual selection, such as male body size, however, are more likely to affect sexual selection by increasing the number of mates obtained rather than paternity share within broods.     

Sperm competition and the level of polyandry in a bushcricket with large nuptial gifts

Variation in paternity due to sperm competition or post-copulatory female choice has a major influence on animal mating system evolution and on the levels of genetic variability in natural populations. However, there are relatively few studies comparing the outcome of sperm-competition experiments in the laboratory with natural variation in polyandry among families from the field. In the bushcricket Ephippiger ephippiger, females mate multiply, and the males provide them with a large, nutritious, and probably expensive, donation at mating. We examined paternity in a series of laboratory matings, where females mated with two males, and amongst a series of families collected from a natural population. In the laboratory, paternity was highly bimodally distributed: 24% of families had offspring fathered by the first male to mate, 68% by the second male (in only 8% was paternity shared). In the field, paternity was more mixed: only 27% of families had a single father, 14% had more than two fathers, whilst 59% had two fathers. While unsuccessful matings may contribute to the highly biased paternity in the laboratory, they cannot fully explain the high incidence of complete P2 families. Nonrandom sperm utilisation is therefore likely. Greater sperm mixing in the field probably results from females mating with more males, but the distribution of paternity also reflects an active process of nonrandom sperm utilisation. Confidence of paternity due to last male advantage may be relatively high in this species, and therefore may have facilitated the evolution of the large spermatophore in E. ephippiger.Communicated by D. Gwynne     

Prior encounters with the opposite sex affect male and female mating behavior in a wolf spider (Araneae,Lycosidae)

Mate availability can vary widely in nature depending upon population density and sex ratio and can affect the ability of individuals to be selective in mate choice. We tested the effects of prior encounters with the opposite sex (i.e., exposure to the opposite sex either with or without mating) on subsequent mating behavior in two experiments that manipulated mate availability for both males and females in the wolf spider, Hogna helluo. The probability of mating in the experimental trial depended upon whether the prior encounter involved mating or not, and males and females responded in opposite directions. Exposure without mating resulted in a higher subsequent frequency of mating for females and a lower subsequent frequency of mating for males, while prior mating experience resulted in a lower frequency of female remating and a higher frequency of male remating. Prior exposure without mating did not affect female aggression. However, mated females engaged in precopulatory cannibalism more frequently than virgins. Mated males escaped postcopulatory cannibalism more frequently than virgins. Our results show that males respond to exposure without mating in the expected manner. However, prior mating (1 week earlier) had unexpected effects on males, which may be due to mated males being of higher quality. There were little or no effects of the size of the prior exposure individual or mate on subsequent mating behaviors. Further research is needed to determine why different species use different degrees of prior information in mate choice.     

Mate choice in the face of both inbreeding and outbreeding depression in the intertidal copepod Tigriopus californicus

 In species vulnerable to both inbreeding and outbreeding depression, individuals might be expected to choose mates at intermediate levels of genetic relatedness. Previous work on the intertidal copepod Tigriopus californicus has repeatedly shown that crosses between populations result in either no effect or hybrid vigor in the first generation, and hybrid breakdown in the second generation. Previous work also shows that mating between full siblings results in inbreeding depression. The present study again found inbreeding depression, with full sibling mating causing significant fitness declines in two of the three populations assayed. In the mate choice assays, a single female was combined with two males. Despite the costs of both inbreeding and outbreeding, mate choice showed clear inbreeding avoidance but no clear pattern of outbreeding avoidance. This lack of outbreeding avoidance may be attributed either to the temporary increase in fitness in the F₁ generation or to the absence of selection for premating isolation in wholly allopatric populations with infrequent migration. If this inability to avoid unwise matings is common to other taxa, it may contribute to the problem of outbreeding depression when allopatric populations are mixed together. Received: 18 May 1999 / Accepted: 25 January 2000     

Factors influencing paternity in multiply mated female red-sided garter snakes and the persistent use of sperm stored over winter

In some species, sperm is stored within the female reproductive tract for months to years, and yet remains viable to fertilize eggs and produce offspring. Female red-sided garter snakes store sperm for over 7 months of winter dormancy. In previous work, we demonstrated that these stored sperm account for an average of 25 % paternity of a litter when the female mates with a male at spring emergence. Here, we tested whether last-male sperm precedence was prevalent when a female mates with two males during the spring. On average, paternity was shared equally among the first (P₁ proportion of paternity of the first male to mate) and second males (P₂) to mate in the spring, and stored sperm (P_ss), but the variance in paternity was high. Thus, last male sperm precedence may diminish when a female has more than two mates. Male size did not affect paternity, but, as the interval between matings increased, P₁ increased at the expense of P_ss. Interestingly, as the second spring male’s copulation duration increased, P₁ also increased at the expense of P₂. This result suggests that female influence over sperm and/or copulatory plug transfer during matings may also affect which male fathers her offspring in response to coercive matings as we assisted females to mate for their second mating. Finally, all females were spring “virgins”; consequently, sperm stored from autumn matings (and/or previous spring matings) remain competitive even when faced with two rivals in sperm competition and is likely the driver of the evolution of sperm longevity.     

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.     

Multiple mating in the ant Acromyrmex versicolor: a case of female control

In eusocial insects, polyandrous mating has the potential to reduce genetic relatedness of individuals within a colony, which may have a profound effect on the stability and social structure of the colony. Here we present evidence that multiple mating is common in both males and females of the desert leaf-cutter ant Acromyrmex versicolor. Females seem to have complete control over the number of matings, and mate on average with three males, even though the sperm transferred in a single copulation is sufficient to fill the spermatheca. To determine whether there is a bias in the representation of sperm from different mates in the spermatheca, females were mated to three or four males in controlled mating experiments and were subsequently allowed to found colonies in the laboratory. Paternity analysis of the offspring by random amplified polymorphic DNA analysis showed that all males that have been mated to a female successfully contributed sperm to the production of her offspring. No significant asymmetry in sperm use was detected, suggesting complete sperm mixing. Different hypotheses to explain polyandrous mating are discussed, and it is argued that the best hypothesis to explain polyandrous mating and complete sperm mixing in A. versicolor is that utilizing genetically diverse sperm confers a selective advantage on females. Received: 14 June 1995/Accepted after revision: 26 November 1995     

Determinants of paternity success in the spider Pholcus phalangioides (Pholcidae: Araneae): the role of male and female mating behaviour

In double mating experiments, we examined whether and to what extent various male and female behavioural traits influence the course of mating and fertilization success in the cellar spider. In males, we focussed on pre-copulatory behaviour and on the rhythmic twisting movements that the male performs with his pedipalps during copulation. In females, we investigated remating decisions and the effect of female termination of copulation. Second males fertilized a high proportion of the eggs (P ₂: median 89%) despite much shorter second matings, with high variation in relative paternity success. The number of pedipalp movements (PPMs) of either male was a better predictor of paternity than copulation duration. Our results suggest that in second matings, PPMs help to remove sperm from previous males, whereas in first matings a high number of PPMs enhances fertilization success, either due to numerical sperm competition or cryptic female choice. Furthermore, we found a negative male age effect on paternity in second matings, implying that age-related deterioration of spermatozoa may promote variation in fertilization success. Female receptivity decreased significantly in second matings; only 70% of the females remated. Females that accepted a second copulation were found to terminate these much earlier and with higher probability than first matings. This suggests that the intensity of conflict between the sexes is higher in second matings. Increased intensity of sexual conflict may be responsible for stronger selection on male traits, as pre-copulatory behaviour and age only affected male copulatory performance and paternity in second matings. Electronic Publication     

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.