Paternity costs from polyandry compensated by increased fecundity in the hide beetle

Polyandry-induced sperm competition is assumed to impose costson males through reduced per capita paternity success. In contrast,studies focusing on the consequences of polyandry for femalesreport increased oviposition rates and fertility. For thesespecies, there is potential for the increased female fecundityassociated with polyandry to offset the costs to males of sharedpaternity. We tested this hypothesis by comparing the proportionand number of offspring sired by males mated with monandrousand polyandrous females in the hide beetle, Dermestes maculates,both for males mating with different females and for males rematingwith the same female. In 4 mating treatments, monandrous femalesmated either once or twice with the same male and polyandrousfemales mated either twice with 2 different males or thricewith 2 males (where 1 male mated twice). Polyandrous and twice-matingmonandrous females displayed greater fecundity and fertilitythan singly mating monandrous females. Moreover, males rematedto the same female had greater paternity regardless of whetherthat female mated with another male. In both polyandrous treatments,male mating order did not affect paternity success. Finally,although the proportion of eggs sired decreased if a male matedwith a polyandrous female, multiply mating females or femalesthat remated with a previous mate laid significantly more eggsand thus the actual number of eggs sired was comparable. Thus,males do not necessarily accrue a net fitness loss when matingwith polyandrous females. This may explain the absence of anyobvious defensive paternity-protection traits in hide beetlesand other species.     

The effect of female mating history on sperm precedence in the two-spot ladybird, Adalia bipunctata (Coleoptera, Coccinellidae)

Effects of two different mating regimes on sperm precedencein the two-spot ladybird, Adalia bipunctata, were studied usingthe polymorphic gene for melanism as a marker for paternity.Virgin nonmelanic females (homozygous recessive) were matedto nonmelanic male(s) and then, after laying fertilized eggs,were mated to a melanic male of known genotype. The resultsafter the two successive single matings showed a highly variabledegree of paternity of the second male. Initial multiple matingwith nonmelanic males did not alter the pattern of paternityafter the subsequent single mating with a melanic male, butit had two other effects: (1) the female showed an increasein rejection behavior, and (2) a longer copulation was requiredfor high success of the melanic male. Additional observationsin which families were reared from beetles collected in copulain the field demonstrated that sperm competition also occursunder natural conditions. The outcome of the competition wasvariable with frequent sperm mixing.     

Sperm stratification and paternity success in red flour beetles

Abstract. When females are inseminated by multiple males, male paternity success (sperm precedence) is determined by the underlying processes of sperm storage and sperm utilization. Although informative for many questions, two-male sperm competition experiments may offer limited insight into natural mating scenarios when females are likely to mate with several males. In this study, genetic markers in Tribolium castaneum are used to trace paternity for multiple sires, and to determine whether displacement of stored sperm that occurs after a third mating equally affects both previous mates, or if fertilizations are disproportionately lost by the female's most recent mate. For 20 days after triple-matings, first males retain significantly higher paternity success (relative to first male paternity in double-matings) compared with second males. These results demonstrate that when females remate before sperm mixing occurs, sperm stratification results in differential loss of sperm from the most recent mate. This study provides insight into the mechanisms underlying sperm precedence in a promiscuous mating system, and suggests that T. castaneum females could limit paternity success of particular mates by remating with more highly preferred males.     

Patterns of sperm precedence are not affected by female mating history in Drosophila melanogaster

In promiscuously mating species, there is strong selection on males to maximize their share of paternity through both defensive and offensive means. This has been most extensively examined using the Drosophila melanogaster model system. In these studies, sperm competition has been examined by mating a virgin female to two consecutive males and then determining the fertilization success of both the first male (defending, P1) and the second male (offending, P2). Recent evidence suggests that male defense may be influenced by female mating history (i.e., virgin versus nonvirgin). Here, by mating females to males with three different genotypes, we show that female mating history does not affect male defensive or offensive abilities in sperm competition. We also show that, although female lifetime fecundity was not correlated with the number of times that she mated, it was reduced by increased exposure to males. These data indicate that measures of P1 and P2 previously reported in D. melanogaster may be robust to the specific mating history of the females used in these studies.     

Genital damage in the orb-web spider Argiope bruennichi (Araneae: Araneidae) increases paternity success

The morphology of male genitalia often suggests functions besidessperm transfer that may have evolved under natural or sexualselection. In several species of sexually cannibalistic spiders,males damage their paired genitalia during mating, limitingthem to one copulation per pedipalp. Using a triple-mating experiment,we tested if genital damage in the orb-web spider Argiope bruennichiincreases male fitness either through facilitating his escapefrom an aggressive female or by obstructing the female's inseminationducts against future copulation attempts from other males. Wefound no survival advantage for males damaging their pedipalps;however, copulations into a previously used insemination ductwere significantly shorter when the previous male had left partsof his genitalia inside the insemination duct. Because copulationduration determines paternity in this species, our result suggeststhat male genital damage in A. bruennichi is sexually selected.By breaking off parts of their intromittent organs inside avirgin female, males can reduce sperm competition and therebyincrease their paternity success.     

Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy

As inbreeding is costly, it has been suggested that polyandry may evolve as a means to reduce the negative fitness consequences of mating with genetically related males. While several studies provide support for this hypothesis, evidence of pure post-copulatory mechanisms capable of biasing paternity towards genetically unrelated males is still lacking; yet these are necessary to support inbreeding avoidance models of polyandry evolution. Here we showed, by artificially inseminating a group of female guppies with an equal number of sperm from related (full-sib) and unrelated males, that sperm competition success of the former was 10 per cent lower, on average, than that of the unrelated male. The paternity bias towards unrelated males was not due to differential embryo survival, as the size of the brood produced by control females, which were artificially inseminated with the sperm of a single male, was not influenced by their relatedness with the male. Finally, we collected ovarian fluid (OF) from virgin females. Using computer-assisted sperm analysis, we found that sperm velocity, a predictor of sperm competition success in the guppy, was significantly lower when measured in a solution containing the OF from a sister as compared with that from an unrelated female. Our results suggest that sperm-OF interaction mediates sperm competition bias towards unrelated mates and highlight the role of post-copulatory mechanisms in reducing the cost of mating with relatives in polyandrous females.     

Female Remating Behavior in a Lekking Moth

In polyandrous species, male reproductive success will at least partly be determined by males' success in sperm competition. To understand the potential for post‐mating sexual selection, it is therefore important to assess the extent of female remating. In the lekking moth Achroia grisella, male mating success is strongly determined by female choice based on the attractiveness of male ultrasonic songs. Although observations have indicated that some females will remate, only little is known about the level of sperm competition. In many species, females are more likely to remate if their first mating involved an already mated male than if the first male was virgin. Potentially, this is because mated males are less well able to provide an adequate sperm supply, nutrients, or substances inhibiting female remating. This phenomenon will effectively reduce the strength of pre‐copulatory sexual selection because attractive males with high mating success will be more susceptible to sperm competition. We therefore performed an experiment designed both to provide a more precise estimate of female remating probability and simultaneously to test the hypothesis that female remating is influenced by male mating history. Overall, approximately one of five females remated with a second male. Yet, although females mated to non‐virgin males were somewhat more prone to remate, the effect of male mating history was not significant. The results revealed, however, that heavier females were more likely to remate. Furthermore, we found that females' second copulations were longer, suggesting that, in accordance with theory, males may invest more sperm in situations with an elevated risk of sperm competition.     

Pre‐ and postcopulatory sexual selection favor aggressive,young males in polyandrous groups of red junglefowl

A challenge in evolutionary biology is to understand the operation of sexual selection on males in polyandrous groups, where sexual selection occurs before and after mating. Here, we combine fine‐grained behavioral information (>41,000 interactions) with molecular parentage data to study sexual selection in replicated, age‐structured groups of polyandrous red junglefowl, Gallus gallus. Male reproductive success was determined by the number of females mated (precopulatory sexual selection) and his paternity share, which was driven by the polyandry of his female partners (postcopulatory sexual selection). Pre‐ and postcopulatory components of male reproductive success covaried positively; males with high mating success also had high paternity share. Two male phenotypes affected male pre‐ and postcopulatory performance: average aggressiveness toward rival males and age. Aggressive males mated with more females and more often with individual females, resulting in higher sexual exclusivity. Similarly, younger males mated with more females and more often with individual females, suffering less intense sperm competition than older males. Older males had a lower paternity share even allowing for their limited sexual exclusivity, indicating they may produce less competitive ejaculates. These results show that—in these populations—postcopulatory sexual selection reinforces precopulatory sexual selection, consistently promoting younger and more aggressive males.     

Determinants of paternity in a butterfly

Success in sperm competition is of fundamental importance to males, yet little is known about what factors determine paternity. Theory predicts that males producing high sperm numbers have an advantage in sperm competition. Large spermatophore size (the sperm containing package) also correlates with paternity in some species, but the relative importance of spermatophore size and sperm numbers has remained unexplored. Males of the small white butterfly, Pieris rapae (Lepidoptera: Pieridae), produce large nutritious spermatophores on their first mating. On their second mating, spermatophores are only about half the size of the first, but with almost twice the sperm number. We manipulated male mating history to examine the effect of spermatophore size and sperm numbers on male fertilization success. Overall, paternity shows either first male or, more frequently, second male sperm precedence. Previously mated males have significantly higher fertilization success in competition with males mating for the first time, strongly suggesting that high sperm number is advantageous in sperm competition. Male size also affects paternity with relatively larger males having higher fertilization success. This may indicate that spermatophore size influences paternity, because in virgin males spermatophore size correlates with male size. The paternity of an individual male is also inversely correlated with the mass of his spermatophore remains dissected out of the female. This suggests that females may influence paternity by affecting the rate of spermatophore drainage. Although the possibility of female postcopulatory choice remains to be explored, these results clearly show that males maximize their fertilization success by increasing the number of sperm in their second mating.     

Patterns of Sperm Transfer in the Golden Orb‐Weaver Nephila edulis

Sperm competition studies typically identify copulation duration as an important predictor of paternity as it may determine the quantity of sperm transferred and thus paternity success. This study explores the relationship between copulation duration, male body size, male age and sperm transfer in the golden orb‐weaving spider, Nephila edulis. Paternity in this species is strongly associated with the relative frequency and duration of copulation, which is also influenced by male size. We determined the number of sperm transferred during copulation, by performing sperm counts in both the male copulatory organs (palps) and female sperm receptacle (spermatheca) of recently mated pairs. The total number of sperm recorded (the sum in the male palps and female spermathecae) was greater for younger males than older males, but did not vary with male body size. In general, younger males transferred more sperm and a greater proportion of their sperm supplies than older males and, among these younger males, larger individuals transferred more sperm. However, there were no significant size effects for older males. More sperm was transferred with longer copulations, but in contrast with previous studies, we found that larger males copulated for longer. The rate of sperm transferred was negatively correlated with the duration of copulation, suggesting that the variation in copulation duration in N. edulis may represent strategic investment by males to alter patterns of paternity, in addition to transferring additional sperm.     

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

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

Male copulation behaviour and the risk of sperm competition

When females mate with more than one male during their reproductive cycle, males may increase their share of paternity by copulating repeatedly with the same female. Accordingly, males should mate repeatedly with the same female more frequently when the risk of sperm competition is greater. We examined this idea experimentally in the orb-web spiderNephila edulis , which is characterized by both extreme sexual size dimorphism and extreme male size variation. Comparison of the mating behaviour of solitary and pairs of males on the webs of virgin and mated females revealed that males adjust the frequency and duration of copulation according to the mating history of the female and the presence of rival males. Males copulated more frequently and for longer with virgin than mated females. The copulation behaviour of males in the presence of rivals depended upon their relative size. Typically, larger males prevented smaller rivals from gaining access to the female and therefore were able to copulate more frequently. Smaller males copulated less frequently, but for longer periods, which may have increased their share of paternity. The size of male N. edulis can vary by an order of magnitude, and our results suggest that this variation may be maintained by the alternative size-dependent strategies of preventing or winning sperm competition. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Effect of male body size on sperm precedence in the polyandrous butterfly Pieris napi L. (Lepidoptera: Pieridae)

Male Lepidoptera produce an ejaculate during copulation thatcontains both sperm and accessory gland nutrients and may functionas paternal investment and/or male mating effort Several studieshave examined how ejaculates function as paternal investment,but few have determined the influence of sperm competition onmale investment This study examines the effect of male bodysize on sperm precedence in the polyandrous butterfly Pierisnapi L. We used male body mass as an indicator of the size ofejaculate transferred and found that relative male size hada significant effect on paternity. The offspring of twice-matedfemales showed a low incidence of mixed paternity. Larger malesobtained the majority of fertilizations, and the degree of second-malesperm precedence was influenced by relative body size of matingmales. In general, second mates obtained fewer fertilizationsthe larger the size of the first mate. The interval betweenthe first and second mating was influenced by the size of thefirst male mate Females first mated to small males remated soonerthan females first mated to larger males Our results suggestthat large males may have a selective advantage over small maleswhen both a male's fertilization success and a female's refractoryperiod are influenced by the size of ejaculate transferred.Furthermore, the effect of male body size on the proportionof offspring sired lends support to the hypothesis that spermcompetition has played a major role in the evolution of ejaculatesize.     

Factors influencing paternity success in Antechinus agilis: last‐male sperm precedence,timing of mating and genetic compatibility

We describe the patterns of paternity success from laboratory mating experiments conducted in Antechinus agilis, a small size dimorphic carnivorous marsupial (males are larger than females). A previous study found last‐male sperm precedence in this species, but they were unable to sample complete litters, and did not take male size and relatedness into account. We tested whether last‐male sperm precedence regardless of male size still holds for complete litters. We explored the relationship between male mating order, male size, timing of mating and relatedness on paternity success. Females were mated with two males of different size with either the large or the small male first, with 1 day rest between the matings. Matings continued for 6 h. In these controlled conditions male size did not have a strong effect on paternity success, but mating order did. Males mating second sired 69.5% of the offspring. Within first mated males, males that mated closer to ovulation sired more offspring. To a lesser degree, variation appeared also to be caused by differences in genetic compatibility of the female and the male, where high levels of allele‐sharing resulted in lower paternity success.     

Old‐male paternity advantage is a function of accumulating sperm and last‐male precedence in a butterfly

Old‐male mating advantage has been convincingly demonstrated in Bicyclus anynana butterflies. This intriguing pattern may be explained by two alternative hypotheses: (i) an increased aggressiveness and persistence of older males during courtship, being caused by the older males' low residual reproductive value; and (ii) an active preference of females towards older males what reflects a good genes hypothesis. Against this background, we here investigate postcopulatory sexual selection by double‐mating Bicyclus anynana females to older and younger males, thus allowing for sperm competition and cryptic mate choice, and by genotyping the resulting offspring. Virgin females were mated with a younger virgin (2–3 days old) and afterwards an older virgin male (12–13 days old) or vice versa. Older males had a higher paternity success than younger ones, but only when being the second (=last) mating partner, while paternity success was equal among older and younger males when older males were the first mating partner. Older males produced larger spermatophores with much higher numbers of fertile sperm than younger males. Thus, we found no evidence for cryptic female mate choice. Rather, the findings reported here seem to result from a combination of last‐male precedence and the number of sperm transferred upon mating, both increasing paternity success.     

Sperm competition and small size advantage for males of the golden orb‐web spider Nephila edulis

Sexual selection, through female choice and/or male–male competition, has influenced the nature and direction of sexual size dimorphism in numerous species. However, few studies have examined the influence of sperm competition on size dimorphism. The orb‐web spider Nephila edulis has a polygamous mating system and extreme size dimorphism. Additionally, the frequency distribution of male body size is extremely skewed with most males being small and few large. The duration of copulation, male size and sexual cannibalism have been identified as the significant factors determining patterns of sperm precedence in spiders. In double mating trials, females were assigned to three treatments: either they mated once with both males or the first or the second male was allowed to mate twice. Paternity was strongly associated with the duration of copulation, independent of mating order. Males that were allowed to mate twice not only doubled the duration of copulation but also their paternity. Small males had a clear mating advantage, they copulated longer than large males and fertilized more eggs. Males of different sizes used different tactics to mate. Large males were more likely to mate through a hole they cut into the web, whereas small males approached the female directly. Furthermore, small males usually mated at their first attempt but large males required several attempts before mating took place. There was no obvious female reaction towards males of different sizes.     

Seasonal variation in genital and body size, sperm displacement ability, female mating rate, and male harassment in two calopterygid damselflies (Odonata: Calopterygidae)

Sperm competition is a pervasive force. One adaptation is the male ability to displace the rivals' sperm that females have stored from previous copulations. In the damselfly, Calopteryx haemorrhoidalis asturica , males with wider aedeagi displace more spermathecal sperm. The present study documents that the same mechanism operates in another damselfly, Hetaerina americana . However, this genital width in both species decreases along the season, but late-emerging females have more sperm displaced than early-emerging females. Because territorial males mated more and were larger in body and genital size than nonterritorial males, late-season females mated with considerably larger males with respect to female size and this produced higher sperm displacement. Assuming female benefits from storing sperm but that such benefit does not prevail if males displace sperm, it is predicted that, along the season, females will mate less and male harassment (in terms of male mating attempts and oviposition duration) will increase. These predictions were corroborated. In H. americana , it was also tested whether spermathecal sperm became less viable along the season. The results obtained did not corroborate this. This is the first evidence indicating that season affects sperm displacement ability and female mating frequency due to changes in male body and genital size.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 815–829.     

Copulation patterns in the golden orb-web spider Nephila madagascariensis

A consequence of multiple mating by females can be that the sperm of two or more males directly compete for the fertilisation of ova inside the female reproductive tract. Selection through sperm-competition favours males that protect their sperm against that of rivals and strategically allocate their sperm, e.g., according to the mating status of the female and the morphology of the spermatheca. In the majority of spiders, we encounter the otherwise unusual situation that females possess two independent insemination ducts, both ending in their own sperm storage organ, the spermatheca. Males have paired mating organs, but generally can only fill one spermatheca at a time. We investigated whether males of the African golden orb-web spider Nephila madagascariensis can prevent rival males from mating into the same spermatheca and whether the mating status of the female and/or the spermatheca causes differences in male mating behaviour. There was no significant difference in the duration of copulations into unused spermathecae of virgin and mated females. We found that copulations into previously inseminated spermathecae were generally possible, but shorter than copulations into the unused side of mated females or with virgins. Thus, male N. madagascariensis may have an advantage when they mate with virgins, but cannot prevent future males from mating. However, in rare instances, parts of the male genitals can completely obstruct a female genital opening.     

Females benefit from mating with different males in the scorpionfly Panorpa cognata

The adaptive significance of female polyandry has become a recurrentsubject of recent theoretical and empirical research. It hasbeen argued that in addition to direct benefits, such as nuptialgifts or an adequate sperm supply, females may gain geneticbenefits from mating with different males. Females of the scorpionflyPanorpa cognata mate with several males during their lifetime.In an experiment designed to rule out any direct nutritionalbenefit of multiple matings, I found that polyandrous femalesthat mated with two different males achieved a significantlyhigher egg-hatching success than monandrous females that matedtwice with the same male. However, individual males did nottrigger the same response in different females as the egg-hatchingsuccess of different females that mated with one and same maledid not correlate. The results, thus, do not conform to predictionsfrom hypotheses assuming that genetic benefits of polyandryare influenced by the intrinsic genetic quality of males. Theresults are, however, consistent with the genetic incompatibilityhypothesis. Nevertheless, substances from different males transferredduring copulation may synergistically affect zygote viability.Furthermore, I discuss why paternity studies can only explicitlytest the genetic incompatibility hypothesis if there are a prioriexpectations of female-male genome compatibilities.     

Effects of age and repeated mating on male sperm supply and paternity in a parasitoid wasp

Post-copulatory paternity biases after female multiple mating are major constraints on both male and female reproductive systems. The outcome of paternity in certain situations is only controlled directly by male sperm stock. This was tested experimentally in the parasitoid wasp Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), in which sperm stocks are small (several hundred) and the fertilizing efficiency of stored sperm is high (the ratio of sperm stored/fertilized eggs is about 0.75). Sperm in seminal vesicles and paternity of males of different status (virgin young, virgin old, or young previously mated) were measured after female single and double mating. The amount of sperm in the seminal vesicle differed according to male status (increasing from previously mated males to old males), but there was no difference in sperm stored by females after a single mating. In double mating experiments with two males of different status, paternity increased linearly with the relative amount of sperm in seminal vesicles. Paternity distribution conforms to 'a fair raffle' of sperm from both donors following complete mixing of sperm prior to fertilization. Thus, in a female multiple mating context, male fitness depends principally on their sperm stock, which in turn depends on life history parameters, such as age and previous mating.