Male insemination decisions and sperm quality influence paternity in the golden orb-weaving spider

In polyandrous species, paternity may be influenced by the timingand frequency of mating. Female spiders possess 2 genital openingsthat lead to separate sperm-storage structures. Thus, even whenmating with a previously mated female, a male may reduce directsperm competition by inseminating the opposite opening to herfirst mate. Such morphology may provide females with greatercontrol over paternity. We examined simultaneously whether malesavoided already inseminated female genital openings and whetherthis behavior varied with the time between successive matings.To explore these questions, we mated female golden orb weaverspiders, Nephila edulis, each to 2 males and manipulated thetiming of their second mating. We documented male inseminationpatterns and explored the influence of male mating decisionson paternity success using the irradiated male technique. Wefound that 60% of males avoided sperm competition by discriminatingagainst inseminated genital openings. Moreover, male matingbehavior had a dramatic impact on the paternity success of irradiatedmales. When males inseminated the same genital opening, thecompetitive ability of the irradiated male's sperm was dramaticallyreduced resulting in lower paternity success. In contrast, whenthe 2 males inseminated opposite genital openings both malessired equal proportions of offspring regardless of their radiationstatus. There was no evidence that the timing of the secondmating affected patterns of paternity. Our data suggest thatdifferences in sperm quality may influence paternity successof N. edulis males under a sperm-competitive scenario. In contrast,females appear to have limited postmating control over paternity.     

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.     

Polygynandry in a red fox population: implications for the evolution of group living in canids?

Canid social groups are typically thought to consist of extendedfamilies, that is, a dominant breeding pair and related nonbreedingsubordinates, that principally obtain indirect fitness benefitsfrom helping to raise the offspring of the dominant pair. Consequently,the monogamous pair has been viewed as the basic fundamentalunit of canid social organization. However, there have beenfew genetic studies that have tested this assumption. We analyzedthe parentage of red foxes (Vulpes vulpes) in a high-density(19.6–27.7 adult foxes/km²) population in Bristol, UK,to determine (1) whether groups typically produced a singlelitter of cubs annually and (2) whether male and female foxesexhibited monogamous mating strategies. Social monogamy (theproduction of one litter in a social group) was observed orassumed in 54% of breeding attempts (N = 13 group-years). However,polyandrous and polygynous patterns of mating were common. Multiplepaternity was confirmed in 38% of litters (N = 16) containingoffspring with resolved maternity and paternity (N = 30 cubs);when including cubs with unresolved paternity (N = 20), multiple-paternitymay have occurred in 69% of litters. Litters were sired by anaverage of 1.6 identified males (range = 1–4); when includingcubs with unresolved paternity, litters may have been siredby up to seven males. Only 20% (6/30) of cubs with resolvedmaternity and paternity were sired by males within the socialgroup. Within groups, dominant females did not breed with subordinatemales; dominant males did breed with subordinate females. Dominantand subordinate females both produced cubs with dominant andsubordinate males from other social groups. Mean adult relatednessin groups typically ranged from 0.15–0.35, indicativeof second-order rather than first-order relatives.     

Mating system of the meadow vole, Microtus pennsylvanicus

Previous studies on parental and spacing behavior of Microtuspennsylvanicus suggest a promiscuous mating system, but attemptsto find multiple paternity in single litters have been unsuccessful.In this paper we present evidence of multiple paternity in singlelitters conceived in the wild early in the breeding season.The proportion of litters sired by multiple males was estimated,by a conservative method, to be 33.1%.We argue that the presenceof promiscuity, rather than polygyny, in M. pennsylvanicus isthe result of two factors. First, overwintered breeding malesare similar in age and size, resulting in small variation incompetitive ability among males. This reduced variation in competitiveability reduces the possibility that some males defend severalfemales and others defend none. Second, the habitat structureof the meadow vole makes it difficult for a male to detect othermales nearby, and this reduces the possibility that one maleexcludes others from mating when a female comes into estrus.     

The Conflict between Nest Guarding and Mate Guarding in Penduline Tits (Remiz pendulinus)

In penduline tits (Remiz pendulinus), polygynous males build several very elaborate nests successively during one breeding season to attract females. The time and effort invested in nest building is positively related to their mating success. Intraspecific competition for nest material resulting in nest material theft, delays males' nest building progress which in turn decreases their mating success. Therefore, a nest guarding strategy was predicted. In many bird species, males develop some kind of paternity strategy during the female fertile phase. However, as nest building and the female fertile phase frequently coincide, one would expect a trade-off between these strategies. In this study we determined in particular how nest guarding in males conflicts with their mate guarding behaviour in penduline tits. Our results show that nest building is costly in terms of a male's time budget. Thieves benefit by increasing their rate of acquiring nest material which reduces the effort invested in nest building. Nest guarding is an efficient strategy to avoid thieves, as indicated by the negative relation between the presence of the male near the nest and the frequency of nest material theft. Nest guarding is required for the whole building period but males, however, increased their mate guarding effort during the peak fertile phase to ensure their paternity. The data suggest that, for the trade-off “mate guarding versus nest guarding”, paternity insurance seems to be more important.     

Paternity Recognition in Multi-male Primate Groups

A traditional view of multi-male primate groups has held thatmales provide relatively little direct care to infants, possiblyas a result of low confidence of paternity associated with arelatively promiscuous breeding system. In the last five yearsthis view has changed as a result of a careful documentationof intimate male-infant affiliations in certain species, especiallythe savanna-dwelling baboons (Papio spp.). The occurrence ofthese affiliations raises the question as to whether males carefor their own offspring preferentially and, if so, on what basismale confidence of paternity is mediated. Recent field studiesof baboons suggest that male-infant relationships are mediatedthrough affiliations between the males and the infants' mothers,but the degree to which these male-female affiliations are basedon prior mating experience (hence, paternity) has not been established. Comparative studies of male-infant relations in primates havegiven little attention to the variation in the intensity andform of male care patterns within the set of species that havea multi-male social organization. Among multi-male species,male care of young is reported most often in baboons and barbarymacaques (Macaca sylvanus) and least often in other macaques,chimpanzees (Pan troglodytes), and vervet monkeys (Cercopithecus).This interspecific variation may result both from differencesin the importance of male care to infant survival and from differencesin male confidence of paternity, which in turn may relate toseasonal breeding patterns and, in particular, to the presenceor absence of conspicuous signs of ovulation in females.     

Extrapair paternity as a cost of polygyny in the rock sparrow: behavioural and genetic evidence of the ‘trade-off’ hypothesis

We studied the association between extrapair paternity (EPP) rate and male mating status in the rock sparrow, Petronia petronia, a facultative polygynous species. Overall, 32.0% (58/181) of the chicks were not sired by the social father and 57.1% (24/42) of the broods contained at least one extrapair young. Polygynous males allocated less time to guarding their mate during her fertile period than monogamous males but did not differ in the time spent guarding their nest. Polygynous males were cuckolded more frequently than monogamous males (50.5 and 6.6% of the young, respectively) and their paternity loss was positively correlated with the degree of overlap between the fertile periods of their primary and secondary females. Paternity loss did not differ between primary and secondary broods of polygynous males and acquiring a second mate was possible only at the expense of paternity in both broods. Late broods contained fewer extrapair young, despite no significant seasonal trend in the time allocated by the male to guarding his mate. Male yellow badge size was not associated with paternity. Old males were cuckolded less frequently than first-year males, but male age had a minor effect on paternity compared with male mating status. Reproductive success (number of young fledged/year) did not differ between monogamous and polygynous males once paternity was accounted for. Together, these results suggest that mate guarding can be efficient in preventing cuckoldry, and that there is a trade-off between attracting an additional mate and protecting paternity in the rock sparrow, whereas male age and phenotype were, at best, fair predictors of paternity. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

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.     

Nonlocal male mountain white-crowned sparrows have lower paternity and higher parasite loads than males singing local dialect

Bird song often varies geographically, and when this geographicvariation has distinct boundaries, the shared song types arereferred to as song dialects. We investigated the role of songdialect in male mating success in a wild breeding populationof mountain white-crowned sparrows (Zonotrichia leucophrysoriantha). In 2 of 3 years, males singing unusual songs ("nonlocal"males) had lower total fertilization success (measured by microsatellitepaternity analysis) than did males singing the local dialect ("local" males). Similarly, females produced disproportionately more young with local than with nonlocal males. However, dialectwas not a significant predictor of male mating success whencontrolling for other factors that might affect paternity.Instead, the low mating success of nonlocal males was apparentlydue to an interaction between song dialect and parasite load.Nonlocal males were more severely infected by bloodborne Haemoproteusthan were local males, although they did not differ in anyother measured aspect of quality. Immigrant birds may be immunologically disadvantaged, possibly due to a lack of previous experiencewith the local parasite fauna, resulting in low mating success.     

No evidence for increased offspring heterozygosity from extrapair mating in the reed bunting (Emberiza schoeniclus)

It has been hypothesized that females mate multiply to increasethe heterozygosity of their progeny because heterozygous individualsare assumed to have a fitness advantage. Females can maximizeheterozygosity of their offspring by mating with geneticallyunrelated and/or heterozygous males. We tested these predictionsin a socially monogamous passerine, the reed bunting (Emberizaschoeniclus), where extrapair paternity occurs frequently. Theresults based on genotypes at nine microsatellite loci revealedthat females were no less genetically related to the extrapairmale(s) (EPMs) than to their pair male (i.e., breeding partner)and that EPMs were no more heterozygous than the males theycuckolded. In addition, a direct comparison of maternal half-siblingsnaturally raised in the same brood showed that extrapair youngwere no more heterozygous than within-pair young. Thus, femalereed buntings do not seem to mate with EPMs to increase offspringheterozygosity. It is not yet known whether extrapair matinginvolves any benefits at all to females in this species.     

Frass clearing by male pine engraver beetles (Ips pini; Scolytidae): paternal care or paternity assurance

Male parental care and paternity assurance are often associatedwith long-duration pair bonds. The mating system of the pineengraver beetle, Ips pini, includes an association between themale and female that persists for most of the prolonged oppositionperiod. The male beetles remove frass that arnmmlatn as thefemales lay their eggs in die phloem tissue of the host tree.Experiments and field observations were done to test possiblebenefits to males that stay in the galleries removing frasswhile die females are ovipositing. Two hypotheses were thatclearing frass (1) provides some form of care that results inmore offspring being produced and (2) is part of a paternityassurance mechanism. Male removal experiments in the field producedno evidence that male presence significantly influenced anyof five measures of offspring production. Laboratory experimentsin which virgin females were bred reciprocally to sterile andfertile males showed that, while there is no strong patternof last-male pr, last-male paternity does increase over time.Field observations revealed that female pine engravers oftencarry sperm from previous maringi when they solicit entry toa male's breeding gallery. The pattern of paternity and thefemale's sperm storage capacity suggest that males must maintainprolonged mating access to females in order to ensure high paternity.Hence, frass clearing is necessary to maximize paternity     

Do male paternity guards ensure female fidelity in a duetting fairy-wren?

Most socially monogamous bird species engage in extra-pair mating,and consequently males may adopt various behavioral strategiesto guard paternity. However, the relationship between mate guardingand extra-pair paternity is unclear: low levels of extra-pairpaternity can be associated either with no mate guarding orwith intense mate guarding. We investigate paternity guardsin the purple-crowned fairy-wren (Malurus coronatus), a duettingspecies where extra-pair paternity is rare. This species isunusual in a genus known for extremely high levels of extra-pairmating. We examine the behavioral interactions between the sexesunderlying these low rates of extra-pair paternity and showthat male purple-crowned fairy-wrens do not use frequent copulationor courtship feeding to assure paternity or guard females acousticallyby duetting. Males maintain close proximity to females bothwhen they are fertile and when they are not breeding and donot invest in courtship displays to extra-pair females. Consistentwith predictions of theoretical models, low extra-pair paternityin this species may be related to female fidelity rather thanmale paternity assurance strategies, but short-term removalof males would be necessary to test this experimentally.     

Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon)

We used data collected over 3 years at two study sites to quantifythe rates and consequences of multiple paternity and to determinethe opportunity for selection on male and female northern watersnakes (Nerodia sipedon). We sampled litters from 45 femalesthat gave birth to 811 offspring. Using eight microsatelliteDNA loci (probability of exclusion of nonparental males >0.99), we assigned paternity to 93% of neonates from one studypopulation and 69% of neonates from the other population. Observationsof participation in mating aggregations predicted individual reproductive success poorly for two reasons. First, males regularlycourted nonreproductive females. Second, more than half ofall sexually mature males obtained no reproductive successeach year, despite the fact that many of them participatedin mating aggregations. The number of sires per litter ranged from one to five, with 58% of all litters sired by more thanone male. Multiple paternity increased with female size, apparentlyboth because bigger females mated with more males and becausethe larger litters of big females provide paternity opportunitiesto more males. Multiple paternity was also more prevalent inyears with shorter mating seasons. We detected no advantage to multiple paternity in reducing either the number of unfertilizedovules or stillborn young. Despite the majority of males siringno young each year, some males fathered young with as manyas three different females in one year. Male reproductive successincreased by more than 10 offspring for each additional mate,whereas female success increased by fewer than 2 offspring foreach additional mate. The opportunity for sexual selectionwas more than five times higher in males than females.     

Does paternity or paternal investment determine the level of paternal care and does female choice explain egg stealing in the fifteen-spined stickleback?

An earlier field study on the fifteen-spined stickleback (Spinachia spinachia) showed that frequent male—male interactionsresult in high frequencies of sneaking and egg stealing. Moreover,sneaking behavior was performed not only by males adoptingalternative mating strategies, but also by males with theirown nests. The advantage of sneaking is easily understood, but it is more difficult to explain the evolutionary benefitof stealing eggs from other males. I investigated whether malessuffering from sneaking adjust their paternal effort in relationto their degree of paternity. I also examined whether femalesprefer males that have more eggs in their nests, as this couldexplain egg stealing. There was no relationship between thedegree of paternity and fanning activity, hatching success,or nest defense. However, the older the eggs become, the morethe males increase their attack rate toward potential egg predators(goldsinny wrasse and shore crabs). Thus, males adjusted theirlevel of defense to the amount of energy and time already investedin the clutch. Females did not prefer males with more eggs intheir nests. On the contrary, females preferred males withreduced clutches over males with enlarged clutches. Therefore,female choice is unlikely to be a driving force behind eggstealing in this species.     

Determinants of reproductive success across sequential episodes of sexual selection in a firefly

Because females often mate with multiple males, it is critical to expand our view of sexual selection to encompass pre-, peri- and post-copulatory episodes to understand how selection drives trait evolution. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, but previous work has shown that male paternity success is negatively correlated with flash attractiveness. Here, we experimentally manipulated both the attractiveness of the courtship signal visible to female Photinus greeni fireflies before mating and male nuptial gift size to determine how these traits might each influence mate acceptance and paternity share. We also measured pericopulatory behaviours to examine their influence on male reproductive success. Firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. We found no effect of courtship signal attractiveness or pericopulatory behaviour on male reproductive success. Taken together with previous results, this suggests a possible trade-off for males between producing an attractive courtship signal and investing in nuptial gifts. By integrating multiple episodes of sexual selection, this study extends our understanding of sexual selection in Photinus fireflies and provides insight into the evolution of male traits in other polyandrous species.     

Trade-off between pre and post-copulatory traits depends on locomotor activity in male Tribolium castaneum beetles

Locomotor performance is an indicator of dynamic exercise; thus, it is a central trait in many animal behaviours. Although higher locomotor endurance may increase male reproductive success (e.g., in mate searching and male–male contests), investment in other male reproductive traits (e.g., male attractiveness and sperm competition) may be decreased through energy consumption due to higher activity levels. Here, I investigated male attractiveness, mating success, and paternity success using males of the red flour beetle Tribolium castaneum selected for higher (H) and lower (L) locomotor endurance. Although there was no difference in male attractiveness between the selection regimes, H males had significantly higher mating success than L males. Conversely, L males had significantly higher paternity success than H males. Therefore, there was a trade-off between mating success and paternity success among the selection regimes, suggesting that locomotor endurance affects male reproduction in T. castaneum, and individual variation of locomotor endurance may be maintained within a population.     

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.     

Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus)

In socially monogamous species, extra-pair paternity can increase the variance in reproductive success and thereby the potential for sexual selection on male ornaments. We studied whether male secondary sexual ornaments are selected through within- and/or extra-pair reproductive success in the blue tit (Parus caeruleus). Male blue tits display a bright blue crown plumage, which reflects substantially in the ultraviolet (UV) and previously has been indicated to be an important sexual signal. We show that males with a more UV-shifted crown hue were less cuckolded, which probably resulted from female preference for more ornamented mates. By contrast, however, older males and males with a less UV-shifted hue sired more extra-pair young. This probably did not reflect direct female preference, since cuckolders were not less UV-ornamented than the males they cuckolded. Alternatively, a trade-off between UV ornamentation and other traits that enhance extra-pair success could explain this pattern. Our results might reflect two alternative male mating tactics, where more UV-ornamented males maximize within-pair success and less UV-ornamented males maximize extra-pair success. Since crown colour was selected in opposite directions by within-pair and extra-pair paternity, directional selection through extra-pair matings seemed weak, at least in this population and breeding season. Reduced intensity of sexual selection due to alternative mating tactics constitutes a potential mechanism maintaining additive genetic variance of male ornaments.     

A trade-off generated by sexual conflict: Mediterranean wrasse males refuse present mates to increase future success

A variety of mechanisms, including intrasexual competition,intersexual conflict, and physiological constraints, can explainpatterns of reproduction and the adaptive value of specificbehaviors. In a Mediterranean wrasse, Symphodus ocellatus (Labridae),large, nesting males occasionally refuse to spawn with willingfemales in the presence of small, sneaker males. We exploredthe possible adaptive significance of this behavior. Nestingmales refuse females despite the fact that it reduces theirimmediate mating success. This nesting-male behavior also decreasesfemale and sneaker mating success and occurs when sneaker malessurround the nest. Experiments that decreased the number ofsneakers around nests showed that nesting males respond immediatelyto mating opportunities when fewer sneakers are present, andthus they are not simply constrained by a lack of energy orlack of sperm. Experiments that increased the number of sneakersat the nest caused nesting males initially to refuse spawningopportunities, followed by a subsequent decrease in sneakerpresence and an increase in mating rate. We propose that thisbehavior is the result of a trade-off between immediate matingsuccess and future reproduction created by competition betweenmales and conflict between the sexes. Males reduce their immediatemating success by reducing spawning at the nest; sneaker malessubsequently leave, and this decreases mate competition forthe nesting male. Unresponsiveness of nesting males also causessexual conflict between females and nesting males over mating.We argue that this behavior and the existence of a trade-offcan only be understood by examining intersexual conflict andintrasexual competition simultaneously.     

HOW WELL DO MATING FREQUENCY AND DURATION PREDICT PATERNITY SUCCESS IN THE POLYGYNANDROUS WATER STRIDER AQUARIUS REMIGIS?

Abstract.— The relationship between mating success and paternity success is a key component of sexual selection but has seldom been estimated for species in which both sexes mate with many partners (polygynandry). We used a modification of Parker's sterile male technique to measure this relationship for the water strider Aquarius remigis in 47 laboratory populations simulating natural conditions of polygynandry. We also tested the hypothesis that prolonged copulation, a characteristic of this species, enhances paternity success. Mating behavior and paternity success were assayed for four days while males and females freely interacted. Paternity success was also assayed for an additional 7 days when females were isolated from males. Mating success significantly predicted paternity success and accounted for ≤ 36% of the variance. Copulation duration was negatively related to both mating success and paternity success and did not explain any of the residual variance in paternity success. Thus, we found no evidence that prolonged copulation functions as a paternity assurance strategy in this species. Comparisons of sterile and fertile males suggested that paternity success is directly influenced by the quantity of sperm transferred. Our results support previous studies that have used mating success to estimate sexual selection, but also highlight the potential importance of sperm competition and other postinsemination processes.