Paternity Loss Research Articles

Extra‐pair paternity and song characteristics in the willow warbler Phylloscopus trochilus

Complexity in bird song is often argued to be advantageous in processes of sexual selection, and numerous studies show that characteristics of song are associated with increased success in territory defence or mate attraction. Less evidence exists on the relationship between bird song characteristics and patterns of extra‐pair paternity. We tested whether males that suffered from extra‐pair paternity differed in song characteristics from males with no extra pair paternity in the willow warbler Phylloscopus trochilus. In the Scottish population that we studied, we found that 23.5% of young were not related to the social father, and that 47% of nests contained at least one extra pair young. Older males were less likely to suffer paternity loss. While song repertoire size was not related to loss of paternity, males with short songs suffered higher paternity loss than males with long songs. Although arrival date is a good correlate of social mate choice in this population, it was not related to extra‐pair paternity. These results suggest that females use song length, or a trait correlated with this song characteristic, as a cue for choosing extra‐pair partners in this species, or alternatively that variance in the success of mate guarding or female coercion is related to this song variable.

Territorial meadow pipit males (Anthus pratensis; Passeriformes) become more aggressive in female presence

Although mate guarding as prevention of extra-pair copulation is common among birds, evidence for aggressive behaviour involving physical contact related to mate guarding in passerines is scarce and cases of the presence of one partner directly influencing the aggressiveness of the other are lacking. We investigated the intra-specific territorial behaviour of male meadow pipits (Anthus pratensis; Passeriformes: Motacillidae) at the beginning of the breeding season by placing a pipit model accompanied by an intra-specific song playback in the territory of socially paired males and compared the responses of males whose mates were physically present during trials with those whose females were out of sight. The level of aggression of males was significantly higher in the presence of the female; half of the males in this group physically attacked the model (the most intense and risky aggressive behaviour). Physical attacks did not occur among males whose female was absent during the trial; response to the playback by most of these males was only weak. This pattern may be related to the prevention of extra-pair copulation; if the risks involved in the conflict are outweighed by potential loss of paternity, such aggressive mate guarding may pay off. The apparently overlooked effect on the territorial behaviour of a partner's passive physical presence during conflict should be further evaluated because it may be important for the design and interpretation of results of behavioural experiments.

No evidence of genetic benefits from extra-pair fertilisations in female sand martins (Riparia riparia)

Genetic parentage studies of socially monogamous birds reveal a widespread prevalence of extra-pair paternity. Variation in extra-pair paternity among individuals may depend on how different individuals benefit from extra-pair fertilisations and on the opportunity to pursue extra-pair copulations. A long-term study of sand martins (Riparia riparia) in Hungary allowed us to examine patterns of extra-pair fertilisations in a large colony of over 3,000 breeding pairs with many known age individuals. We used multi-locus DNA fingerprinting to determine whether extra-pair fertilisations occur when females are paired to (1) presumably low quality mates, or (2) genetically similar or dissimilar mates, and whether extra-pair fertilisations result in offspring of higher quality. Extra-paternal young were found in 38% of 47 broods and comprised 19% of 190 offspring. Males that lost paternity did not differ significantly from others in age or body condition. Social mates of broods containing extra-pair offspring did not differ in genetic similarity from pairs without extra-pair offspring. Furthermore, there was no significant difference in body condition between extra-pair young and their maternal half-siblings. We were unable to assign paternity and therefore cannot exclude the possibility that extra-pair males differed from the within-pair males they cuckolded, in age, body condition or genetic similarity with the female. We found a positive relationship between paternity losses and breeding density, suggesting that low breeding density may constrain opportunities for seeking extra-pair copulations.

Paternity loss in contrasting mammalian societies

Recent genetic analyses show that, in social mammals, loss of paternity by breeding males varies with strategies of mate guarding rather than with the degree of polygyny.

The energetic cost of mate guarding is correlated with territorial intrusions in the New Zealand stitchbird

Male stitchbirds (hihi) Notiomystis cincta attempt to minimize paternity losses by engaging in intense mate guarding centered on the fertile period of their social mate. While this strategy is directed at preventing intruding extrapair males from successfully achieving forced copulation with their female, it is likely to be energetically costly because of the large amount of time spent chasing intruders. In this study, I measured the energetic cost of mate guarding by recording the daily body weight of 28 breeding male stitchbirds during first clutch attempts and used a classification and regression tree (CART) analysis to assess the relationship between their weight fluctuations and (1) measures of mate-guarding intensity, (2) the total duration of extrapair male intrusions into their territory, (3) the age of the focal male, (4) the local population density, and (5) proximity to supplementary food. The CART model divided resident males into two groups based on the level of intrusions by extrapair males. For the low-intruder group, resident males maintained a stable weight during their female's fertile period, whereas, for the high-intruder group, males lost an average 4.3% of their body weight, with their weights reaching a minimum on days - 1 and 0 relative to the date of first egg lay. This pattern of weight loss mirrored the pattern of extrapair territorial intrusions into the focal male's territory. While the costs of harassment associated with forced extrapair copulation have previously focused on females, this study shows that these costs can also be significant for the resident male. Copyright 2006.

Manipulation of male quality in wild tits: effects on paternity loss

Extrapair paternity (EPP) has proved to be widespread and highly variable among birds and other taxa, including sociallymonogamous species. A multitude of hypotheses have been put forward to explain this variation, but its occurrence is not fullyunderstood. Male age, social dominance rank, song and breeding density or synchrony have been among the suggestedcorrelates of EPP, but results so far are inconclusive. We interspecifically cross-fostered blue tits (Parus caeruleus) and great tits(Parus major) in the wild, thus manipulating males to exhibit reduced social dominance rank, sing aberrant songs, andconsequently be perceived as low-quality males as compared to controls. This allowed us to test if male quality had an influenceon loss of paternity. We found no statistically significant differences between cross-fostered and control males of either species,neither with respect to levels of cuckoldry nor proportions of extrapair young (EPY) in the broods. Paternity levels werecomparable to other studies on the same species. No effect of density could be detected on levels of EPP either, while an ageeffect seemed to be present at least in the blue tit, EPY being almost absent in broods of older blue tit males. We conclude thatthe effects of male quality on paternity loss are minor, if any, in these populations. Key words: cross-fostering, early learning,extrapair paternity, microsatellite, sexual imprinting, social rearing conditions. [Behav Ecol]

Male share of provisioning is not influenced by actual or apparent loss of paternity in western bluebirds

Approximately 45% of western bluebird (Sialia mexicana) females have some chicks in the nest that are not sired by their social mates. Extrapair fertilizations account for 42% of offspring in these nests and 19% of nestlings overall. I tested the hypothesis that males reduce nestling provisioning when their certainty of paternity or share of paternity is reduced. Capture and detention of socially monogamous males for 1 h or 24 h during the laying period reduced males' copulatory access and their ability to mate guard, increasing the frequency with which extrapair males intruded and attempted to copulate with resident females. Males detained during laying did not reduce their share of feeding trips compared to control males detained during incubation, compared to unmanipulated males, or compared to males that were captured but not detained. Males detained on territory for 1 h during the laying period did not reduce their share of feeding trips when they observed male intrusion, nor when they observed their mates accepting extrapair copulations. Males that witnessed their mates accepting extrapair copulations did not reduce their share of risk in provisioning. Genetic fingerprinting at nonexperimental nests indicated that males also failed to reduce their feeding contributions when their estimated share of paternity was reduced, even when a helper male was present to reduce the impact on nestlings. These results suggest that male western bluebirds do not make significant adjustments in their share of provisioning when they have evidence of partial paternity loss. Together with prior results, this study suggests that western bluebird males use an all-or-none rule, contributing approximately half of the parental provisioning at nests, as long they have some copulatory access to the female during egg laying.

Extra-pair paternity in the facultatively polygynous spotless starling, Sturnus unicolor

A potential cost of polygyny that may have restrained its evolution in some avian species is the presence of extra-pair offspring in the nests of males mated with several females. However, this relationship is not frequently found and an experimental approach investigating the association between extra-pair offspring and polygyny, while controlling for male traits related to polygyny, has not been undertaken. In this study, we manipulated the testosterone levels of facultatively polygynous spotless starlings, Sturnus unicolor, to establish experimentally different groups of polygyny and analyse its influence on levels of extra-pair offspring in males for which other traits were randomised. During two consecutive breeding seasons, we examined the effects of harem size on the ability of males to assure genetic paternity, assessed by DNA fingerprinting, and on reproductive success in their own nests. The frequency of extra-pair fertilisations varied between 10% (14/140) in 1996 and 20% (39/194) in 1997. Year-to-year analyses of extra-pair paternity variables with treatment as factor and harem size (number of simultaneous mated females) as covariate, were significant only in relation to harem size. Males with few simultaneously mated females were less cuckolded than more polygynous males in 1997 but not in 1996, indicating that mating costs of polygyny occurred, at least in the year with the higher rate of extra-pair paternity. Because polygynous males have more social mates, they may accrue higher reproductive success irrespective of their risk of being cuckolded. However, our results suggest that to be polygynous is costly in terms of paternity loss when we experimentally induce mating status controlling for individual male traits. However, the low values of our power tests for the statistically non-significant results of hormone on cuckoldry do not allow us to discard this hormone effect altogether.

Fertility Assurance through Extrapair Fertilizations and Male Paternity Defense

Extrapair paternity has been observed in many formally monogamous species. Male pursuit of extrapair fertilizations is explained by the advantages of having offspring that receive essential paternal care from other males. Since females are capable of exercising a degree of control over the post-copulatory sperm competition, extrapair paternity cannot persist unless it confers fitness benefits on cuckolding females. Thus, extrapair paternity involves cooperation between mated females and extrapair males. On the other hand, paired males frequently exhibit strategies that minimize their loss of paternity and/or conserve paternal investment if paternity is lost. Hence, extrapair attributes of diverse species and populations reported in the literature are particular solutions of evolutionary games involving gender-specific cuckolding/anti-cuckolding strategies. Here we use methods of evolutionary game theory to study the role of male paternity guarding strategies in situations where females seek extrapair fertilizations for reasons of genetic compatibility and/or in pursuit of genetic diversity for their offspring. Our results indicate that in these circumstances pursuit of extrapair fertilizations is the only evolutionary stable female strategy. Males, on the other hand, have two, mutually exclusive, evolutionary stable strategies: full time pursuit of extrapair fertilizations and a compromise strategy wherein they protect in-pair paternity during their mate's fertile periods and pursue extrapair paternity the rest of the time. The relative merits of these two strategies are determined by the efficiency of male in-pair paternity defense, breeding synchrony, fitness advantages of extrapair over in-pair offspring, and the intensity of competition for extrapair fertilizations from floater males.

Reed warblers guard against cuckoos and cuckoldry

Previous studies have shown that reed warblers, Acrocephalus scirpaceus, are more likely to reject a cuckoo, Cuculus canorus, egg if they have seen a cuckoo at their nest. This suggests that they would benefit from watching out for cuckoos. We tested whether presentations of a cuckoo mount near the nest (to simulate nest inspection) led to increased nest attendance by the warblers. Cuckoo presentations at completed nests before laying, when males guarded their females closely, led to desertion at 40% of nests before any eggs were laid (there were no desertions after presentations of a jay,Garrulus glandarius , a nest predator). In the remaining cases, there was no effect of the cuckoo on nest attendance before laying began, but a marked increase in male nest attendance (compared with jay and no-presentation controls) on the days the first and second eggs were laid. Cuckoo presentations at the one-egg stage led to the same increase in male nest attendance as did the prelaying presentations. Increased male nest attendance at the one–two-egg stage was not at the expense of mate guarding, because this declined anyway when laying began, and it did not lead to increased paternity loss compared with controls. Overall, 15% of broods had one or two extrapair young (6% of all young extrapair). We conclude that male reed warblers do increase nest guarding in response to cuckoos, but only after their females have begun egg laying, when there are less likely to be costs in lost paternity. Females did not increase nest guarding, perhaps because they need to spend more time foraging during the egg-laying period. Our results suggest that cuckoos should be secretive not only when they lay but also when they monitor host nests beforehand. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Age‐Related Variation in Mate‐Guarding Intensity in the Bluethroat (Luscinia s. svecica)

AbstractFemale extra‐pair copulations (EPCs) have selected for male paternity guarding strategies in many bird species. In the bluethroat, Luscinia s. svecica, males guard their mates closely during the last 2 d before the start of egg laying, but there is great individual variation in the intensity of mate guarding. Here we show that some of this variation is related to male age. Old males guarded their mates with much lower intensity and sang more than young males, although the latter difference was not statistically significant. Controlling for male age, male and female coloration and size were not significantly related to the intensity of mate guarding. We have previously shown that young and old males had a similar paternity loss in their own broods. On the other hand, old males were far more successful than young males in achieving extra‐pair fertilizations. These patterns suggest that young and old males have different trade‐offs between preventing paternity loss in own nest and gaining paternity in others, because male skills in obtaining EPCs improve with experience and/or because of female preferences for old males as copulation partners. There were no significant relationships between paternity and male mate‐guarding behaviour during the fertile period, indicating that mate guarding is not a very effective paternity‐assurance strategy in the bluethroat.

Badge size, paternity assurance behaviours and paternity losses in male house sparrows

Male quality may influence both the outcome of sperm competition and female faithfulness. In male house sparrows Passer domesticus, the size of the black throat patch (badge) signals dominance and perhaps attractiveness. So far, however, no study has reported any significant relationships between badge size, paternity and paternity assurance behaviours in this species. We found that the time mates spent together at the nest was positively correlated with badge size. Furthermore, although paternity losses were influenced by both the time spent at the nest and within‐pair copulation frequency, we found no relationship between copulation rate and badge size. It seems therefore that copulation frequency served as a paternity assurance behaviour, whereas the time mates stayed together at the nest may have reflected male attractiveness. Alternatively, females may have decided to stay with large‐badged males because they were better able to protect them from harassment by strange males. We also found that paternity losses were related to male badge size; average‐badged males cuckolded were more often than males with smaller or larger badges. We suggest that average‐badged males suffered higher paternity losses because they had different time allocation strategies than other males.

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

Reduction of maternal care: a new benefit of multiple mating?

Cost/benefit analyses have been used to understand the evolution of mating by females with multiple males, as in extrapair copulations (EPCs), which are now known to occur commonly in socially monogamous and polygynous birds. Indirect (genetic) benefits have been invoked to explain such mating patterns in some cases, but direct benefits have received less attention. We report a study of direct benefits in the communally rearing Mexican jay (Aphelocoma ultramarina). The social mate of the mother (putative father) is the most reliable feeder of the young in his nest, regardless of cuckoldry. Feedings provided by social fathers are not reduced in relation to their paternity loss. In contrast, mothers having nestlings sired by a second male tend to have lower feeding rates than those without such young. Secondary fathers provided a significantly higher level of feeding to the brood of their female than did (1) random nonbreeders of all ages and both sexes, (2) random male nonbreeders of all ages, and (3) older (2+ years), male nonbreeders. Surprisingly, however, broods with two fathers did not receive a higher level of total feeding, despite our observation that two-father broods had two more helpers, on average, compared to broods without extra fathers. Regardless of age or breeding status, males were more frequent feeders than females. This study provides the first evidence that one of the major costs of reproduction, maternal care of nestlings, is reduced for females that have young sired by secondary males. Copyright 2002.

Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk.

Males may increase their fitness through extra-pair copulations (copulations outside the pair bond) that result in extra-pair fertilizations, but also risk lost paternity when they leave their own mate unguarded. The fitness costs of cuckoldry for Seychelles warblers (Acrocephalus sechellensis) are considerable because warblers have a single-egg clutch and, given the short breeding season, no time for a successful replacement clutch. Neighbouring males are the primary threat to a male's genetic paternity. Males minimize their loss of paternity by guarding their mates to prevent them from having extra-pair copulations during their fertile period. Here, I provide experimental evidence that mate-guarding behaviour is energetically costly and that the expression of this trade-off is adjusted to paternity risk (local male density). Free-living males that were induced to reduce mate guarding spent significantly more time foraging and gained significantly better body condition than control males. The larger the reduction in mate guarding, the more pronounced was the increase in foraging and body condition (accounting for food availability). An experimental increase in paternity risk resulted in an increase in mate-guarding intensity and a decrease in foraging and body condition, and vice versa. This is examined using both cross-sectional and longitudinal data. This study on the Seychelles warbler offers experimental evidence that mate guarding is energetically costly and adjusted to paternity risk.

When do Males Sing Songs? Costs and Benefits of Singing during a Breeding Cycle.

To maximize their reproductive success, male birds have to acquire females, ensure their paternity, and increase the survival of their offspring. Males therefore allot their reproductive efforts to several activities during the nesting cycle, because there are trade-offs among the reproductive behaviours. In the Great Reed Warbler, Acrocephalus arundinaceus, there is a negative correlation between singing frequency and intensity of mate guarding, and between singing frequency and male feeding rate. Furthermore, male Great Reed Warblers adjust the time of singing by estimating the risk of paternity loss and abundance of potential secondary mates. In the Bush Warbler, Cettia diphone, males vigorously sing throughout the breeding season, which may be due to frequent female remating due to nest predation, resulting in a continuous source of potential mates for males. Thus, the timing of male singing is influenced by the costs and benefits of singing, which are related to other reproductive activities. Therefore, to understand singing activity, the social and ecological circumstances of the species should be considered, especially the occurrence of extra-pair fertilization, the pattern of parental care, the pattern of female arrival at the breeding area, and successiveness of pairbonds.

Explicit experimental evidence for the role of mate guarding in minimizing loss of paternity in the Seychelles warbler

Extra-pair copulations (EPCs) (copulations outside the pair bond) resulting in extra-pair fertilizations (EPFs) are widespread in birds. To increase reproductive success, males should not only seek EPCs, but also prevent their females from having EPFs. Male Seychelles warblers (Acrocephalus sechellensis) follow their partner closely during the period when these females are most receptive (fertile period). The Seychelles warbler is the first species to offer explicit experimental evidence that mate guarding functions as paternity guarding: in territories where free-living males were induced to stop mate guarding during the pair female's fertile period, the rates of intrusions by other males and successful EPCs (male mounting female) were significantly higher than those observed in the control group and in the absence of mate guarding the frequency of successful EPCs increased significantly with local male density. Male warblers do not assure their paternity through frequent copulations to devalue any sperm from other males: males do not copulate with their partners immediately following a successful EPC obtained by their partners, the frequency of successful within-pair copulations does not increase with the frequency of successful EPCs and females initiate all successful copulations and are capable of resisting copulation attempts.

Reproductive skew and the threat of eviction: a new perspective

Most recent models of the partitioning of reproduction attempt to explain patterns of skew on the assumption that dominant individuals have complete control over breeding opportunities within the group, but may nevertheless concede a share of direct reproduction to subordinates as an incentive to remain peacefully in the association. Although these models may be applicable to some animal societies, we argue that they fail to provide a comprehensive theory of skew. Instead, we suggest that subordinates may often be able to claim unsanctioned reproduction for themselves, but will be forced to exercise a degree of reproductive restraint lest they incite ejection by the dominant. Reproductive skew, in other words, may reflect the threat of ejection (inducing subordinate restraint) rather than the threat of subordinate departure (inducing reproductive concessions by dominants). We present a simple ESS model of reproductive skew under these circumstances, which demonstrates that a shift in emphasis from reproductive concessions by dominants to reproductive restraint on the part of subordinates, radically alters the predictions of skew models. High group productivity, high relatedness and (when group members are related) strong ecological constraints are all expected to lead to reduced skew (the opposite conclusions to those of previous, concession-based analyses). The reason is that these factors reduce the benefits (or increase the costs) of ejection to the dominant, who therefore does best to tolerate more subordinate reproduction.

The function of extrapair paternity in blue tits and great tits: good genes or fertility insurance?

DNA fingerprinting of an island population of blue tits and great tits in southeast Norway revealed that extrapair paternity accounted for 36% (17/47) and 27% (15/55) of broods and for 7% (31/466) and 8% (33/408) of young in the two species, respectively. Cuckolded males did not differ from noncuckolded males with respect to morphology, age, or survival. There was no seasonal pattern in the frequency of extrapair paternity, and males showed no individual consistency in paternity loss over multiple broods. Extrapair offspring did not grow faster, they did not fledge widi a higheT body mass, and they did not show a higher local survival rate than their half siblings. Hence, there was no evidence of any association between extrapair paternity and male phenotypic or genotypic quality. Extrapair offspring were randomly distributed among broods, with die only exceptions of one blue tit and two great tit broods in which all young (six to nine) were sired by an extrapair male. This pattern is best explained by a small proportion of males (2%—4%) being infertile and by most females performing a few extrapair copulations as insurance against laying infertile eggs. We conclude that the results suggest a role for fertility insurance but that alternative functional explanations to extrapair paternity in these populations cannot yet be ruled out. Key words: DNA fingerprinting, extrapair paternity, good genes, infertility insurance, offspring survival. Pants caeruleus, Parus major. [Behav Ecol 9:649-656 (1998)]

High Frequency of Extra-Pair Paternity in a Dense and Synchronous Population of Willow Warblers Phylloscopus trochilus

Genetic parentage was studied in a Norwegian, sub-alpine population of Willow Warblers Phylloscopus trochilus by means of multilocus DNA fingerprinting. We found that 33% (36/109) of the offspring were unrelated to the putative father, and that one additional offspring was unrelated to both putative parents. Altogether 50% (10/20) of the broods contained illegitimate young. The distribution of extra-pair paternity was bimodal, with several broods containing many extra-pair offspring. These results contrast markedly with a previous study of the same species, reporting no cases of mismatched parentage in a Swedish lowland population. Potentially, the high frequency of extra-pair paternity could be attributed to a higher breeding density and/or synchrony in our study population. Cuckolded males had a lower body mass, but no shorter tarsi or wings, than non-cuckolded males. This suggests that a male's loss of paternity is somehow related to his body condition. The data set includes five broods in which the pair male was permanently removed on the day the first egg was laid. There was no tendency that the manipulation increased the