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.     

Weather conditions affect levels of extra-pair paternity in the reed bunting Emberiza schoeniclus

Extra-pair paternity (EPP) is common in many socially monogamous birds, but large variations in frequency of EPP are found both between and within species. Local ecological factors can affect the costs and benefits of extra-pair mating behaviour, and may therefore influence the chance that individuals engage in extra-pair copulations (EPCs). We investigated the effect of weather conditions during the peak fertile period of the female on the levels of EPP in reed buntings Emberiza schoeniclus . The reed bunting is a socially monogamous passerine, with extremely high levels of EPP (50% of offspring in 80% of broods). We found that higher daily minimum temperatures and more rainfall during the peak fertile period were associated with lower proportions of EPP. As during adverse weather conditions individuals have to invest more in self maintenance, we suggest that during long periods of rain the extra-pair mating behaviour of all individuals will be restricted, leading to lower proportions of EPP. During cold mornings, time-consuming activities such as mate guarding are likely to be more strongly affected than less time-consuming activities such as EPCs, leading to higher proportions of EPP.     

Factors influencing mate guarding and territory defence in the stitchbird (hihi)

Socially monogamous male birds are predicted to maximise their reproductive success by pursuing extra-pair copulations (EPCs) while engaging in anti-cuckoldry behaviour such as mate guarding. In the stitchbird, Notiomystis cincta, high levels of forced EPCs and a high proportion of nestlings resulting from extra- pair fertilisations lead to the prediction that males of this species should exhibit intense paternity guarding behaviours. While studying an isolated stitchbird population on Tiritiri Matangi Island New Zealand (3636'S, 17453'E), I collected daily behavioural data throughout the breeding season from 15 males in 2000/01 and 27 males in 2001/02. In this study, male stitchbirds demonstrated clear paternity guarding by exhibiting: (1) an increased likelihood of being close to their mate during her fertile period, (2) an increased initiation of mate contact during her fertile period, (3) switching from site-specific territorial defence during the pre-fertile period to defending an area centring on the their female partners location during her fertile period, and (4) an increased following of the female to communal feeding sites outside the territory during her fertile period. For polygynous males, mate guarding and territorial defence were conditional on which of their females was fertile. Additional evidence supporting the hypothesis that mate guarding in this species is a form of paternity assurance, rather than protection from harassment, is that males protected their partner from harassment by other stitchbird males but did not intervene when females were harassed by male bellbirds, Anthornis melanura. While mate-guarding intensity in many species is conditional on the stage of female fertility, male stitchbirds also modified their behaviour depending on the location of the female and the rate of intrusions by extra-pair males. Resident males adopted a best-of-a-bad-job tactic when they were unable to locate their female by defending an area around her last known location. Furthermore, when the rate of intrusions by extra-pair males increased they traded-off the area they could defend within their territory against their ability to guard the female. Territory takeovers were uncommon, but when they did occur older males displaced younger males and healthy birds displaced sick ones. Contrary to the prevailing view that mate guarding is a male response to female infidelity, male stitchbirds appear to use mate guarding primarily to prevent paternity losses from forced EPCs. Future assessments of mate guarding function should consider the possibility that mate guarding involves a combination of conflict and co-operation between the sexes.     

Extra-pair paternity in the strongly monogamous Wandering Albatross Diomedea exulans has no apparent benefits for females

Although 92% of avian species are socially monogamous, extra-pair copulation (EPC), resulting in extra-pair paternity (EPP), is a common reproductive strategy in birds. Among seabirds, in which the rate of social monogamy reaches 100%, Procellariiformes (albatrosses and petrels) show low EPP rates, with the noticeable exception of the only albatross investigated in this regard, the Waved Albatross Phoebastria irrorata . This species, in which forced copulations are known to occur, showed a surprisingly high rate of EPP (25% of chicks). We investigate here EPP rates in another albatross species, the Wandering Albatross Diomedea exulans , subject to a demographic survey conducted for 38 years. We combined data on pair bonds with analysis of ten microsatellite loci and found that 10.7% of 75 chicks had an extra-pair sire. Although there was some evidence for inbreeding avoidance, within-pair and extra-pair chicks showed similar levels of heterozygosity, and the incidence of EPP was independent of age, experience or past reproductive success. Hence, we found no evidence that females benefit from EPCs. Owing to the male-biased sex ratio in adults, widowed and divorced males required more time to find a new mate (+28 and +72%, respectively) than did females. Combined with high sexual size dimorphism, this phenomenon might promote the forced copulations observed in this species. Our data therefore suggest that EPC is beneficial to unpaired males but occurs at random in females, consistent with the hypothesis that EPP results solely from forced EPCs. However, the importance of the latter for EPP and the part played by solitary males require further investigation.     

Does competition for nests affect genetic monogamy in Cory's shearwater Calonectris diomedea?

Most bird species are socially monogamous. However, extra‐pair copulations (EPCs), resulting in extra‐pair paternity (EPP), commonly occur. EPCs should allow females to adjust social mate choice and allow males that fail to obtain a nest a chance to avoid missing a breeding season, especially when poor nest supply constrains social mate choice. Procellariiformes (albatrosses and petrels) are socially monogamous seabirds which seldom divorce, even when nest availability constrains social mate choice. In Cory's shearwater Calonectris diomedea, a burrow‐nesting petrel, two studies conducted in the Mediterranean, where competition for nests is weak, detected no EPP. EPP remains to be investigated at localities where competition for nests is much stronger, such as Vila islet, Azores archipelago, Atlantic Ocean. We conducted a genetic (microsatellites) study over two successive years on Vila, involving the breeding pairs of the same 65 nests each year and their single chick. EPPs occurred each year, the overall rate being 11.6%. Coupling genetic analyses to a 7‐year demographic survey provided additional data on pair bonds and competition for nests. Overall, cuckoldry was unrelated to divorce, nest density and inbreeding avoidance, but was more frequent when the social male was small. Nest changes were more costly for males than for females, and some apparently unpaired males attempted to dislodge social males during within‐pair copulations. These results are compatible with the existence of a link between poor nest availability and EPP and confirm that even species considered strongly monogamous can adopt flexible mating strategies.     

Extra-pair copulations can insure female blue tits against male infertility

Mating outside the pair-bond occurs frequently in socially monogamous birds, but the benefits that females gain from this behaviour remain debated. One hypothesis is that females engage in extra-pair copulations (EPCs) to ensure that their clutch is fertilised in case their own mate is infertile, but evidence for this idea is scarce. We report on a case of an infertile male blue tit that bred in three successive years with three different females. In the first year, all eggs were sired by an extra-pair male whereas in the second year all eggs were unfertilised and contained no sperm. In the third year, the female produced two clutches that were fertilised by an extra-pair male, but – unlike ‘normal’ clutches – sperm numbers on the perivitelline membrane decreased rapidly over the laying sequence. Our findings show that blue tit females mated to an infertile male can escape reproductive failure by engaging in EPCs and support previous suggestions that EPCs in blue tits cease after the onset of egg laying.     

Inclusive fitness of 'kissing cousins': new evidence of a role for kin selection in the evolution of extra-pair mating in birds

Social monogamy is nearly ubiquitous across avian taxa,but evidence from a proliferation of studies utilizing molecular paternity analysis suggests that sexual monogamy is the rare exception rather than the rule (Griffith et al. 2002). Efforts to explain the prevalence of extra-pair paternity (EPP) have largely focused on the potential fitness benefits for offspring genetic quality, as females are less likely to benefit directly from seeking extra-pair mates. In particular, there has been considerable interest in the degree to which EPP may represent an adaptive female strategy to avoid inbreeding (or outbreeding)depression when paired with a highly related (or unrelated)social mate (Kempenaers 2007). Others have argued that, because relatives share many genes identical by descent,females might increase their own inclusive fitness by providing additional breeding opportunities to genetically related males (Waser et al. 1986; Kokko & Ots 2006). Thus, in the absence of significant inbreeding depression, pursuing EPP with relatives should be favoured by kin selection, although there exist few unambiguous empirical examples of such preferences in the literature. In this issue of Molecular Ecology, Wang &Lu (2011) present an analysis of mating patterns with respect to genetic relatedness of social and extra-pair partners in the ground tit (Parus humilis), a facultative cooperative breeder in which socially monogamous pairs occasionally form cooperative groups with unpaired helper males (Fig. 1). Consistent with the predictions of the kin-selection hypothesis, females in both bi-parental and cooperative groups preferentially engaged in extra-pair matings with relatives, irrespective of relatedness to their social mates, and while suffering no apparent costs of inbreeding depression in their progeny. These finding shave several exciting implications for our understanding of avian mating system diversity and the evolution of cooperative breeding.     

How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods

Extra-pair paternity is an important aspect of reproductive strategies in many species of birds. Given that in most species females control whether fertilization occurs, they are expected to benefit in some way from the extra-pair matings. In this study we use patterns of extra-pair paternity (EPP) in broods of individual reed buntings (Emberiza schoeniclus), both within and between seasons, to test four hypothesized female benefits: (1) assessing potential future partners and seeking (2) genetic diversity (3) good genes, or (4) compatible genes. Reed buntings are socially monogamous, multibrooded passerines with extremely high levels of extra-pair paternity. We studied a population of reed buntings in the Netherlands in 2002 and 2003; 51% of offspring in 74% of nests were extra-pair. We showed that patterns of EPP did not support the first and second hypotheses, since females did not form a pair with previous extra-pair partners, EPP was not evenly distributed among broods and more broods than expected were sired by a single male. Furthermore, there was no relation between a male's within- and extra-pair fertilization success, no consistency in EPP between breeding attempts, no effect of parental relatedness on EPP and several cases of reciprocal paternity. These patterns do not support the good genes hypothesis and are most consistent with the genetic compatibility hypothesis. However, our previous finding that older males are more successful in gaining EPP, suggests some effect of good genes. These hypotheses need not be mutually exclusive, as females may select compatible males above a certain quality threshold (e.g. old males).     

Do female great tits (Parus major) assess males by eavesdropping? A field study using interactive song playback

Male singing behaviour correlates with extra-pair success in several passerine birds. Singing interactions during territorial contests provide relative information on the males involved. Such information may be important in female extra-pair behaviour and eavesdropping on singing interactions among males may allow females to make such relative assessments. We used interactive playback to instigate singing contests with male great tits during the peak fertile period of their mate in an attempt to alter females'' assessment of mates'' quality relative to neighbours (potential extra-pair partners). We escalated a contest to one male (by overlapping his songs) and then subsequently de-escalated a contest (by alternating) to a neighbour. Intrusions onto neighbouring territories by females mated to either treatment male were then monitored. Females mated to escalation treatment males were more likely to intrude following playbacks than females mated to de-escalation treatment males. Although the absolute song output of males did not differ between treatments, males produced more song relative to playback in de-escalation treatments and relative song output was positively correlated with female intrusions. Therefore, female great tits eavesdrop on singing interactions and change their visitation rates to neighbouring territories according to their mate''s singing performance relative to neighbours.     

Female ground tits prefer relatives as extra‐pair partners: driven by kin‐selection?

Socially monogamous female birds routinely mate with males outside the pair bond. Three alternative hypotheses consider genetic benefits as the major driver behind the female strategy. The inbreeding avoidance hypothesis predicts that females paired with closely related males should seek copulations with distantly related extra-pair partners to avoid fitness loss from inbreeding depression; the outbreeding avoidance hypothesis predicts the opposite; the kin-selection hypothesis suggests that regardless of social mate relatedness, females should give related males extra-pair fertilization opportunities to gain inclusive fitness if the costs from inbreeding are minor. We test these hypotheses with a facultative cooperative breeder, the ground tit (Parus humilis). Social pairs of ground tits formed randomly with respect to genetic relatedness. In both bi-parental and cooperative groups, a female's engaging in extra-pair mating was independent of relatedness to her social mate; however, females preferred extra-pair sires to which they were more related than to their social mates. Moreover, females had higher relatedness with either their extra-group extra-pair sires in both bi-parental and cooperative groups, or within-group helper sires in cooperative groups, than expected by chance. When more than one potential extra-pair partner was available around a female's nest, she tended to select a relative. There was no indication of fitness reduction from extra-pair mating, which occurred at an intermediate level of inbreeding. These data support the kin-selection hypothesis, although there might be alternative nongenetic reasons associated with the extra-pair mating preference. Our finding offers a new explanation for why female birds pursue extra-pair mating. It also may broaden our understanding of the role of kin-selection in the evolution of cooperative society.     

No evidence for extra-pair paternity in the western gull

The genetic mating system of western gulls Larus occidentalis breeding on Southeast Farallon Island, California, was determined using multilocus DNA fingerprints of 33 chicks from 22 broods. No extra-pair paternity (EPP) was found, despite extra-pair copulations (EPCs) occurring. This suggests that paternity guards are effective, and that females gain few genetic benefits from EPCs. The EPP in western gulls concurs with that of other seabirds, reinforcing the idea that seabirds generally have a monogamous genetic mating system.     

Female mate guarding: no evidence in a socially monogamous species

To understand the behavioural aspects of sperm competition, the costs and benefits to both sexes should be considered. However, few studies have addressed the costs to females of their social mate engaging in extrapair copulations (EPCs). Measures of female mate guarding have concentrated on female solicitation and copulation; however, females may also control access to their mate by maintaining close proximity, as is common in males. I recorded the maintenance of pair proximity behaviour of an urban population of the socially monogamous European blackbird, Turdus merula, over three breeding seasons. There was no evidence that females guarded their mates to prevent them from engaging in EPCs, nor were there any effects of the potential quality indicators of age, body size or male bill colour on the intensity of mate guarding between individuals. The study adds to a small body of literature suggesting that female mate guarding may be found in (facultatively) polygynous species, but not in socially monogamous ones. Copyright 2000 The Association for the Study of Animal Behaviour.     

Cuckoldry and recapture probability of adult males are not related in the socially monogamous coal tit ( Parus ater)

Despite substantial research effort, the benefits of female extra-pair matings in socially monogamous bird species remain elusive. The good genes hypothesis assumes that females engage in extra-pair copulations with males of superior genetic quality compared to their respective social mate. Therefore, a negative association between the degree of cuckoldry and male survival is predicted, if genetic quality is phenotypically reflected by high viability. Furthermore, genetic sires of extra-pair offspring (EPO) should survive better than the social fathers they cuckolded. We tested these predictions in a nestbox population of the coal tit (Parus ater), a socially monogamous passerine with low breeding dispersal and high rates of extra-pair paternity (EPP). Based on 257 genotyped first broods of two consecutive years, we found no relationship between the incidence of EPP or the proportion of EPO within a given brood and male or female recapture probabilities. Furthermore, recapture rates did not differ between social and genetic fathers of EPO or males that did or did not appear as extra-pair sires in other broods. Our results were not affected by differential (short-range) breeding dispersal with respect to EPP or by other potentially confounding variables. Hence, they are not in accordance with the good genes as viability genes hypothesis.Communicated by F. Bairlein     

Reed bunting females increase fitness through extra-pair mating with genetically dissimilar males

Females of many socially monogamous species accept or even actively seek copulations outside the social pair bond. As females cannot increase the number of offspring with promiscuous behaviour, the question arises why they engage in extra-pair mating. We used microsatellite data to determine paternity, heterozygosity and genetic relatedness in the reed bunting (Emberiza schoeniclus), a species with high levels of extra-pair paternity (EPP). We found that extra-pair young (EPY) were more heterozygous than within-pair young (WPY). The high heterozygosity of the EPY resulted from a low genetic similarity between females and their extra-pair mates. EPY were heavier and larger when compared with their maternal half-siblings shortly before they left the nest. Recapture data indicated a higher fledgling survival of EPY compared with WPY. Our data suggest that reed bunting females increase the viability of their offspring and thus fitness through extra-pair mating with genetically dissimilar males.     

Extra-pair paternity does not result in differential sexual selection in the mutually ornamented black swan (Cygnus atratus)

We studied patterns of parentage in 85 broods (332 cygnets) of black swans during three breeding seasons, using a set of eight polymorphic microsatellite markers. We detected both intraspecific brood parasitism (IBP; < 5% of cygnets per year) and extra-pair paternity (EPP). In these years, 10-17% (mean = 15.1%) of cygnets resulted from EPP, and 27-40% (mean 37.6%) of broods contained at least one extra-pair cygnet. Compared with levels of EPP in closely related species with similar life histories, these values are unexpectedly high. EPP in black swans appears unrelated to ecological factors (breeding density and synchrony) or genetic factors (genetic similarity between pair members or genetic quality of the offspring). We found no evidence that a mutual sexual feather ornament known to play a role in social mate choice in black swans (curled wing feathers) is involved in extra-pair mate choice. EPP does not lead to greater variance in reproductive success in males, relative to females in this species. We therefore suggest that EPP does not result in differential sexual selection on males and females, explaining why they are ornamented to the same degree.     

Explicit experimental evidence for the effectiveness of proximity as mate-guarding behaviour in reducing extra-pair fertilization in the Seychelles warbler

Extra-pair copulations (EPCs; copulations outside the pair bond) are widespread in birds and may result in extra-pair fertilizations (EPFs). To increase reproductive success, males should not only seek to gain EPFs, but also prevent their own females from gaining EPFs. Although males could reduce the number of EPCs by their mates, this does not necessarily mean that they reduce the number of EPFs; indeed several studies have found no association between EPCs and EPFs. Male Seychelles warblers (Acrocephalus sechellensis) follow their partner closely during the period when the pair female is most receptive (fertile period). We show that males that guarded their mates more closely were less likely to have extra-pair young in their nest. This study on the Seychelles warbler is the first to provide explicit experimental evidence that mate guarding is effective in reducing EPFs. First, in territories where free-living males were induced to stop mate guarding during the pair female's fertile period, extra-pair parentage was higher than in the control group. Second, in the experimental group, the probability of having an extra-pair nestling in the nest was positively associated with the number of days during the fertile period for which mate guarding was artificially stopped. Thus, male mate guarding was effective in reducing the risk of cuckoldry.     

Female extra-pair behaviour and environmental quality in the serin (Serinus serinus): a test of the 'constrained female hypothesis'

Recent behavioural and molecular studies have shown that in most monogamous bird species extra-pair copulations and fertilizations outside the pair bond occur routinely. The consequences of female extra-pair behaviour might comprise effects on important life-history traits, such as the extent of male parental care. In this study we test the assumption that, within a species, females'' options for extra-pair mating depend on female quality and the environments that females occupy. This ''constrained female hypothesis'' predicts that females in good environments or high-quality females are able to resist males'' control efforts better than females in poor environments or low-quality females. We test the idea in the socially monogamous serin. We found that the likelihood of extra-pair paternity is significantly higher in territories with high availability of food. There was a negative relationship between environmental quality (food availability) and paternity both in natural and in experimentally manipulated habitats. Male feeding rates were negatively related to food availability and positively related to paternity. These data and the additional result that in better environments all of a females'' offspring were sired by one extra-pair male provide support for Gowaty''s ''constrained female hypothesis''.     

Extra-pair young in house wren broods are more likely to be male than female

Sex-allocation theory predicts that females should preferentially produce offspring of the sex with greater fitness potential. In socially monogamous animal species, extra-pair mating often increases the variance in fitness of sons relative to daughters. Thus, in situations where offspring sired by a female''s extra-pair mate(s) will typically have greater fitness potential than offspring sired by the within-pair mate, sex-allocation theory predicts that females will bias the sex of offspring sired by extra-pair mates towards male. We examined the relationship between offspring sex and paternity over six breeding seasons in an Illinois population of the house wren (Troglodytes aedon), a cavity-nesting songbird. Out of the 2345 nestlings that had both sex and paternity assigned, 350 (15%) were sired by extra-pair males. The sex ratio of extra-pair offspring, 0.534, was significantly greater than the sex ratio of within-pair offspring, 0.492, representing an increase of 8.5 per cent in the proportion of sons produced. To our knowledge, this is the first confirmed report of female birds increasing their production of sons in association with extra-pair fertilization. Our results are consistent with the oft-mentioned hypothesis that females engage in extra-pair mating to increase offspring quality.     

MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler

The existence and nature of indirect genetic benefits to mate choice remain contentious. Major histocompatibility complex (MHC) genes, which play a vital role in determining pathogen resistance in vertebrates, may be the link between mate choice and the genetic inheritance of vigour in offspring. Studies have shown that MHC-dependent mate choice can occur in mammal and fish species, but little work has focused on the role of the MHC in birds. We tested for MHC-dependent mating patterns in the Seychelles warbler (Acrocephalus sechellensis). There was no influence of MHC class I exon 3 variation on the choice of social mate. However, females were more likely to obtain extra-pair paternity (EPP) when their social mate had low MHC diversity, and the MHC diversity of the extra-pair male was significantly higher than that of the cuckolded male. There was no evidence that females were mating disassortatively, or that they preferred males with an intermediate number of MHC bands. Overall, the results are consistent with the 'good genes' rather than the 'genetic compatibility' hypothesis. As female choice will result in offspring of higher MHC diversity, MHC-dependent EPP may provide indirect benefits in the Seychelles warbler if survival is positively linked to MHC diversity.     

Sequential mating patterns suggest extra-pair mating is not part of a mixed reproductive strategy by female red-winged blackbirds

Studies aimed at determining why female birds often produce offspring sired by males other than their social mates generally compare traits of social and genetic mates. Here I examine paternity patterns in nests of the same female red-winged blackbirds (Agelaius phoeniceus) in successive breeding seasons. Returning females preferentially selected their former social mates as their new social mates when those males were present. However, paternity patterns were much less consistent. A female''s behaviour (faithful versus unfaithful) in one year did not predict her behaviour the following year. Females unfaithful in successive years did not prefer the same extra-pair males. Females unfaithful in one year that switched social mates the next year did not preferentially choose their former extra-pair mates as their new social mates. By switching genetic mates, females did not generally improve the quality of their mates. These results, together with previous analyses, suggest that female blackbirds in this population have little control over extra-pair mating. Although females may benefit from extra-pair mating because extra-pair males are generally longer lived, paternity patterns in this population are not consistent with extra-pair mating being part of a finely tuned female reproductive strategy.