Social and ecological factors affecting paternity allocation in American robins with overlapping broods

Factors that affect extra-pair mating in birds are likely to vary across the breeding season. Changing densities of active nests may alter the opportunities for extra-pair mating, and parental duties may alter a male’s opportunity to guard his mate from extra-pair mating. The latter affects species with multiple broods, where males care for fledglings from first nests while females initiate second nests. We studied a population of multi-brooded American robins (Turdus migratorius) to assess how seasonal changes in nesting density and changes in mate-guarding opportunity influenced paternity patterns over successive breeding attempts. Extra-pair paternity (EPP) occurred in 71.9% of broods and accounted for 48.1% of young. High nesting densities in the study population may explain the high overall rate of EPP, but seasonal variation in breeding density did not explain patterns of EPP among nests. Contrary to the predictions of the mate-guarding hypothesis, EPP did not increase in the second nests that followed successful first nests, and the percentage of extra-pair young in second nests did not decline as the overlap between successive nests increased. The fact that EPP was actually lower when the interval between clutches was shorter suggests that the sooner the males can assume sole care of first broods and allow their mates to renest (indicative of superior paternal quality), the more paternity they realize in the next nest. These results suggest that mate-guarding opportunity does not influence paternity in this population of American robins and that female robins may allocate paternity based on their assessment of male parental performance at first nests.     

Why do females have so few extra-pair offspring?

It is generally accepted that if a female can improve her offspring’s genetics via extra-pair copulations (EPC), it is by copulating with extra-pair males whose phenotypes are more superior or whose genes are more compatible to hers than those of her bonded male. Here, we present a model that puts together uncertainties about the male genetic quality, a postcopulatory sperm bias in favor of the better or the more compatible genes, and costs that females pay by being choosy about extra-pair male quality. The model’s conclusions challenge traditional views of good genes explanations of EPC. When phenotypes give incomplete information about genotypes, a female choosing a phenotypically superior extra-pair male, may nevertheless find herself trading good genes of a bonded male for poor genes of an extra-pair male. Such “unfortunate sperm replacements” can limit the female involvement in EPC even when EPC are otherwise cost-free. The model also shows that even a female bonded to a phenotypically superior male may benefit by EPC, provided that sperm competition is biased toward sperm with more fit or more compatible genes. Furthermore, if choosiness is sufficiently costly, a female may even do best by copulating with a random extra-pair male.     

Parentage and paternal care: consequences of intersexual selection in Savannah sparrows?

Empirical relationships between parentage and male parental care are commonly interpreted in the context of life-history models that consider increased offspring survivorship as the only benefit of paternal effort. However, indirect benefits associated with male care can also influence a male's response to cuckoldry: if females allocate paternity according to their prior experience with male parental care, it may pay for males to provision extra-pair young in early broods. Here, I assess the relationship between first-brood parentage and paternal care in a population of Savannah sparrows (Passerculussandwichensis) where a male's fertilization success in the second brood appears to be influenced by his prior parental performance. Based on the multi-locus DNA fingerprinting of 17 first broods, male feeding effort was influenced by parentage (percent of brood resulting from within-pair fertilizations) but not by brood size, male mating status (monogamous versus polygynous), timing of breeding (hatching date), structural size (wing length) or condition (mass). Males provided more care to broods that contained few within-pair young. This result supports the idea that males provision young to increase their future mating success, but alternative hypotheses involving male quality and timing of breeding cannot be excluded. Received: 13 August 1996 / Accepted after revision: 22 February 1997     

Replacement males in the western bluebird: opportunity for paternity, chick-feeding rules, and fitness consequences of male parental care

In western bluebirds (Sialia mexicana), most pairs remain together for life and share equally in post-hatching parental care. We removed resident males of socially monogamous pairs during laying and after clutch completion to examine chick-feeding rules used by replacement males and current and future fitness consequences of paternal care. Replacement males were not infanticidal and 7 (47%) fed nestlings. Feeding replacement males and the females they joined fed at rates similar to controls. Females without a feeding replacement male compensated by feeding more themselves so that overall feeding rates were not compromised, but they reduced their brooding time. Unlike assisted females, unassisted females exhibited reduced nesting success and their 14-day-old chicks weighed less than controls. Field metabolic rates of unassisted females were 17% higher than those of control females, but the difference was not statistically significant. Older females were better able to raise young without the male's help than were yearling females. Female condition was not affected by male provisioning and unassisted females were as likely to survive to the next breeding season as assisted females. We found no future benefits of provisioning by replacement males; those that fed were no more likely to breed with the female on her subsequent attempt than were males that did not feed, and subsequent clutch sizes were not reduced for females rearing young without the male's help. These experiments suggest that male parental care increases nesting success in western bluebirds and that replacement males use an all-or-none rule to determine whether or not to feed chicks: if they are present during the fertile period they feed at typical rates; if they are not, they usually do not feed at all. Because chick-feeding by males is tied to opportunity for paternity, influences success in the current nest, and does not affect the male's future breeding success, it appears to be parental rather than mating effort. Received: 8 May 1998 / Accepted after revision: 23 July 1998     

Manipulating the perceived opportunity to cheat: an experimental test of the active roles of male and female zebra finches in mate guarding behavior

Birds are commonly sexually promiscuous, which can lead to conflict between the sexes and the evolution of paternity assurance strategies, such as mate guarding. Adaptive explanations for mate guarding have tended to focus on fitness consequences for males, but mate guarding and participation in being guarded is also likely adaptive for females in certain contexts. To better understand the adaptive explanations for mate guarding as well as the observed variation in paternity patterns, it is necessary to explore the relative costs and benefits of guarding (and being guarded) from both the male and female perspective. To investigate these costs and benefits, we conducted an experiment with the Australian zebra finch (Teniopygia guttata) in which we independently varied the perceived opportunity for each member of a captive breeding pair to engage in extra-pair copulation (EPC) solicitation behavior; as an individual’s EPC opportunity increased, the partner’s EPC opportunity remained constant. Our results indicate that, for males, mate guarding intensity increases when their female’s EPC opportunity increases but decreases when their own (i.e., male) EPC opportunity increases. We did not find evidence of flexible female guarding behavior, but we found that females do not evade their partners more as female EPC opportunity increases.     

Duetting and mate-guarding in Australian magpie-larks (Grallina cyanoleuca)

A recently favored hypothesis is that duetting in birds has a mate-guarding function: a male responds vocally to his partner’s song, thereby forming a duet that repels males who are attracted to her song. Previous studies have not provided unambiguous tests of the mate-guarding hypothesis because: (1) the probability of a male answering his partner’s song has not been shown to increase specifically when the female is fertile, and (2) the probability of a male answering his partner’s song has not been assessed separately from simply a higher song initiation rate. We investigated extra-pair paternity, mate-guarding, and duetting in the socially monogamous Australian magpie-lark (Grallina cyanoleuca). DNA fingerprinting revealed that 3% of young were the result of extra-pair paternity, and we found that males guarded fertile females by staying close to them. However, males did not initiate songs at a higher rate when females were fertile and actually reduced their probability of replying to female song during this period. We conclude that although male magpie-larks did guard fertile females in an attempt to prevent extra-pair copulations, they did not use duetting for this purpose. Received: 10 May 1999 / Received in revised form: 27 September 1999 / Accepted: 2 October 1999     

Mate guarding,copulation strategies and paternity in the sex-role reversed,socially polyandrous red-necked phalarope<Emphasis Type="Italic"> Phalaropus lobatus</Emphasis>

In a recent review, Westneat and Stewart (2003) compiled evidence that extra-pair paternity results from a three-player interaction in which sexual conflict is a potent force. Sequentially polyandrous species of birds appear to fit this idea well. Earlier breeding males may attempt to use sperm storage by females to obtain paternity in their mates subsequent clutches. Later-breeding males may consequently attempt to avoid sperm competition by preferring to pair with previously unmated females. Females may bias events one way or the other. We examined the applicability of these hypotheses by studying mating behavior and paternity in red-necked phalaropes (Phalaropus lobatus), a sex-role reversed, socially polyandrous shorebird. Male red-necked phalaropes guarded mates more strongly than other shorebirds. Males increased within-pair copulation attempts during their mates fertile period, and maintained or further increased attempts towards the end of laying, suggesting an attempt to fertilize the females next clutch; these attempts were usually thwarted by the female. Paired males sought extra-pair copulations with females about to re-enter the breeding pool. Multilocus DNA fingerprinting showed that 6% of clutches (4/63) each contained one chick sired by a male other than the incubator, producing a population rate of these events of 1.7% (n=226 chicks). Male mates had full paternity in all first clutches (n=25) and 15 of 16 monogamous replacement clutches. In contrast, 3 of 6 clutches of second males contained extra-pair young likely fathered by the females previous mate. Previously mated female phalaropes may employ counter-strategies that prevent later mating males from discriminating against them. The stability of this polyandrous system, in which males provide all parental care, ultimately may depend on females providing males with eggs containing primarily genes of the incubating male, and not a previous mate.Communicated by M. Webster     

Breeding synchrony and paternity in the barn swallow (Hirundo rustica)

The barn swallow (Hirundo rustica) is a socially monogamous passerine which usually breeds in colonies where extra-pair copulations are frequent. Males intensively guard their mates during the female fertile period. Since males are more likely to be available for extra-pair copulations when their mate is not fertile, synchrony in timing of breeding may affect paternity of individual males. In this study, we analysed the change in mate-guarding rate by males in relation to the fertility condition of the female, and the relationships between breeding synchrony and density with paternity in first broods of 52 male barn swallows. Paternity (proportion of nestlings fathered in own brood) was assessed by typing of three highly polymorphic microsatellite loci. Mate guarding by males peaked during the fertile period of their mates. Paternity increased as breeding synchrony in the colony increased. Paternity of barn swallows is positively associated with the degree of exaggeration of male tail ornaments. The relationship between male ornamentation and paternity was partly mediated by an effect of ornament size on breeding synchrony. We suggest that females might delay breeding with low-quality males to enhance their opportunities for being fertilised by high-quality extra-pair males. Received: 16 January 1998 / Accepted after revision: 25 October 1998     

Mixed reproductive strategy and mate guarding in a semi-colonial passerine,the swallow Hirundo rustica

Summary Both male and female swallows Hirundo rustica have a mixed reproductive strategy (parental care for offspring and extra-pair couplations). Mate guarding protects females from male harassment and male swallows from being cuckolded. Females hide their fertile period by copulating successfully with their mates for an extended period during first clutches. Males guard in the pre-fertile period, when many unpaired males are present. Early breeding swallows guard more than late breeders since more sexual chases of females by non-mate males take place in the early period. Solitarily breeding females experience few chases by strange males; copulation frequency, length of copulation period and mate guarding is adjusted to a lower level than among colonial birds. Male guarding activity is more intense in the fertile than in the pre-fertile period. Guarding reduces success of extra-pair copulation attempts.Three female swallows each paired and copulated with a single male and later changed to a new male before starting to breed. Extra-pair copulations most often take place between neighbouring swallows in the fertile period of the female. Many old, early breeding males and many young, late breeding females participate in extra-pair couplations. Successful extra-pair copulations peak in the fertile period contrary to success of pair copulations which does not change during the copulation period.     

Breeding synchrony and extra-pair mating in red-winged blackbirds

Using data from a 6-year paternity study of red-winged blackbirds, I tested the hypotheses that increased nesting synchrony should either promote extra-pair mating by increasing the advantage of extra-pair mating to females, or decrease extra-pair mating by constraining males from seeking extra-pair copulations. Contrary to these hypotheses, the occurrence of extra-pair paternity did not vary with nesting synchrony over the breeding season, or vary with the number of synchronous nests within territories or within marshes, or with nesting order on territories. However, for nearly all nests with extra-pair young, there were fewer females synchronous with that nest on the cuckolder's territory than on the territory of the cuckolded male. This “advantage” of a synchrony difference was less pronounced for older males that cuckolded younger males, particularly when the two males were not neighbors. Collectively, these results suggest that breeding synchrony affects extra-pair mating by affecting mate guarding, but that breeding synchrony alone can not be used to predict which females are more likely to engage in extra-pair mating, nor with which extra-pair males they will mate. Understanding why extra-pair mating by older males is less affected by breeding synchrony may explain much about both the proximate and ultimate causes of extra-pair mating in red-winged blackbirds. Received: 7 June 1996 / Accepted after revision: 25 November 1996     

Condition-dependent control of paternity by female purple martins: implications for coloniality

Proposed causal links between extra-pair copulation (EPC) and colony formation in socially monogamous birds hinge on the question of which sex controls fertilizations. We examined in colonial purple martins Progne subis (1) whether EPCs were forced or accepted by females, and (2) the degree to which apparently receptive females were able to obtain EPCs against their mates’ paternity defenses. Paternity analyses of multilocus DNA fingerprinting confirmed previous findings of a marked relationship between age class and extra-pair fertilizations (EPFs), with young males losing paternity of 43% (n = 53) of their putative offspring compared to 4% (n = 85) by old males. All assignable extra-pair offspring were sired by old males, with one male obtaining most EPFs each year. Contrary to the hypothesis that EPCs are forced, EPF frequency within age class did not increase with seasonal increases in the number of males per fertile female. Whereas the male control hypothesis predicted that the male age class that mate-guarded more would be cuckolded less, the reverse was true: young males guarded significantly more intensely. The male age class difference in cuckoldry could not be explained by the possibility that young and inexperienced females (which are usually paired to young males) were more vulnerable to forced copulation because EPFs were unrelated to female age. These findings suggest that females (1) pair with old males and avoid EPCs, or (2) pursue a mixed mating strategy of pairing with young males and accepting EPCs from old males. The receptivity to EPCs by females paired to young males put them in conflict with their mates. Two factors determined the paternity achieved by young males: (1) the relative size of the male to the female, with young males achieving much higher paternity when they were larger than their mates, and (2) the intensity of mate-guarding. Both variables together explained 77% of the variance in paternity and are each aspects of male-female conflict. Given female receptivity to EPCs, mate-guarding can be viewed as male interference with female mating strategies. We conclude that EPCs are rarely or never forced, but the opportunity for females paired to young males to obtain EPCs is relative to the ability of their mates to prevent them from encountering other males. Evidence of mixed mating strategies by females, combined with other features of the martin mating system, is consistent with the female-driven “hidden lek hypothesis” of colony formation which predicts that males are drawn to colonies when females seek extra-pair copulations. Received: 23 March 1995/Accepted after revision: 14 January 1996     

Paternal care in the European starling,Sturnus vulgaris: nestling provisioning

The extent to which male birds in polygynous species with biparental care assist in nestling feeding often varies considerably between nests of different mating status. Both how much polygynous males assist and how they divide their effort between nests may have a profound effect on the evolution of mating systems. In this study we investigated how males in the facultatively polygynous European starling Sturnus vulgaris invested in their different nests. The amount of male assistance affected the quality of the offspring. Polygynous males invested as much as monogamous males, but divided their effort asymmetrically between nests, predominantly feeding nestlings of first-mated (primary) females. Although females partly compensated for loss of male assistance, total feeding frequency was lower at primary females’ nests than at monogamous females nests. Secondary females received even less assistance with nestling rearing, and the extent to which males assisted decreased with the length of the interval between the hatching of the primary and secondary clutches. These results are contrasted with those from a Belgian populations of starlings with a much more protracted breeding season and thus greater opportunities for males to attract additional mates during the nestling rearing period. The results show that both the “defence of male parental investment model” and the “asynchronous settlement model” have explanatory power, but that their validity depends on the potential length of the breeding season. Received: 21 July 1995/Accepted after revision: 13 July 1996     

Polygyny and extra-pair paternity enhance the opportunity for sexual selection in blue tits

Polygyny and extra-pair paternity are generally thought to enhance sexual selection. However, the extent to which these phenomena increase variance in male reproductive success will depend on the covariance between success at these two strategies. We analysed these patterns over four breeding seasons in facultatively polygynous blue tits Cyanistes caeruleus. We found that both polygyny and extra-pair paternity increased variance in male reproductive success and that standardised variance in annual number of genetic fledglings was 2.6 times higher than standardised variance in apparent success when assuming strict monogamy. Nevertheless, male success at securing within-pair paternity was unrelated to success at gaining extra-pair paternity and, when considering the positive effect of age on extra-pair success and attracting a second female, polygynous males were no more likely to sire extra-pair fledglings. Overall, polygynous males fledged more genetic offspring than monogamous males, but first-year polygynous males lost a greater share of within-pair paternity. A literature review suggests that this adverse effect of polygyny on within-pair paternity is frequent among birds, inconsistent with the prediction that females engage in extra-pair copulation with successful males to obtain good genes. Furthermore, a male's share of paternity was repeatable between years, and among females of polygynous males within years, such that a compatibility function of extra-pair copulations was likewise unsupported. Instead, we suggest that the observed patterns are most consistent with a fertility insurance role for extra-pair copulations, which does not exclude the greater opportunity for sexual selection through differential ability of males to gain paternity.     

Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus)

Extra-pair copulations, which occur when individuals that have formed social relationships to breed copulate outside their pairbond, now are recognized as an important component of reproductive success in many species. In situations where both males and females benefit from extra-pair copulations without incurring much risk, an inevitable conflict arises between pairbonded mates. In this study I investigated the conflict of interest between male and female reproductive strategies in a western population of red-winged blackbirds (Agelaius phoeniceus). Female red wings in this population initiate extra-pair copulations, which resulted in a 35% rate of extra-pair fertilization. Females initiated the majority (78%) of extra-pair copulations away from their nesting territory where pairbonded individuals typically copulate, and females that engaged in extra-pair copulations spent a significantly greater amount of time off the marsh during peak fertilization compared to females that did not. In addition, females that nested in areas with a large number of potential extra-pair partners produced significantly more extra-pair fertilized young compared to females that nested on marshes with few male neighbors. Males’ strategies to protect paternity were limited primarily to patrolling territory boundaries and to opportunistically preventing extra-pair copulations off the marsh when they were visible. In this population females appear to use behavioral means to control nestling paternity, which in turn directly affected their mate’s reproductive success, and males were restricted to using strategies that were largely ineffective at preventing the threat of extra-pair paternity. Received: 23 December 1994/Accepted after revision: 17 December 1995     

The pursuit of extra-pair copulations by monogamous female razorbills: how do females benefit?

Summary Monogamous female razorbills Alca torda actively sought extra-pair copulations (EPCs) in mating arenas outside their nesting colony. Females showed marked variation in promiscuity, defined as the number of EPCs they accepted (0–7), and in receptivity, defined as the percentage of EPC opportunities accepted (0%–100%). The opportunity of females to encounter males for EPCs was measured by (a) the time spent in the mating arena, and (b) the guarding effectiveness of their mates. Females appeared to encounter males and accept EPCs independently of opportunity, which suggests that variation in promiscuity and receptivity is caused by differences in the degree to which individual females might benefit from EPCs. I tested predictions of four hypotheses which propose benefits which females could obtain from EPCs: good genes, genetic diversity of offspring, insurance against infertility of mate, and acquisition of a new mate. No evidence was found to support two predictions made exclusively by the good genes hypothesis: (a) paired males did not achieve greater EPC success than unpaired males, and (b) males who were cuckolded did not obtain fewer EPCs than males whose mates avoided EPCs, suggesting that a male's attractiveness to other females does not ensure his own mate's fidelity. A prediction of both the insurance and good genes hypotheses was supported: females (who in this species retain their mates between years) showed similar receptivity to EPCs between years. This finding contradicts the genetic diversity hypothesis which predicts that in species that lay one egg per year, females who refuse EPCs in one year will accept them in the next. The good genes and genetic diversity hypotheses both predict that females who accept EPCs will behave as if to maximize their chances of being fertilized by extra-pair males. Results contradicted this prediction: females who accepted EPCs were more, rather than less receptive to their mates' copulation attempts than were females who did not accept EPCs. This finding is compatible with the insurance hypothesis which only requires females to store the sperm of extra-pair males, without necessarily being fertilized by it. Insurance against male infertility was the only hypothesis whose predictions were not contradicted by any of the results.     

Male tail streamer length predicts fertilization success in the North American barn swallow (Hirundo rustica erythrogaster)

In socially monogamous species, extra-pair paternity has the potential to increase the variance in male reproductive success, thereby affecting the opportunity for sexual selection on male extravagant ornamentation. In the European barn swallow (Hirundo rustica rustica), the tail streamer length is a sexually selected male ornament and an honest indicator of viability. The North American barn swallow (Hirundo rustica erythrogaster) also shows sexual dimorphism in tail streamer length, but whether this trait holds the same signalling function in this subspecies is a controversial issue, and the available literature is presently scarce. Here, we present data on paternity in the North American barn swallow, including a complete sampling of extra-pair sires in four colonies. We analysed how extra-pair paternity affected the variance in male fertilization success and examined whether male tail streamer (i.e. the outermost tail feather) length correlated with fertilization success (n=86 males). Extra-pair paternity constituted 31% of all offspring and significantly increased the variance in male fertilization success. The number of offspring sired by extra-pair males accounted for almost half of the total variance in male fertilization success. Males with naturally long tail streamers had a higher fertilization success than males with shorter tail streamers, and this pattern was mainly caused by a higher extra-pair success for males with long tail streamers. Males with long tail streamers also paired with early breeding females in prime body condition. These results are consistent with the idea that there is directional sexual selection on male tail streamer length, possibly mediated through male extra-pair mating success or the timing of breeding onset.     

Certainty of paternity covaries with paternal care in birds

Summary Male investment in parental care has been hypothesized to be affected or not to be affected by their certainty of paternity, depending on the particular assumptions of theoretical models. We used data on paternal care and extra-pair paternity from 52 bird species to determine whether male parental care was related to certainity of paternity. Paternal care was measured as the relative male contribution to nest building, courtship feeding, incubation, and feeding of nestlings, respectively. Males of avian taxa did not provide less parental care during nest building, courtship feeding and incubation if the frequency of extra-pair paternity was high. However, male participation in feeding of offspring was significantly negatively related to the frequency of extra-pair paternity. This was also the case when the effects of potentially confounding variables such as developmental mode of offspring (which may result in males being freed from parental duties), extent of polygyny (which may result in less paternal care), and the frequency of multiple clutches during one breeding season (which may increase the probability of finding fertile females during the nestling period) were controlled statistically. These results suggest that the extent of paternal care has been affected by certainty of paternity, and that sex roles during the energetically most expensive parts of reproduction have been shaped by sperm competition.     

Multi-locus DNA fingerprinting supports genetic monogamy in Florida scrub-jays

Extensive behavioural and pedigree data on a colour-marked population of Florida scrub-jays (Aphelocoma coerulescens) suggested that this cooperatively breeding species is monogamous, with extremely rare exceptions in which males have two mates. We used multi-locus DNA fingerprinting to test these observations by determining genetic parentage. Despite restricted dispersal and high relatedness between behavioural parents and non-breeding members of the group, DNA fingerprints provided sufficient variability to determine parentage unambiguously in almost all cases. We found no evidence of extra-pair fertilisation of females or egg dumping, and confirmed a suspected case of polygyny in which a mother and daughter laid and incubated in the same nest. Our results confirm that detailed behavioural data allow accurate assignment of genetic parentage in this species. In Florida scrub-jays, large territory size may limit opportunities for cuckoldry, and persistent intense competition for limited breeding space may lead to low variance in the quality of established male breeders. These factors would reduce both the opportunity for, and benefits of engaging in extra-pair fertilisations. Delayed dispersal and cooperative breeding in this species have not evolved as avenues for direct reproduction by unpaired individuals. Received: 25 May 1998 / Accepted after revision: 26 June 1998     

Testosterone and the allocation of reproductive effort in male house finches (Carpodacus mexicanus)

Testosterone has been proposed to serve as the mediator that controls the relative effort that an individual male bird will devote to mating effort versus parental effort. Here, we demonstrate a testosterone-influenced trade-off between parental and mating efforts in male house finches. Male house finches with experimentally elevated testosterone fed nestlings at a significantly lower rate, but sang at a higher rate than males without manipulated testosterone levels. Females mated to testosterone-implanted males fed nestlings at a significantly higher rate than females mated to males without testosterone implants, resulting in similar feeding rates for both treated and untreated pairs. The effects of testosterone on male house finches, however, were not as dramatic as the effects of testosterone observed in some other socially monogamous species of birds. Because extra-pair copulations are uncommon in house finches and males provide substantial amounts of parental care, these more modest effects may be due to differences in how the allocation of reproductive effort affects the costs and benefits of different reproductive behaviors. Received: 6 June 2000 / Accepted: 17 July 2000     

Extra-pair copulations in a lek: the secondary mating system of monogamous razorbills

Summary I studied the mating strategies of razorbills Alca torda, a monogamous colonial seabird, during 1987–1989 in Wales, U.K. The outstanding feature of the study population's mating system was the performance of most copulations in mating arenas outside the colony. Females visited the arenas and sometimes accepted extra-pair copulations (EPCs), and males aggressively competed for EPCs. During the fertilizable period of most females, the arenas resembled leks because they contained no resources except mates, and males contributed only sperm to extra-pair females. Typical of leks, the operational sex ratio was strongly male-biased, and male mating success was highly skewed. To examine the potential for sexual selection to operate in this system, I correlated male EPC success with variables that could be associated with male-male competition and/or female choice. The frequencies of three behaviors (interference of copulation attempts, fights won against other males, and EPC attempts), accounted for 62% of the variance in EPC success and were strongly intercorrelated, with interference explaining most of the variance in a multivariate test. EPC success was not correlated with body size, age, paired status or either of two estimates of the time spent in the arena. The hypothesis that male EPC success was determined by active female choice was tested by examining the relative success (EPCs per attempt) of males. Relative success was not correlated with any of the three behaviors associated with absolute success, or with age, body size or attendance, suggesting that male-male competition, mainly in the form of copulation interference, is the principal correlate of EPC success. These findings in a monogamous species illustrate that EPC is a secondary mating system of razorbills in which sexual selection operates. The existence of this system outside the colony raises the possibility that lekking for EPCs may also occur within the nesting territories of other monogamous, colonial species but is hidden by competition for nests and breeding partners.