Levels Of Extra-pair Paternity Research Articles

The evolution of extra-pair paternity and paternal care in birds.

Extra-pair paternity (EPP) influences the relatedness between social parents and offspring. Therefore, one might expect the level of EPP to influence levels of paternal investment. Here, we investigated the effect of variation in EPP rates on male contributions to parental care within a phylogenetic framework of up to 271 primarily socially monogamous bird species representing 85 families. We used proportion of male provisioning and occurrence of male incubation and nestbuilding as measures of paternal care. We tested the relationship between EPP rates and different components of paternal care while controlling for various life-history traits, namely lifespan, clutch size, and body mass in a phylogenetic path analysis framework. EPP was significantly negatively associated with the occurrence (i.e., whether males participate or not) of male nestbuilding and incubation, but not with the relative amount (proportion) of nestbuilding or incubation performed by the male. Importantly, the proportion of provisioning and biomass delivery by males was clearly negatively associated with EPP. These analyses thus confirm that the effect of EPP on proportion of provisioning visits by males is similar to proportion of biomass delivery, an often assumed but rarely tested assumption. Analysing only Passerine species provided similar results, although only proportion of provisioning was significantly negatively associated with EPP. This study, therefore, provides the most comprehensive support to date of a negative relationship between EPP and paternal care across species. However, a causal relationship between EPP and paternal care cannot necessarily be concluded. We also identify key methodological improvements for future research within the topic.

Extra‐pair paternity correlates with genetic diversity, but not breeding density, in a Neotropical passerine, the black catbird

The frequency of extra‐pair paternity (EPP) varies widely across socially monogamous birds, but the proximate mechanisms driving this variation remain unclear. In this study, we tested two major factors hypothesized to influence extra‐pair mating – breeding density and genetic diversity – by comparing genetic mating patterns in two populations of black catbirdsMelanoptila glabrirostris. This Neotropical songbird is endemic to the Yucatán Peninsula, including eastern Mexico, and its offshore islands. We sampled one mainland (Sian Ka'an Biosphere Reserve) and one island (Isla Cozumel) population and used single‐nucleotide polymorphisms (SNPs) to quantify heterozygosity and genetic parentage over two breeding seasons. Moderate levels of EPP occurred in both populations (9.5–35% of offspring and 17–45% of nests). Contrary to predictions, breeding density did not affect EPP: although breeding densities were much higher on the mainland than on the island, EPP rates did not differ between populations, and local breeding density was not correlated with EPP at individual nests. In contrast, partial support emerged for the hypothesis that genetic diversity influences EPP: extra‐pair offspring were more heterozygous than within‐pair offspring. However, the two populations did not differ in genetic diversity, and neither the heterozygosity of social fathers nor within‐pair relatedness predicted EPP. These results are consistent with recent comparative studies suggesting that breeding density is not a critical driver of EPP rates, and that not all tropical songbirds exhibit low rates of EPP.

Report of an extra-pair copulation in the Rufous Hornero, Furnarius rufus (Aves: Furnariidae)

In the last decade, studies in bird breeding biology have shown that infidelity is prevalent in socially monogamous species. Here, we describe an extra-pair copulation (EPC) event in the Rufous Hornero (Furnarius rufus), a socially monogamous bird with year-round territoriality and low levels of extra-pair paternity. Before the EPC, a within-pair copulation (WPC) occurred inside the pair’s territory. The WPC occurred on the ground and between a banded male (ca. 6 years-old) and an unbanded female. Ten minutes later this breeding pair invaded a neighboring territory, presumably to forage. The territorial male was chased back to its territory by an unbanded male neighbor after being detected. The male neighbor was paired with an unbanded female that did not participate in the aggressive interaction. When flying back to its territory the male neighbor copulated with the territorial female on the ground (ie. EPC). The territorial male flew, vocalized, and perched above the male neighbor, interrupting the EPC. The aggressive interaction then ceased as each pair resumed foraging in their respective territories. These observations suggest that Rufous Horneros can use EPC to obtain immediate benefits (food access in a neighbor’s territory). Moreover, WPC may be detected by neighbors and physical mate guarding and/or frequent WPC may be necessary to prevent EPC in the Rufous Hornero.

Determining the level of extra-pair paternity in yellow-bellied prinias, a socially monogamous passerine

Previous work based on molecular evidence has shown that most socially monogamous birds follow a genetic polyandrous mating system. However, our knowledge about avian mating systems is heavily biased toward the north temperate zone, with data on tropical birds remaining relatively scarce. This uneven distribution of both phylogenetic and spatial sampling has hampered our understanding and interpretation of results. In this study, we investigated the frequency of extra-pair paternity (EPP) in a tropical population of yellow-bellied prinias (Prinia flaviventris) in Guangxi, southern China. A total of 129 individuals belonging to 24 nests were sampled, among which 12 out of 83 chicks (14.46%) in seven nests were found to be EPP offspring. In nests in which all nestlings were sampled, only five out of 56 chicks were EPP offspring, accounting for an unbiased EPP rate of 8.93%. This rate is below the average rate of EPP in the family Sylviidae. The possible causes of EPP in prinias and the occurrence of EPP in birds with high resource investment and intensive parental care are discussed. This study highlights the value of genome-wide markers in determining relatedness in a wild bird species without a reference genome.

Extra-pair paternity and antiparasitic defence

BackgroundExtra-pair paternity (EPP) in birds provides benefits in terms of more offspring, and characteristics for maintenance of this behaviour have been the subject of investigation. Microorganisms are known to be transmitted during mating, especially when mating with multiple partners, and factors reducing this cost of multiple mating are expected. Further, plumage brightness and colour intensity have been shown to be important traits to benefits from multiple mating as predicted by sexual selection. The aim of this study was to investigate the relationship between the rate of extra-pair paternity and the relative size of the uropygial gland at the interspecific level, as the uropygial gland is an exocrine gland hypothesized to produce antiparasitic substances and further identified to affect plumage brightness. Because of the expected benefits of large uropygial gland in scenarios of sexual selection, we predicted a positive correlation with EPP.MethodsWe collected information from the literature of uropygial gland size and frequency of extra-pair paternity of 60 avian species of different families and explored the predicted positive correlation between them. We did so with means of comparative analyses that considered phylogenetic relationship as random factor and included body mass as covariate. We used Markov chain Monte Carlo generalized linear mixed models that were weighted by number of nests used to estimate extra-pair paternity.ResultsWe detected a positive relationship between level of extra-pair paternity and uropygial gland size at an interspecific level. This finding is consistent with the prediction.ConclusionsWe discuss the importance of this result in scenarios of sexual selection and argue that the detected relationship may have arisen by utilizing antiparasitic secretions through secondary sexual characters indicating parasite resistance.

Analysis of within-individual variation in extrapair paternity in blue tits (Cyanistes caeruleus) shows low repeatability and little effect of changes in neighborhood.

Many studies investigated variation in the frequency of extrapair paternity (EPP) among individuals. However, our understanding of within-individual variation in EPP remains limited. Here, we comprehensively investigate variation in EPP at the within-individual level in a population of blue tits (Cyanistes caeruleus). Our study is based on parentage data comprising >10 000 genotyped offspring across 11 breeding seasons. First, we examined the repeatability of the occurrence of EPP, the number of extrapair offspring, the number of extrapair partners, and the occurrence of paternity loss using data from males and females that bred in multiple years. Second, we tested whether within-individual changes in EPP between breeding seasons relate to between-year changes in the local social environment. Repeatabilities were generally low but significant for the occurrence and number of extrapair young in females and for whether a male sired extrapair young or not. We found no evidence that the presence of the former social partner or changes in the proportion of familiar individuals or in phenotypic traits of the neighbors influenced changes in levels of EPP in females. However, in adult males, a decrease in the average body size of male neighbors was associated with higher extrapair siring success. If confirmed, this result suggests that the competitive ability of a male relative to its neighbors influences his extrapair mating success. We suggest that alternative hypotheses, including the idea that within-individual changes in EPP are due to “chance events” rather than changes in an individual’s social breeding environment, deserve more consideration.

An experimental increase in female mass during the fertile phase leads to higher levels of extra-pair paternity in pied flycatchers Ficedula hypoleuca

Female mass in most altricial birds reaches its maximum during breeding at egg laying, which coincides temporally with the fertile phase when extra-pair paternity (EPP) is determined. Higher mass at laying may have two different effects on EPP intensity. On the one hand, it would lead to increased wing loading (body mass/wing area), which may impair flight efficiency and thereby reduce female’s capacity to resist unwanted extra-pair male approaches (sexual conflict hypothesis). On the other hand, it would enhance female condition, favouring her capacity to evade mate guarding and to search for extra-pair mates (female choice hypothesis). In both cases, higher female mass at laying may lead to enhanced EPP. To test this prediction, we reduced nest building effort by adding a completely constructed nest in an experimental group of female pied flycatchers (Ficedula hypoleuca). Our treatment caused an increase in mass and thereby wing loading and this was translated into a significantly higher EPP in the manipulated group compared with the control group as expected. There was also a significant negative relationship between EPP and laying date and the extent of the white wing patch, an index of female dominance. More body reserves at laying mean not only a higher potential fecundity but a higher level of EPP as well. This interaction had not previously received due attention but should be considered in future studies of avian breeding strategies. While most research has been focused on determining possible criteria for extra-pair mate choice by females, less effort has been made on establishing if female traits are related to EPP and its intensity. One such trait is mass at laying which attains its highest level for breeding females of altricial birds. Our study indicates that a higher mass during the fertile phase not only has implications for female fecundity and predation risk but also for EPP in the resulting brood as more mass means a higher EPP.

Extra-pair paternity in two passerine species living in an extreme-arid desert region

The level of extra-pair paternity (EPP) is extremely variable among avian species. Although a powerful interspecific database has been provided, further extra-pair paternity investigations on different species and populations in different environments are needed to advance our understanding of avian mating systems. Two passerine species living in same desert environment, the Isabelline Shrike (Lanius isabellinus) and Saxaul Sparrow (Passer ammodendri), are socially monogamous, but exhibit differences in many traits. We identified 6 polymorphic microsatellite loci for the Isabelline Shrike and 10 loci for the Saxaul Sparrow to estimate the rate of EPP. The results indicated that 4.92% of Isabelline Shrike broods (3/61) contained extra-pair offspring, with 1.46% of nestlings (3/ 206) being sired by extra-pair mates. Of the Saxaul Sparrow, 38.82% of broods (33/85) had at least one extra-pair offspring; the percentage of extra-pair offspring was 11.22% (44/392). In conclusion, these 2 passerines have different levels of EPP; however, these levels are comparable to those found in congeneric species.

Experimentally flight-impaired females show higher levels of extra-pair paternity in the pied flycatcher Ficedula hypoleuca.

There is no consensus yet on the reasons why females engage in extra-pair copulations (EPCs). In some species, females have been shown to accrue some indirect benefits, but these effects are not consistent across species and studies. The sexual conflict hypothesis posits that extra-pair paternity (EPP) is the result of strong selection for male pursuit of EPC without real benefits for females. In order to test this hypothesis, we experimentally reduced wing area (reversibly tying together some primary feathers), in a group of pied flycatcher females (Ficedula hypoleuca). The manipulation increases wing loading (body mass/wing area), which is negatively associated with flying ability, and thus with the capacity to escape from unwanted copulations. We compared the levels of EPP in this experimental group with those of a group of un-manipulated females. Experimental females almost doubled the proportion of extra-pair young (EPY) with respect to control females. In addition, more males sired EPY in experimental than in control broods containing EPY. These results suggest that in our study population, EPP could be partially a product of female capacity to avoid EPCs. We also discuss the alternative hypothesis that results might be due to an eventual reduction of female attractiveness.

Socio-ecological conditions and female infidelity in the Seychelles warbler.

Within socially monogamous breeding systems, levels of extra-pair paternity can vary not only between species, populations, and individuals, but also across time. Uncovering how different extrinsic conditions (ecological, demographic, and social) influence this behavior will help shed light on the factors driving its evolution. Here, we simultaneously address multiple socio-ecological conditions potentially influencing female infidelity in a natural population of the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis. Our contained study population has been monitored for more than 25 years, enabling us to capture variation in socio-ecological conditions between individuals and across time and to accurately assign parentage. We test hypotheses predicting the influence of territory quality, breeding density and synchrony, group size and composition (number and sex of subordinates), and inbreeding avoidance on female infidelity. We find that a larger group size promotes the likelihood of extra-pair paternity in offspring from both dominant and subordinate females, but this paternity is almost always gained by dominant males from outside the group (not by subordinate males within the group). Higher relatedness between a mother and the dominant male in her group also results in more extra-pair paternity—but only for subordinate females—and this does not prevent inbreeding occurring in this population. Our findings highlight the role of social conditions favoring infidelity and contribute toward understanding the evolution of this enigmatic behavior.

Indirect fitness benefits through extra-pair mating are large for an inbred minority, but cannot explain widespread infidelity among red-winged fairy-wrens.

Extra‐pair paternity (EPP) has been suggested to improve the genetic quality of offspring, but evidence has been equivocal. Benefits of EPP may be only available to specific individuals or under certain conditions. Red‐winged fairy‐wrens have extremely high levels of EPP, suggesting fitness benefits might be large and available to most individuals. Furthermore, extreme philopatry commonly leads to incestuous social pairings, so inbreeding avoidance may be an important selection pressure. Here, we quantified the fitness benefits of EPP under varying conditions and across life‐stages. Extra‐pair offspring (EPO) did not appear to have higher fitness than within‐pair offspring (WPO), neither in poor years nor in the absence of helpers‐at‐the‐nest. However, EPP was beneficial for closely related social pairs, because inbred WPO suffered an overall 75% reduction in fitness. Inbreeding depression was nonlinear and reduced nestling body condition, first year survival and reproductive success. Our comprehensive study indicates that EPP should be favored for the 17% of females paired incestuously, but cannot explain the widespread infidelity in this species. Furthermore, our finding that fitness benefits of EPP only become apparent for a small part of the population could potentially explain the apparent absence of fitness differences in population wide comparisons of EPO and WPO.

Extra-pair paternity in socially monogamous Streaked Shearwaters: forced copulation or female solicitation?

Seabirds are long-lived birds that invest in offspring at very high levels, for which male parental care is indispensable. These characteristics are thought to explain seabirds’ generally low level of extra-pair paternity (EPP). Although the Streaked Shearwater (Calonectris leucomelas) is a socially monogamous seabird, it is known to copulate outside its social pair bond, which implies the frequent occurrence of EPP. In the closely related Cory’s Shearwater Calonectris borealis, cuckoldry is related to body size of the social male. To determine whether body-size-related EPP occurs among Streaked Shearwaters, we established 39 new microsatellite markers for parentage analysis and compared body size between cuckolded and non-cuckolded males. With the new markers, we found that extra-pair males sired 17 (15.0%) of 113 offspring during the 2014–2016 study period, which included three 1.5-month chick-rearing periods. This percentage is among the highest recorded for seabirds. We also found the bill and wing length of cuckolded males to be significantly shorter than those of non-cuckolded males, and that females can reject attempted copulations. These observations imply that EPP in this species is size related and involves female acceptance.

Linking the fine-scale social environment to mating decisions: a future direction for the study of extra-pair paternity.

Variation in extra-pair paternity (EPP) among individuals of the same population could result from stochastic demography or from individual differences in mating strategies. Although the adaptive value of EPP has been widely studied, much less is known about the characteristics of the social environment that drive the observed patterns of EPP. Here, we demonstrate how concepts and well-developed tools for the study of social behaviour (such as social network analysis) can enhance the study of extra-pair mating decisions (focussing in particular on avian mating systems). We present several hypotheses that describe how characteristics of the social environment in which individuals are embedded might influence the levels of EPP in a socially monogamous population. We use a multi-level social approach (Hinde, 1976) to achieve a detailed description of the social structure and social dynamics of individuals in a group. We propose that the pair-bond, the direct (local) social environment and the indirect (extended) social environment, can contribute in different ways to the variation observed in the patterns of EPP, at both the individual and the population level. A strength of this approach is that it integrates into the analysis (indirect) interactions with all potential mates in a population, thus extending the current framework to study extra-pair mating behaviour. We also encourage the application of social network methods such as temporal dynamic analysis to depict temporal changes in the patterns of interactions among individuals in a group, and to study how this affects mating behaviour. We argue that this new framework will contribute to a better understanding of the proximate mechanisms that drive variation in EPP within populations in socially monogamous species, and might ultimately provide insights into the evolution and maintenance of mating systems.

Female splendid and variegated fairy-wrens display different strategies during territory defence

Contrary to the traditional view that territory defence is a male behaviour, there is now evidence that female birds actively engage in territory defence, either alone or with their mate. In males, song sharing between neighbours has been shown to facilitate territory defence, but little is known about the importance of song sharing for such behaviour in females. Here, I examined sex roles and song element sharing in two related species: the splendid fairy-wren, Malurus splendens , and the variegated fairy-wren, Malurus lamberti . I first described song structure and song element sharing between partners and neighbours in both male and female songs. I then simulated conspecific intrusions by broadcasting a female or a male song within a pair's territory. Both splendid and variegated fairy-wren females sang songs as complex as their male counterparts and responded to playback of simulated conspecific intrusions. Song element sharing with neighbours was common in both species, but only splendid fairy-wren females shared more elements with their mate than with other recorded males on average. Females in each species engaged in different strategies when responding to territory intruders: female splendid fairy-wrens competed with female intruders, while variegated fairy-wren females coordinated their defence with their mates and exhibited cooperative defence behaviours toward male intruders. I discuss the ideas that variation in levels of extrapair paternity and/or female competition may drive the evolution of different female strategies when responding to territory intruders.

Effects of load-lightening and delayed extrapair benefits on the fitness consequences of helping behavior.

In most cooperative breeders, helping is directed at close kin, allowing helpers to gain indirect fitness benefits by increasing the reproductive success of close relatives, usually their parents. Extrapair paternity (EPP) occurs at high rates in some cooperative breeders, reducing the relatedness of helpers to the young they help raise. Even so, a son that helps is related to the brood by at least 0.25 through his mother and to within-pair young by 0.5, whereas a potential helper that has EPP in his own nest is related only to the offspring he sires and unrelated to any extrapair offspring. In birds, EPP often favors older males, which in the extreme case can result in sons being more closely related to young in their parents' nest than to young in their own nests. The fitness benefit of helping will thus be enhanced if helping lightens the workload and increases survival of helpers and their fathers, enabling them to become old, hyper-successful extrapair sires. Here, we develop and analyze a proof-of-concept model, grounded in the western bluebird (Sialia mexicana) system, demonstrating the conditions under which high population levels of EPP can generate inclusive fitness benefits of helping behavior that outweigh the costs. This model provides a new perspective on the relationship between EPP and helping behavior in cooperative breeders and suggests a strong need for empirical work to gather unprecedented data on paternity over the lifetime of helpers and their parents.

Roles of phenotypic and genetic characteristics in the social mating pattern of Silver-throated Tits (Aegithalos glaucogularis)

Choice of mating partners may affect fitness. Both phenotypic and genetic traits have been shown to play roles in the mating processes of animals. We investigated the roles of phenotypic and genetic characteristics in the patterns of social mating in the Silver-throated Tit (Aegithalos glaucogularis), a sexually monochromatic species that exhibits sexual size dimorphism, rarely sings, does not occupy territories, and has a relative low level of extrapair paternity. To explore the role of phenotype traits, we tested for assortative mating based on the sizes of seven morphological traits. To explore the role of genetic traits, we tested for assortative mating with respect to genetic heterozygosity (the heterozygous mate hypothesis) and whether birds mated with genetically dissimilar individuals (the compatible mate hypothesis). We found significant correlations between paired individuals for bill length and body length, indicating possible assortative mating based on these two traits. In contrast, genetic heterozygosity was not correlated between paired individuals, and the mean relatedness of the mates was not significantly different from that of randomly mated individuals, which do not support the idea that Silver-throated Tits assortatively mate with heterozygous individuals or choose genetically dissimilar mates. Also, individual heterozygosity was not reflected in the measured morphological traits, as no correlation was detected. Neither the individual heterozygosity nor the relatedness between mates was correlated with reproductive performance measures, including clutch size, brood size, and number of fledglings. However, we found that clutch size increased with female body length, which could explain the benefit to males of mating with larger females. Taken together, while our current data failed to provide evidence for an effect of genetic characteristics on the social mating pattern of Silver-throated Tits, the results suggest that phenotypic traits are likely associated with their mating pattern.

Crimson-breasted Shrike females with extra pair offspring contributed more to duets

Many socially monogamous bird species follow a genetically promiscuous reproductive strategy. Duetting birds may be an exception, as they appear to exhibit very low levels of extra pair paternity—which is thought to be connected to duetting. Duets are predicted to function either in paternity guarding or as signals of commitment to the pair bond, reciprocally reducing extra pair mating in both sexes. In this study, we used four microsatellites to document paternity loss in the Crimson-breasted Shrike (Laniarius atrococcineus), a socially monogamous subtropical duetting species. Extra pair paternity was surprisingly high, with extra pair males siring 20 % of young in 30 % of broods. Furthermore, we compared the levels of extra pair paternity of each pair to certain characteristics of their duets to test the paternity guard and the commitment hypotheses. Our results offered no support that duets function in paternity guarding, although the fact that males which had been cuckolded answered more of their female’s calls could represent an adaptation to avoid future cuckoldry. We also found no evidence for duets functioning as signal of commitment. Female vocal behaviour was in fact the reverse of that predicted: Levels of infidelity amongst social females were positively related to female answer rate of their mates’ songs. These results indicate that females may use increased answer rates as a form of manipulation, in an attempt to avoid potential costs associated with their extra pair matings.

Low extrapair paternity observed in a tropical bird despite ample opportunities for extrapair mating

Abstract. The occurrence of extrapair paternity (EPP) in socially monogamous species varies greatly among species and across latitudes. Recent work suggests that birds residing in less seasonal, tropical environments will have lower levels of EPP than seasonal tropical and temperate species. Less seasonal tropical birds are predicted to have the lowest rates of EPP because their presumed low breeding densities and low breeding synchrony may reduce the opportunities for extrapair mating, and their potentially higher adult survival and longer-term pair bonds may increase the costs of retaliation by males, resulting in reduced paternal care. Nevertheless, the limited number of studies in tropical regions impedes our understanding of whether EPP varies across environments and why. We report on rates of EPP and the potential underlying mechanisms for the observed rate in the Black-crowned Antshrike (Thamnophilus atrinucha, previously known as the Western Slaty Antshrike), a Neotropical and socially monogamous ...

Extra-pair paternity in two sympatric Aegithalos tits: patterns and implications

The explanation for extra-pair paternity (EPP) variation continues to attract research interest in the area of avian breeding systems. Comparisons among closely related species are recommended to explore factors that affect EPP rate variations. We utilised microsatellite markers to investigate extra-pair paternity in two sympatric populations of congeneric Black-throated Tits, Aegithalos concinnus, and Silver-throated Tits, A. glaucogularis. The two species share a similar breeding period at our study site and have helpers during breeding at some nests. The results suggest that the two species had low levels of extra-pair paternity: 5.7 % of the offspring in the Black-throated Tits and 6.8 % of the offspring in the Silver-throated Tits. The proportion of broods with extra-pair paternity in the Silver-throated Tits (33.3 %) was higher overall than the Black-throated Tits (17.2 %). This difference is consistent with the prediction by their different male attendance of incubation, but failed to be explained by major ecological factors. On the one hand, we conducted the study at the same site during the same time, which therefore limited the potential effect of different environmental conditions and habitat on their EPP incidence. On the other hand, other factors such as the inter-nest distances failed to explain the observed pattern. Current results also could not rule out an effect of evolutionary history on the EPP patterns of these two related species. Our research on their cooperative breeding system found a low proportion of cooperative breeding nests with offspring sired by helpers (Black-throated Tit, 8.3 % and Silver-throated Tit, 25.0 %), indicating that a direct reproductive benefit is not a likely major reason for the existence of the helpers in these two species.

Causes of extra-pair paternity and its inter-specific variation in socially monogamous birds

Based on molecular technology, researchers find that extra-pair paternity (EPP) prevails among socially monogamous bird species. This phenomenon challenges traditional views of sexual selection and mating system, and has become one of the hot-spots in the avian behavior ecology. This review focuses on the evolutionary causes leading to EPP and the potential factors affecting it. Early studies of EPP in birds used a wide variety of tools, including plumage color polymorphism, polymorphic enzymes, and sex-differences in estimation of the heritability of morphological traits. Although each of these methods can be used to estimate the likelihood that EPP are present or absent in a population, none of them provide enough accurate estimation to allow meaningful cross-species comparison. Currently, studies of EPP mainly use “DNA-methods”, namely multi-locus mini-satellite fingerprints, single-locus mini-satellite fingerprints, and micro-satellite genotyping, because they can provide accurate outcome of paternity identification and their results are reproducible. From the point of the female, the driving forces for EPP are that females may gain direct benefits or indirect genetic benefits from EPP. Hypotheses explaining the benefits include fertility assurance, good genes, genetic compatibility, and genetic diversity. Despite large numbers of theoretically plausible explanations for EPP, there have been few direct empirical tests that can provide unambiguous support for only one type of explanation. The most straightforward test of the genetic benefit hypothesis of extra-pair copulation is a comparison of the performance of maternal half-siblings from multiply sired broods. Some highly-cited landmark studies spectacularly support the genetic benefit hypothesis, while other studies failed to reveal any systematic differences in maternal half-sibling performance, even in the same species or in taxonomically closely-related species. Briefly, the point that purpose of extra-pair copulation is to gain genetic benefits is still facing great challenges. Therefore, some researchers suggest that more attention should be focused on the interactions between parties involved in the extra-pair paternity phenomenon. Others, however, believe that such interactions can also be of a cooperative nature, and involve exchange of direct benefits. In brief, an approach focusing on interactions (involving either conflict or cooperation) seems to be the most promising direction to improve our understanding of the phenomenon of extra-pair paternity. As for the factors leading to intra- and inter-specific variation in the level of EPP, current researches mainly focus on the breeding density, breeding synchrony, the complexity of the habitat, paternal care, adult mortality, food availability, and genetic diversity. Explaining intra- and inter-specific variation in the extent of EPP has been difficult, but an appreciation of the problems of small sample sizes, and an ever-increasing comparative database have led to several recent advances. It now seems probable that differences between species in the rate of EPP are due to a combination of differences in life history, pattern of parental care, and local opportunities for promiscuity. In a word, although there have been a lot of theoretical and empirical researches about EPP of birds, no consensus on the basic questions has been received in this area. Thus, more scientific statistical analysis method and more empirical experiments are still badly needed to improve the theoretical system.