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

Acta Ecologica Sinica 33 (2013) 158–166

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Causes of extra-pair paternity and its inter-specific variation in socially monogamous birds Dongmei Wan ⇑, Peng Chang, Jiangxia Yin Key Laboratory of Animal Resource and Epidemic Disease Prevention, Department of Life Science, Liaoning University, Liaoning Province, Shenyang 110036, China

a r t i c l e

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Article history: Received 9 December 2011 Revised 11 September 2012 Accepted 20 November 2012

Keywords: Monogamy Birds EPP Fertility assurance Genetic benefits Ecological pressure

a b s t r a c t 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. Ó 2013 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

1. Introduction As a behavioral strategy, mating system plays an important role in animal reproductive process. It is resulted from the evolution ⇑ Corresponding author. Tel.: +86 13840022402. E-mail address: [email protected] (D. Wan).

process and is closely related with natural selection. As an evolutionary strategy, mating system is the outcome of animals’ adaptation to the natural environment and intra-population environment [1]. Avian mating systems generally fall into four categories: monogamy, polygony, polyandry, and promiscuity. Monogamy is one of the most common form of mating system, with about 92% of bird species are monogamous [2]. The

1872-2032/$ - see front matter Ó 2013 Ecological Society of China. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.chnaes.2013.03.006

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application of molecular techniques has revolutionized our view of avian mating systems. The phenomenon that copulation occurring outside of the pair-bond and resulting in extra-pair offspring is common, suggesting that the social mating systems identified on the basis of behavioral observations may not always accord with the actually genetic mating system. The phenomenon that females copulate with extra-pair males is defined as the extra-pair copulations (EPCs), and the results that resulting in extra-pair fertilities (EPFs) and ultimately extra-pair young (EPY) caused by extra-pair copulations is named extra-pair paternity (EPP) [3]. In fact, EPC exist in monogamous, polygynous, and polyandrous species, but are most common in monogamous mating systems [4]. Study of extra-pair copulations and causes of extra-pair paternity and its inter-specific variation is currently one of the hot spots in avian behavior and ecological research. 2. EPP in monogamous birds DNA fingerprinting analysis reveals that EPP occurs rarely in non-passerine birds, especially in raptors [5], but prevails in small socially monogamous passerine birds, such as tree swallow (Tachycineta bicolor), northern house martin (Delichon urbica), asian stubtail (Cettia squameiceps), purple martin (Progne subis), superb fairy–wren (Malurus cyaneus), hooded warbler (Wilsonia citrina), and great reed warbler (Acrocephalus arundinaceus) [6]. Early studies of EPP in birds used a wide range of methods, including plumage color polymorphism [7], polymorphic enzymes, and sex-differences in estimates of the heritability of morphological traits [8]. Each of these methods can be used to examine the probability of occurrence of EPP in a population. Nevertheless, none of them is robust enough to make cross-species comparisons. For example, plumage polymorphism is striking in a few bird species but cannot be used as a general approach for all species. On the other hand, allozyme variation is widespread across avian species but it is a variation by itself. Thus, using this method cannot identify paternity accurately. Heritability estimates are difficult to obtain for many avian populations, and sex differences in heritability estimates are easily affected by the defect of statistical confidence limits and other factors (such as environmental effects). Given the shortcomings of above mentioned methods, the current studies of EPP mainly use ‘‘DNA-methods’’, such as multi-locus mini-satellite fingerprints, single-locus mini-satellite fingerprints, and micro-satellite genotyping [9]. Compared with other methods, the molecular methods can improve the accuracy and repeatability of paternity identification. Stewart et al. [10] found that 34 of 305 nestlings (11.2%) were the result of extra-pair fertilizations; and 21 of 79 broods (26.6%) had at least one extra-pair nestling in eastern bluebirds (Sialia sialis). Kudernatsch et al. [11] demonstrated that 26% of the offspring in 46% of the broods were sired by other males rather than the social fathers in Northern Wheatear (Oenanthe oenanthe). Lubjuhn et al. [12] analyzed paternity of great tits (Parus major) and found that each year 27.8–44.2% of broods contained at least one nestling that derived from a male other than its social father. Rätti et al. [13] reported that 11% of offspring resulted from EPF, and that 22% of broods included extra-pair young (EPY) among 36 nests containing 223 nestlings in the pied flycatcher (Ficedula hypoleuca). Similar studies had been investigated in yellow-rumped flycatcher (Ficedula zanthopygia) [8], house wren (Troglodytes aedon) [14], with the results showing that 20–40% of offspring was sired by extra-pair males. Females nurtured a large number of extra-pair yearlings in these bird species. 3. Initiator of the extra-pair copulations The female is a key player in the process of interacting among female-pair male-extra-pair male and in the generation of EPP. A

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female encounters an extra-pair male in two ways: she can stay home and wait for males that moving to her or she can move away from the area she normally uses and into areas containing extra-pair males (a foray). Male forays that lead to EPC are the most commonly observed extra-pair events in birds. For the total of 43 species showing the phenomenon that males foraying into a fertilizable female’s area, EPP occurs in 39 species. For those species that male mate guarding was low, field observation found that all EPC were initiated by intruding males and none occurred through female forays [15]. However, female can also be the initiator of EPC and may even prevail in many of these species. Female forays are quite rare and cryptic, but have a disproportionate effect on EPP [15]. To date, there have been more than 10 species for which female forays and genetic evidence of EPP have been described. For example, radio transmitters were used to track females of superb fairy– wrens (M. cyaneus). Females moved directly to the extra-pair territory and then returned home immediately. Although copulations have not be observed in the day, males in the visited territory sired some of the female’s offspring [16]. In black-capped chickadees [17], females briefly foray into other territories, usually those of neighbors, and copulate with the local resident male whose sites contain little food or nesting material. These studies suggest that females move away from their own territories to seek EPC. In several other birds, females initiate EPC but little or no EPP occurs (e.g. northern fulmar (Fulmarus glacialis) [18]; oystercatcher (Haematopus ostralegus) [19]). Therefore, data about female forays leading to EPP are still badly needed. 4. Causes of EPP The process that ejaculates from two or more males compete to fertilize the ova of a particular female is referred as sperm competition [20]. The potential for sperm competition in birds is high because, unlike most mammals, female birds can store sperm for prolonged periods and ejaculates from different males may coexist in the female reproductive tract at the same time. Sperm competition occurs not only among birds with polyandrous mating systems, but also among monogamous species, because EPC is frequent despite a range of paternity guards, and EPC usually results in EPP. Sperm competition is the fundamental of sexual selection. It leads to the differential reproductive success of individuals. Male adaptations to sperm competition include relatively large testes, large sperm stores and long spermatozoa, mate guarding, and frequent pair copulations. Females show no obvious morphological adaptations to sperm competition, whereas they probably determine its frequency and extent by controlling whether copulations are successful. It is the sperm competition that makes EPP possible in socially monogamous bird species. Why do the social monogamous birds seek EPC and produce the EPO? From the perspective of males, they can enhance their lifetime reproductive success by pursuing extra-pair copulations with non-mate females, as long as the costs are not higher than the benefits from EPC, then this behavior will have adaptive value. What benefits can females obtain from EPC? Some researchers proposed that females may gain direct or indirect benefits. 4.1. Direct benefits According to the fertility assurance hypothesis, females seek EPC as an insurance against infertility of their mate. If females could copulate with no less than two males, then, it would increase the probability of eggs which are all fertilized [21]. Fertility assurance is important for maintaining the fitness of females. However, little is known about infertility in wild birds. Some studies indicate that permanent sterility may occur, but temporary infertility

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caused by injury, diseases, or parasites may be more common [22]. There have been few tests of the fertility insurance hypothesis, but some evidence is provided by studies on house sparrows (Passer domesticus) [23] and red-winged blackbirds (Agelaius phoenicus) [24]. Paternity assurance is critical to male fitness, particularly in species that females frequently participate in EPC and males provide costly parental care. In response to fitness loss due to cuckoldry, several types of paternity assurance behavior have evolved. One strategy is constant mate guarding. Males can protect their paternity by ensuring that no other male has an opportunity to mate with their paired female [25]. However, for some species, constant mate guarding may be constrained by territory protection or other activities, as mate guarding is time-consuming. When mate guarding cannot avoid the occurrence of loss of paternity, males will adopt another strategy, namely, frequent copulations. Males copulate frequently with their paired females to avoid being cuckolded [26]. Crowe et al. [27] examined copulation behavior in the socially monogamous tree swallow (T. bicolor). They found that the frequency of within-pair copulation attempts increased and peaked just before the appearance of the first egg. When the first egg was laid, the frequency of copulation attempts would be reduced significantly. Hoi et al. [28] proposed that male used two alternative strategies, namely frequent copulation and mateguarding to assurance infertility in house sparrows (P. domesticus). At the beginning of the fertile period, pairs at the dense colony started to copulate at a higher rate than those of the medium-sized colony and solitary breeding pairs. Male house sparrows seem to adjust their strategies according to the breeding density. Both strategies can be alternatively used in the weak fertile period but are simultaneously used in the peak fertile period [28]. A special case of the fertility insurance hypothesis is the phenotype-linked fertility hypothesis [29], which states that if functional fertility co-varies with male phenotype, females may obtain both direct and indirect benefits by performing EPC with attractive males. This means that support for the good genes hypothesis also could be support for the phenotype-linked fertility hypothesis, thus it would be difficult to distinguish those two hypotheses. 4.2. Indirect genetic benefits The premise of indirect genetic benefits is that females can obtain benefits from copulations with extra-pair males. There are three main hypotheses about the indirect benefits: (1) Good genes hypothesis [30]. Good gene is defined as an allele that increases fitness, diploid organisms, including the homologue to the particular good allele. Across the genome, good genes will show additive genetic variation. The premise of the good genes hypothesis is that good genes are beneficial to all females. This hypothesis assumes that females paired with lower genetic quality would solicit the extra-pair copulations, and extra-pair males should differ from within-pair males in a trait reflecting genetic quality. (2) Genetic compatibility hypothesis [31]. Compatible gene is defined as an allele that increases fitness when in a specific genotype. Across the genome, compatible gene will show non-additive genetic variation. In contrast to good genes models, the genetic compatibility hypothesis does not require that the genetic quality of some males be intrinsically superior, rather it proposes that male genetic quality depends upon the interaction between male and female genotypes. According to the genetic compatibility hypothesis, there is no single best male in the population; a male’s quality is relative to each female. Therefore, a male that is compatible with one female may be incompatible with

another. If a female mates with two males, only one of which is compatible, she can exert some post-copulatory control so that her eggs are fertilized by the compatible male [32]. (3) Genetic diversity hypothesis [33]. It is demonstrated that females can modify the diversity among offspring through EPC, the heterozygosity of EPO should be higher than that of WPO. Genetic diversity among offspring should increase the probability that some offspring will survive, in unpredictable especially fluctuating environments. 4.2.1. The good genes hypothesis The good genes hypothesis is one of the main explanation for the mechanism of females’ involving in EPC. The good genes model is based on two fundamental assumptions: (1) females improve their offspring’s fitness if they copulate with males who have better genes than those of their bonded males; (2) qualities of phenotypes and genotypes strongly correlate. These assumptions make three predictions upon which most tests of the good genes function are based: (1) Extra pair offspring (EPO) should have, on average, better fitness than within pair offspring (WPO). (2) Only females bonded to poor quality males should be engaged in EPC. (3) These females should only do it with extra-pair males who are phenotypically superior to their bonded males. The good genes hypothesis assumes that females mating with males of higher genetic quality through engaging in EPC could obtain genetic benefits for their offspring, and that males of high genetic quality could also increase the number of their sons through seeking EPC [34]. Some studies support the point. For example, Kempenaers et al. [35] proposed that males of blue tit (Parus caeruleus) that did not lose paternity would be more likely to survive to the next breeding season than males that lost paternity. Johnsen et al. [36] found enhanced cellular immunity in EPY compared with WPY in the bluethroats (Luscinia svecica); Dunn et al. [37] reported that nestlings had a stronger immune response in nests with at least one extra-pair nestling than in nests with all within-pair nestlings in socially monogamous tree swallows (T. bicolor). According to the good genes hypothesis, if extra-pair males are more attractive and hold higher genes quality than pair males, sons benefit more than daughters from inheriting their father’s attractiveness traits. If the breeding value of a certain gender is larger than that of the other, parents should show an increasing tendency to bias the production of their young toward one sex or the other. If males of high quality pass on their high quality to his sons, the reproductive value of sons would, thus, be likely to exceed that of daughters. Accordingly, females should bias their broods towards sons, that is the sex allocation theory [38,41]. Svensson and Nilsson [39] provided the first evidence that phenotypic quality of fathers contributes to the sex ratio variation in a wild population. They showed that females of blue tit mated to males with high survivability bias sons of their broods [39]. Dreiss et al. [40] found that the length of the strophe bout of fathers was positively related with the proportion of sons in their broods, but they found no significant difference in sex ratio between within-pair and extra-pair chicks. However, Dietrich-Bischoff et al. [41] found no evidence for a male-bias in EPO sex ratios compared to their within-pair maternal half-siblings in the coal tit and thus, they did not support the sex allocation they concluded that the goal of extra-pair copulated may be not for obtaining attractiveness genes. Results from some studies do not support the good genes hypothesis. For example, Lee [42] conducted genetic parentage analyses in vinous-throated parrotbills (Paradoxornis webbianus), and they found that females did not obtain good genes, extra-pair

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young were not better than within-pair young in terms of their body condition at the nestling stage or their survival rate to their first winter. O’Brien and Dawson [43] found no evidence that EPO exhibited enhanced immune responses, grew more rapidly, or fledged in a better condition relative to their within-pair nest mates in the tree swallows (T. bicolor). Recently, Arnqvist and Rowe [44] pooled data from 12 species to have a comparative analysis, and they found that extra-pair paternity is correlated with loss of paternal care in those species. Thus, they concluded that females were unlikely to benefit from engaging in extra-pair copulations, and that such copulations should instead be regarded as a result of sexual conflict, where male strategy is actually harming the females benefits. 4.2.2. The genetic compatibility hypothesis According to the genetic compatibility hypothesis, females possess cellular and cytological mechanisms by which the compatibility of male genotypes can be assessed directly. Thus, selection for genetic compatibility does not use indicators, but relies on direct assessment [32,45]. The choice of a compatible mate can occur either before copulation, based on phenotypic cues, or after copulation, based on interactions between sperm and the female reproductive tract [46]. Increasingly, evidence is being found in many taxa for the latter mechanism, being referred as cryptic female choice [47]. Compatibility does, however, not equal with dissimilarity. The relationship between genetic dissimilarity and offspring fitness is such that the highest level of fitness (compatibility) is achieved at intermediate levels of genetic dissimilarity [48]. In the low dissimilarity end of the continuum, reproduction between close relatives yields low fitness, as reproduction does between species in the other end of the continuum. Even within populations, maximal genetic dissimilarity between parents might not yield the highest fitness of offspring [49]. Females are predicted to pursue extra-pair copulations to increase the chances of securing paternal contribution that is more compatible with their own contribution [32]. Inbreeding is one form of genetic incompatibility, so females may benefit from EPP by decreasing the inbreeding level of their offspring. Although still being poorly supported, this inbreeding avoidance hypothesis has received some support in both socially monogamous birds. Stapleton et al. [47] tested the genetic compatibility hypothesis in tree swallows over five breeding seasons using data from ten micro-satellite loci. They found that 47% of offspring were the result of extra-pair fertilizations and that 83% of females produced at least one extra-pair offspring. In accordance with the genetic compatibility hypothesis, they also found that EPO were more heterozygous than WPO. However, Barber et al. [50] found that genetic similarity of a social pair, as measured by multi-locus DNA fingerprints in the same population of tree swallows, tended to be negatively related to the proportion of extra-pair young within broods, which do not support the genetic compatibility hypothesis. The compatible genes hypothesis is a relative newcomer to the extra-pair paternity literature, but several studies have now accumulated. In practice, most studies of the compatible genes hypothesis use relatedness or genetic similarity between partners as the test variable. Empirical tests of the compatible genes hypothesis are similar to those of the good genes hypothesis, with one important difference when comparing extra-pair young and within-pair young: under the compatible genes hypothesis, in addition to having higher fitness than their maternal half-sibs, extra-pair young can also have higher fitness than their paternal half-sibs. Recently, investigators began to consider whether good genes and compatibility processes may operate simultaneously [51]. These two hypotheses are not mutually exclusive, females can use both methods and may adjust their choice depending on conditions.

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If good genes are termed as additive genetic variance in fitness and compatibility is termed as non-additive genetic variance in fitness, good genes and genetic compatibility are, by definition, uncorrelated. Actually, females might use both criteria in mate choice [52]. By combining information about additive genetic quality and about compatibility of potential mates, a female might have offspring with higher fitness than by using either criterion alone. Katsura et al. [53] indicated that in a system with apparent precopulatory female choice for good genes, a post-copulatory mechanism may still promote the production of offspring that carry compatible genes. Neff and Pitcher [51] assumed that females obtained benefits from mating with multiple males, females mating with neighbor males may be the result of pursuit for the good offspring, whereas females mating with non-neighbor males might be the result of seeking for heterozygous offspring, therefore, the good genes and the genetic compatibility hypothesis could explain the causes of females mating with different males among the same populations. 4.2.3. The genetic diversity hypothesis The genetic diversity hypothesis assumes that most females in a population may purse EPC with multiple males in order to increase the genetic diversity of their offspring; that EPY is distributed randomly among broods; that females enrich genotypes without engagement; and EPP varies with the extent to what females control fertilization, which is restricted by mate guarding and other costs [54]. However, according to the good genes hypothesis, EPY would not be randomly distributed among broods, but be more frequent in broods where the female bonded to a male of low quality. Consequently, the most crucial factor to distinguish between the genetic diversity hypothesis and the good genes hypothesis is whether EPY is distributed randomly among broods. If females seek extra-pair copulations to increase the diversity of offspring’s genotypes, thus we can expect that females mate with more than one males, and that EPY do not derive from the single extra-pair males, and that EPY are more heterozygous than WPY; however, if females solicit extra-pair copulations to increase gene quality of offspring, and females will choose single males (good or compatible males) as fathers for EPY. Kudernatsch et al. [11] found that some females chose more than one male as the father for EPY in a population of the Northern Wheatear (O. oenanthe), this was in accordance with the genetic diversity hypothesis. However, they also found that some females chose only single male as father for EPO, this tends to support the good genes and the genetic compatibility hypotheses, but opposes the genetic diversity hypothesis. Another contradictory result is that EPO were not distributed randomly among broods, this result also reject the genetic diversity hypotheses. The most crucial test methods to object to the genetic diversity hypothesis is that EPY were not more heterozygous than WPY. However, most of the studies on EPP in birds do not support or even reject this hypothesis, such as house sparrow [55]. Up to now, the evidence that supports the genetic diversity hypotheses is rare in the study on EPP in birds. 5. Causes of the intra- and inter-specific variation in EPP Research shows that the factors leading to intra- and inter-specific variation in the levels of EPP seem to be the breeding density, breeding synchrony, the complexity of the habitat, paternal care, adult mortality, food availability, genetic diversity, and so on. 5.1. Breeding density From the field observation, extra-pair copulations are more common among colonially nesting species than among species

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with more dispersed nests based on an extrapolation. Møller and Birkhead [56] proposed a hypothesis that interspecific variation in the rate of EPP is linked to breeding density. Such an extrapolation assumes that the rate of EPP is closely correlated with the rate of extra-pair copulation, and that colonially nesting species are typical of high nesting density species. However, when these assumptions have been tested using molecular data and a more sophisticated interspecific comparative analysis, no robust evidence has been found for a relationship interspecific variation in the rate of EPP and breeding density [9]. Charmantier and Perret [57] tested the effect of manipulation of breeding density on the occurrence of extra-pair paternity in a blue tit population with a correlative approach. Results showed that the proportion of extra-pair young in broods was affected by the number of breeding neighbors within 100 m around the nest-box, by the distance to the nearest breeding neighbor. When density was high, there were more extra-pair young in broods, but the number of extra-pair fathers did not increase and stayed close to one. The nearest neighbors accounted for only 39.3% of extra-pair paternities and distance of extra-pair fathers was significantly higher than the nearest neighbor distance. This may indicate that the effect of density on the occurrence of extra-pair paternities is associated with active female choice. The relationship between breeding density and the rate of EPP is quite complicated, with positive (e.g. Yellow Warbler (Dendroica petechia) [58]), no relationship (e.g. house swallows (P. domesticus) [59]) and negative relationship (e.g. great reed-warbler (A. arundinaceus) [60]) have been found. There are several reasons for the lacking of a consistent relationship between breeding density and EPP: (i) most of the published studies are observational rather than experimental; (ii) the published studies have low statistical power due to the small number of populations involved; and (iii) the tests fail to control the large standard error around the estimates of EPP [9]. In summary, there is little evidence that interspecific variation in the rate of EPP is due to variation in breeding density. 5.2. Breeding synchrony Breeding synchrony refers to the proportion of females that are fertile at any one moment in time, so that high synchrony refers to a situation where many females are reproductively active at the same time [9]. The hypothesis of breeding synchrony was first championed by Stutchbury et al. who showed a positive correlation between these two variables in 21 genera of passerines. Based on this evidence, Stutchbury and Morton [61] suggested that in a synchronously breeding population, females are better able to compare between different males, facilitating their choice of extra-pair partners. Unfortunately, however, their original analyses were unable to control for two factors that may potentially jeopardize the validity of the correlation: the phylogenetic relationships between species in the analysis; and the measurement error around the estimates of EPP. After controlling for the phylogenetic non-independence, Stutchbury show a significant correlation between breeding density and the rate of EPP, leading them to claim that the breeding synchrony hypothesis remains the most viable explanation of the great variation in EPP frequency among bird species worldwide [62]. However, Weatherhead and Yezerinac [63] argued that, if the level of synchrony generally does drive variation in levels of EPP between species, there should also be a relationship between populations within a species or among individuals within a population. In an experimental study, Hoi-Leitner et al. [64] aimed to test whether an alteration of local breeding synchrony by means of acceleration and postponement of egg laying could generate differences in the rate of EPP in House Sparrows, they swapped nest

material between the nests of neighbors to change its breeding period and found that higher occurrence of EPY within broods was associated with laying order. The latest broods within a local nesting aggregation contained significantly more EPY than those of earlier breeding pairs, but there was no clear evidence for breeding synchronization. Overall, there was much debate about the breeding synchrony in determining interspecific variation in EPP. 5.3. The complexity of the habitat Sherman and Morton [65] proposed that the complexity of habitat could influence the success of EPP, such as male’s ability of mate guarding. In a comparative study, Blomqvist et al. [66] found that species breeding in closed habitats had higher EPP rates than those breeding in more open habitats. Mate guarding was also more frequent in closed habitats, but not high copulation rates. These relationships, however, were influenced strongly by taxonomic position, particularly by differences between passerines and non-passerines, implying that phylogeny and traits associated with it play an important role in explaining the occurrence of EPP and paternity guards. Such a comparison is also biased because the level of EPP depends not only on habitat visibility and female opportunities but also on male intruders and the frequency of intrusions which may be influenced by other variables than habitat visibility. In a word, the idea that complexity of habitat influences the level of EPP had not been generally accepted by most of people. 5.4. Paternal care Another factor leading to the variation in the level of EPP can be parental care. There might be a negative correlation between high rates of EPP and little requirement for paternal care. The core of this hypothesis is that females should be more likely to seek EPCs when they can rear offspring with little help from their male partner, and can therefore risk the cost of reduced parental care. The hypothesis was first proposed by Birkhead and Møller [67], who used a species-based comparative approach to show that EPP rates tend to be comparatively low in species where male care is essential. However, their analysis was quite preliminary and without testing for the effect of phylogenetic non-independence. Therefore, Arnold and Owens [68] performed a phylogeny-based comparative analysis to test whether high rates of EPP really are associated with little need for paternal care. As predicted, studies found that interspecific variation in the rate of EPP significantly correlated with paternal care. Hoi-Leitner et al. [64] manipulated the abundance of food around the nest in the serin (Serinus serinus). As predicted by the paternal care hypothesis, females breeding in areas of high food abundance were indicted to have a higher occurrence of EPO in their broods. In summary, the evidence that the link between the need for paternal care and the rate of EPP is still insufficient. There was more difficulty in the aspect that parental care may play in explaining variation among more closely related species, or among populations of the same species, or even among individuals within the same population. 5.5. Adult mortality Another factor that has been suggested to explain interspecific variation in the rate of EPP is the rate of adult mortality. Based on a series of state-dynamic models, Mauck et al. [69] proposed that males of species with short reproductive lifespans should tolerate higher EPP rates than those with long reproductive lives. Thus, there should be greater range of EPP rates for species with short than long reproductive life spans, high rates of EPP will only

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be evolutionarily stable in species with short reproductive lifespans. They found that EPP rates in passerine birds range from 0% to more than 70%, whereas in long-lived birds such as procellariiformes, and EPP rates range from 0% to 14%. With a species-based comparative method, Mauck et al. [69] tested the prediction of an association between EPP and adult mortality rates, they confirmed that variation in the rate of adult mortality explained nearly 50% of the variation in the rate of EPP. In species with annual mortality rates of less than 30%, the rate of EPP very rarely higher above 20%; whereas in species with a higher rate of mortality, the rate ranges from 0% to 95%. The use of phylogeny-based comparative methods also supported the association. When evolutionarily independent contrasts are used to control for the effects of phylogeny, changes in the rate of adult mortality still account for approximately 25% of variation in changes in the rate of EPP [69], which agrees with the results from Bennett and Owens [70] that both EPP rates and life history traits show extensive variation at the same ancient phylogenetic levels . To our knowledge, there has been no experimental test for a causal relationship between the rate of mortality and the rate of EPP. Because the logic of this argument is based on changes over an evolutionary timespan, rather than facultative changes within an individual, such tests would not be straightforward. Other than by using long-term selection experiments, it may not be able to perform elegant manipulations of life histories that last over tens of generations. We therefore conclude that, as with the parental care hypothesis, there is robust correlative evidence in support of a link between adult mortality and EPP, but lacking of experimental evidence for the causal nature of this relationship. 5.6. Food availability The influence of food availability on EPP has already been discussed in the section related to parental care. Some experimental studies revealed that manipulating food supply could affect the level of EPP, although with contrasting results. This may be due the different breeding situation (solitary or colonial) and food supplementation may affect either females and their EPP behavior or males and their abilities of guarding paternity [64]. 5.7. Genetic diversity Based on the difficulties of traditional ecological hypotheses such as breeding density and breeding synchrony in explaining the variation, some researchers suggest that the key factor in determining interspecific variation in EPP may be genetic rather than ecological. After the tests of genetic diversity hypothesis in intra-and interspecific level, Petrie et al. [71] proposed that most females in a population may seek EPC with multiple males to produce extrapair paternity, local genetic structures may shape the amount of benefits that females accrue through EPP. A low frequency of extra-pair paternity will be predicted in species with low genetic diversity, because females may hardly benefit from EPC with males genetically similar to their social partners. Øigarden et al. [72] reported a low frequency of EPP (2% extra-pair offspring) in a Norwegian population of the white-throated dipper (Cinclus cinclus), their results supported the genetic diversity hypothesis that predicts a low frequency of EPP in species with low genetic diversity. However, Christin et al. [73] made a comparative study of frequency of EPP between mainland and island populations, they found that the differences between mainland and island populations in the rate of EPP was not significant, although the diversity of island populations was much lower than that of mainland populations, this might suggest that there was no special island effect which can affect the frequency of EPP, thus they did not support the

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genetic diversity hypothesis. In addition, Lee [42] found no significant effect of local genetic diversity on the occurrence of EPP in vinous-throated parrotbills, and thus, they also did not support the genetic diversity hypothesis. To sum up, there was no consensus on the idea of the genetic diversity determined the interspecific variation in EPP. 5.8. Hierarchical explanation Griffith et al. [9] pooled previous review of the various explanations for variation in the rate of EPP and come to the conclusion that there was no single explanation for this EPP phenomenon, because none of these hypotheses could provide an overwhelming evidence to explain the inter-specific variation across all levels containing among major avian lineages, among closely related species, among populations of the same species and among individuals within a single population. For example, Arnold and Owens [68] suggested that the level of differences in EPP between species might be explained by differences in fundamental life history parameters such as adult mortality rate and the form of parental care. The level of variation in EPP among closely related species and between populations of the same species may be more likely to be influenced by contemporary ecological factors such as breeding density, breeding synchrony, and the extent of genetic variation. Thus, according to these inconsistent results, they suggest a hierarchical explanation for variation in EPP, with variation at different organizational levels determined by different ecological, genetic and social correlates. Bennett and Owens [70] proposed that reason of variation in the rate of EPP between species were more likely to be differences in the probable costs of extra-pair behavior, parental care and reproductive history, and that variation in the rate of EPP among populations of the same species or among individuals in the same population, on the other hand, were more likely to be determined by the opportunity to indulge in alternative reproductive strategies. 6. Problems in the research of EPP and its inter-specific variation in socially monogamous birds So far, despite the large number of theoretically plausible explanations for EPP, there have been few direct empirical studies that have provided unambiguous support for only one type of explanation. The reasons for this phenomenon may be: (1) failure to gather sufficient types of data to differentiate between different hypotheses; or (2) failure to use an experimental approach to control for potentially confounding factors. The interpretation of the idea that females engage in extra-pair copulations to obtain good genes can be problematic, because: First, good genes effects are likely to be small which explain an average of just 2% of the variation in offspring viability, thus numerous sample sizes are required to attain sufficient statistical power. Second, although it is commonly assumed that good genes effects are equated with survivorship, such genes may show their effects through an alternative mechanism such as high fecundity. Therefore, a lack of good genes effects may simply be due to the absence of a more diverse and complete set of fitness measures. Of course, someone may argue that the good genes hypothesis need not explain extra-pair paternity in all species, but it may be valid only in a subset of species. To be complete and testable, this argument needs a ‘meta-theory’ that specifies when the good genes hypothesis is important and when not. We are unaware of any such proposal, provided one that predicts the good genes hypothesis should be more important when additive genetic variation is higher [33]. Regardless of the truth of the good genes hypothesis, the point of a meta-theory predicting different selection pressures in different taxa and contexts is appealing. The most

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straightforward test of the genetic benefit hypothesis is the comparison of the performance of maternal half-siblings from multiply sired broods. The biggest limitation on the study of EPP is that a lack of the data about differences between EPO and WPO. Evidence for a genetic type of benefit based on maternal half-sibling comparisons is rather mixed across studies. Some highly cited landmark studies spectacularly support the genetic benefit hypothesis. In contrast to these findings, other studies failed to reveal any systematic differences in maternal half-sibling performance, sometimes in the same or in closely related species [19,74]. Furthermore, application of identical experimental protocols (e.g. the phytohemagglutinin test of cellular immunocompetence) in different species with similar extra-pair mating systems produced mixed results [75,76]. The inconsistence of results across EPP studies may be caused by methodological challenges and/or reflect true and meaningful differences in the respective. Some factors may affect the validity of estimation of genetic benefits. For example, several studies that compared singly mated females multiply mated females were unable to control for potential differences in direct benefits such as the number of spermatophores which females receive, however, direct benefits could increase the fitness of the offspring independent of its genetic quality and could result in an overestimation of genetic benefits. In other words, when mating has direct costs to the female, such as sexually transmitted diseases, it is possible that these costs could lead to reduced offspring fitness and an underestimate of genetic benefits. And females may also invest disproportionately in offspring based on their genetic quality by providing more resources to offspring of high genetic quality [77]. A second difficulty with many of the studies of genetic benefits is their ignorance of genetic  environmental interaction effects on fitness. The interaction effect occurs when the quality of a gene or genotype varies across environmental contexts. To some extent, although most genes or genotypes will vary in quality across environments, few studies calculate fitness of individuals in multiple environments. Recently, some researchers propose a concept that the magnitude of genetic fitness benefits from extra-pair mating may depend on the environmental context, the context dependency of the genetic effects of extra-pair mating behavior may offer an opportunity for explaining inconsistent results from different extra-pair paternity studies within and across species. Unfortunately, to date, context-dependent genetic effects in maternal half-sibling comparisons have been demonstrated for only five passerine bird species [77]. None of these studies, however, has experimentally manipulated the environmental dimensions (e.g. food availability, abundance of parasites) and, therefore, the results are open to different alternative explanations. Furthermore, these studies did not control for the effects of maternal investment and hatching sequence. However, in none of the studies were the crucial environmental conditions experimentally manipulated, and the potentially confounding effects of differential maternal investment in relation to paternity were also largely not accounted for. If females selectively bias their EPO, superior EPO performance may at least partly be due to maternal rather than paternal genetic effects. Therefore, differential maternal investment with respect to paternity may have the potential to confound paternal genetic effects on offspring fitness. Recent studies suggesting that EPO occur earlier in the laying order and, accordingly, in the hatching sequence than their WPO maternal half-siblings, giving them an advantage in sibling competition [78,79]. For example, Magrath et al. [78] not only demonstrated that EPO hatch slightly earlier than WPO, but also that statistically significant differences between maternal half-siblings in morphology and survival until fledging tend to diminish once hatching sequence is statistically controlled for. At present, it is unclear whether females time EPC to occur early in their laying phase, whether these sequence effects

reflect mating effort patterns of social or extra-pair sires or whether they simply represent a by-product of social or ecological constraints on EPC behavior. That might indict that such effects may confound paternal genetic effects on offspring fitness, possibly leading to an overestimation of paternity. Therefore, evidence for context-dependent genetic benefits from extra-pair mating in birds is more likely to be suggestive rather than conclusive, and it is unclear how important and how widespread context-dependent genetic effects of extra-pair mating may actually be. Currently, there are two main ways by which these ideas can be tested – firstly, by use of the comparative method and secondly by experiment. Comparisons between populations of the same species or between sister species have fewer interpretation problems and have yet to be widely used to test some of the more likely ideas, however, this means is prone to be affected by the size of samples and statistical analysis methods, thus the results of comparative analysis have certain limitations. In addition, many studies use a large number of unpublished statistic results deriving from the study of level of EPP, thus, it may affect the reliability of the intraand inter-specific variation in the level of EPP. Experimental studies would be a good choice, however, they rest heavily on the assumption that females are sensitive to the created population differences and that their behavior towards extra-pair partners is not fixed, therefore, it is uncertain whether the results of experimental studies can truly reflect the real situation. 7. Prospects Reproduction is an absolute temptation for all the organisms. Living creatures can adopt all possible strategies to obtain the reproductive opportunities. As an behavioral strategy, mating system plays an important role in the process of animal reproduction. EPP is widespread and common in socially monogamous birds, and it is a powerful source of pre- as well as post-copulatory sexual selection. Therefore, it is hard to understand avian mating systems and sexual selection without understanding the evolutionary causes and consequences of this phenomenon. Despite the substantial research efforts in the field, there is still no consensus on a number of fundamental questions related to this topic. For example, there is sustained debate about which sex is actually in control of EPC behavior, and about the adaptive significance of extra-pair mating behavior for female birds [15,34]. A number of different hypotheses have been put forward to explain why female birds mate extra-pair, which have been discussed in detail above. In fact, the view that females involved in the extra-pair copulations to get genetic benefits remains a great challenge. Westneat and Stewart [15] proposed that more attention should be focused on the interactions between parties involved in the extra-pair paternity phenomenon. However, Akçay et al. suggest that such interactions could also be of a cooperative nature, and involve exchange of direct benefits. In summary, an approach focusing on interactions (involving either conflict or cooperation) seems to be one of the most promising direction to improve our understanding of the phenomenon of EPP [34]. With the widely application of molecular technology in the study of EPP, data about parent–child relationship are easier to collect and more diverse. Up to now, there have been more than 150 published literatures about the rate of EPP in birds, resulting in a large interspecific database and these data spur a substantial comparative analysis. However, our understanding of inter-specific variation in the rate of EPP is still based largely on statistically inadequate tests. Explaining interspecific variation in the extent of extra-pair paternity has proved difficult, but an appreciation of the problems of small sample sizes, and an ever-increasing comparative database, have led to several recent advances. It seems that differences between species in the rate of EPP are probably

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