Are there correlates of male Australian Magpie Gymnorhina tibicen reproductive success in a population with high rates of extra‐group paternity?

The reproductive success of a male bird is often correlated with measurable traits that predict his intrinsic quality. Females are thought to base their selection of mates on the latter's 'quality' in order to gain their 'good genes'. Male Australian Magpies Gymnorhina tibicen of the white-backed race tyrannica were trapped in two breeding seasons. Measurements were taken of morphometric and other characteristics in order to discover whether particular traits of males were associated with: (1) percentage of offspring sired in the territory, (2) number of fledglings produced in the territory per season and (3) whether females select males for their 'good genes'. There were no consistently significant correlations between any of the measured variables and male Magpie reproductive success within territories. In particular, none of the traits measured had any consistent correlation with the percentage of offspring sired in a territorial group. This was an unexpected result given that the species is strongly territorial but also engages regularly in extra-group copulations. These findings appear contrary to the predictions of the 'good genes' hypothesis. The general lack of correlation between the variables and level of genetic paternity may in fact be due to females engaging in extra-group mating primarily to avoid breeding with a close relative rather than to choose a high-quality male. In this case, males would not have to be 'high quality', but merely genetically different from the female's social mate.     

Demography of male reproductive queues in cooperatively breeding superb fairy-wrens Malurus cyaneus

1. Subordinate helpers in cooperative societies may gain both immediate and future benefits, including paternity and territorial inheritance. However, if such opportunities correlate with rank in the queue, it is unclear why such queues should be stable. 2. In cooperatively breeding superb fairy-wrens Malurus cyaneus, only males are generally philopatric, and form stable hierarchical queues for the dominant position. 3. Male opportunities for reproduction are influenced both by their dominance status within the group, and their relatedness to the breeding female. For young queuing subordinates, the breeding female is typically their mother. Because of incest avoidance, reproduction is possible only through extra-group mating, even if the dominant position is achieved while the mother is still on the territory. If the mother dies while the helper is still a subordinate, he can seek matings both outside the group, and with the unrelated replacement female within the group. Finally, males can achieve the dominant position and pair with an unrelated female by inheritance, dispersal to a neighbouring vacancy, or by forming a liaison with an immigrant subordinate female that causes fission of the natal territory. 4. On average males spent more time living with unrelated females than with their mother. Subordinate males gained no survival advantages when living with their mother rather than an unrelated female, contrary to the prediction that parents facilitate the survival of their offspring. 5. Dominants and subordinates also had similar survival. Mortality accelerated over time, probably because older males invest more in extra-group courtship display. 6. Fairy-wren queues are likely to be stable because older birds are superior, and because extra-pair mating provides direct benefits to subordinates.     

Mating system of the Eurasian badger, Meles meles, in a high density population

Badgers are facultatively social, forming large groups at high density. Group-living appears to have high reproductive costs for females, and may lead to increased levels of inbreeding. The extent of female competition for reproduction has been estimated from field data, but knowledge of male reproductive success and the extent of extra-group paternity remains limited. Combining field data with genetic data (16 microsatellite loci), we studied the mating system of 10 badger social groups across 14 years in a high-density population. From 923 badgers, including 425 cubs, we were able to assign maternity to 307 cubs, with both parents assigned to 199 cubs (47%) with 80% confidence, and 14% with 95% confidence. Age had a significant effect on the probability of reproduction, seemingly as a result of a deficit of individuals aged two years and greater than eight years attaining parentage. We estimate that approximately 30% of the female population successfully reproduced in any given year, with a similar proportion of the male population gaining paternity across the same area. While it was known there was a cost to female reproduction in high density populations, it appears that males suffer similar, but not greater, costs. Roughly half of assigned paternity was attributed to extra-group males, the majority of which were from neighbouring social groups. Few successful matings occurred between individuals born in the same social group (22%). The high rate of extra-group mating, previously unquantified, may help reduce inbreeding, potentially making philopatry a less costly strategy.     

Pre-dawn infidelity: females control extra-pair mating in superb fairy-wrens

Despite great interest in the use of extra-pair mating as a tool for examining female choice and intersexual selection, the underlying assumption of female control has proved difficult to verify empirically. We combined microsatellite genotyping and radiotelemetry of fertile females in order to investigate mate choice in superb fairy-wrens Malurus cyaneus, the bird with the highest known rate of extra-pair fertilization. All five females radio tracked during the peak of fertility, two to four days before the first egg is laid, undertook pre-dawn forays. All extra-pair young produced by the female were sired by a male visited during their forays, indicating that females control extra-pair fertilizations. In a larger sample of paternity data, some broods were sired by two extra-group males. In virtually all the cases the territory of the two sires were on an identical linear trajectory from the female's territory. This again suggests that extra-group paternity in superb fairy-wrens is directly linked to female extra-territorial forays. In other species mixed paternity has been taken to indicate that females attempt to insure against infertile pairings or try to maximize the genetic diversity of their brood. However, in fairy-wrens the likelihood of multiple extra-group paternity increased greatly as females traversed more territories in order to mate, perhaps suggesting that females which foray further are more likely to have difficulties locating the preferred male.     

Yearling male great tits, Parus major, suffer more strongly from cuckoldry than older males

In the majority of socially monogamous bird species, females have offspring sired by males other than their social mate as the result of extra-pair copulations. While it is widely recognised that there is considerable variation in the frequency of extra-pair paternity between species, between populations of a species and between individuals of a population, determinants of this variation are surprisingly difficult to establish. With respect to individual variation within a population, it is an important step to test for male and female correlates of cuckoldry to better understand the patterns as well as the adaptive significance of extra-pair mating behaviour. Here, we analysed patterns of extra-pair paternity in relation to male age, female age and their interaction in the great tit Parus major, a socially monogamous passerine with a moderate frequency of extra-pair paternity. Based on a large sample of 316 genotyped first broods from five successive years, we failed to demonstrate interaction effects of male and female age on both the proportion of extra-pair offspring and the likelihood that at least one extra-pair offspring is present within a brood. However, both the proportion of extra-pair offspring and the likelihood of paternity loss were higher for yearling as compared to older males, while this was not the case for yearling vs. older females. Furthermore, the proportion of extra-pair offspring within a brood decreased with increasing age of the attending male in within-individual analyses. We found a comparable effect also for attending females in within-individual analyses, but only when excluding two individuals with 100% extra-pair paternity. A female (extra-pair) mating preference for older males and/or a limited ability of yearling males to prevent cuckoldry in their broods could explain these age-related patterns of paternity loss. Effect sizes, however, were not particularly large and substantial residual variation within age categories suggests the importance of further yet unidentified determinants of variation in paternity loss in the study population.     

Mating system, philopatry and patterns of kinship in the cooperatively breeding subdesert mesite Monias benschi

In the first molecular study of a member of the threatened avian family, Mesitornithidae, we used nine polymorphic microsatellite loci to elucidate parentage, patterns of within-group kinship and occurrence of extra-group paternity in the subdesert mesite Monias benschi, of southwest Madagascar. We found this cooperatively breeding species to have a very fluid mating system. There was evidence of genetic monogamy and polygynandry: of the nine groups with multiple offspring, six contained one breeding pair with unrelated helpers and three contained multiple male and female breeders with related helpers. Although patterns of within-group kinship varied, there was a strong positive relationship between group size and relatedness, suggesting that groups form by natal philopatry. There was also a strong positive correlation between within-sex and between-sex relatedness, indicating that unlike most cooperatively breeding birds, philopatry involved both sexes. In contrast to predictions of kin selection and reproductive skew models, all monogamous groups contained unrelated individuals, while two of the three polygynandrous groups were families. Moreover, although between-group variation in seasonal reproductive success was related to within-group female relatedness, relatedness among males and between the sexes had no bearing on a group's reproductive output. While kin selection may underlie helping behaviour in females, factors such as direct long-term fitness benefits of group living probably determine helping in males. Of the 14 offspring produced by fully sampled groups, at least two were sired by males from neighbouring groups: one by a breeding male and one by a nonbreeding male, suggesting that males may augment their reproductive success through extra-group paternity.     

Subordinate superb fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males

Explanations of cooperative breeding have largely focused on the indirect benefits philopatric offspring gain from investing in kin. However, recent molecular studies have revealed that in many species subordinates provision unrelated offspring. This has led to the re-evaluation of the direct and indirect benefits of helping behaviour. In this study, we used microsatellite genotyping to assess the extra-group reproductive success of subordinate superb fairy-wrens (Malurus cyaneus), a species with extremely high rates of extra-group paternity. Extra-group subordinate males sired 10.2% (193 out of 1895) of all offspring sampled between 1993 and 2000 and 21.4% (193 out of 901) of all illegitimate offspring sired by known males. The extra-group success of subordinates was greatly influenced by the attractiveness of their dominant male. Subordinates of attractive dominants sired more extra-group young than did average dominants. Evidence suggests that mate choice in superb fairy-wrens is error-prone and subordinates can gain direct reproductive benefits through parasitizing the reproductive success of attractive dominants.     

EXTRAPAIR MATE CHOICE AND HONEST SIGNALING IN COOPERATIVELY BREEDING SUPERB FAIRY-WRENS

In many species of monogamous birds females copulate with males other than their social mates, resulting in extrapair fertilizations. Little is known about how females choose extrapair mates and whether the traits used to choose them are reliable indicators of male quality. Here we identify a novel male trait associated with extra-group mating success in the superb fairy-wren (Malurus cyaneus), a cooperatively breeding bird with one of the highest known frequencies of extra-group mating. Female fairy-wrens chose extra-group mates that molted earlier into breeding plumage. Males molted up to five months before the breeding season began, and only males that molted at least one month prior to its onset gained any extra-group fertilizations. This conclusion held after controlling statistically for the effect of age and social status on molt date. Once males acquired breeding plumage, they began courtship display to females on other territories. Thus, some males were displaying to females for several months before the breeding season began. This extraordinarily long period of advertisement by males may be facilitated by the long-term ownership of territories. We suggest that early acquisition of breeding plumage or the subsequent display behavior can be reliable cues for mate choice because they are costly to acquire or maintain.     

Reproductive skew and relatedness in social groups of European badgers, Meles meles

Reproductive skew is a measure of the proportion of individuals of each sex that breed in a group and is a valuable measure for understanding the evolution and maintenance of sociality. Here, we provide the first quantification of reproductive skew within social groups of European badgers Meles meles , throughout an 18-year study in a high-density population. We used 22 microsatellite loci to analyse within-group relatedness and demonstrated that badger groups contained relatives. The average within-group relatedness was high ( R =  0.20) and approximately one-third of within-group dyads were more likely to represent first-order kin than unrelated pairs. Adult females within groups had higher pairwise relatedness than adult males, due to the high frequency of extra-group paternities, rather than permanent physical dispersal. Spatial clustering of relatives occurred among neighbouring groups, which we suggest was due to the majority of extra-group paternities being attributable to neighbouring males. Reproductive skew was found among within-group candidate fathers ( B  = 0.26) and candidate mothers ( B  = 0.07), but not among breeding individuals; our power to detect skew in the latter was low. We use these results to evaluate reproductive skew models. Although badger society best fits the assumptions of the incomplete-control models, our results were not consistent with their predictions. We suggest that this may be due to female control of paternity, female–female reproductive suppression occurring only in years with high food availability resulting in competition over access to breeding sites, extra-group paternity masking the benefits of natal philopatry, and/or the inconsistent occurrence of hierarchies that are linear when established.     

Territory quality drives intraspecific patterns of extrapair paternity

Despite the potential reproductive benefits of extrapair matings,extrapair paternity rates in many avian species often vary greatlyamong populations. Although ecological factors have been shownto influence intraspecific patterns of extrapair paternity insome species, for cooperatively breeding species living in familygroups, social/demographic factors may also play a role. Thisstudy examined how ecological factors related to territory quality(vegetation cover, insect abundance) and social/demographicfactors (group size, number of breeding pairs, genetic relatedness)influenced intraspecific patterns of extrapair paternity incooperatively breeding superb starlings, Lamprotornis superbus.Superb starlings inhabit spatiotemporally variable African savannaswhere high temporal variability drives reproductive decisions(adoption of breeding roles, offspring sex allocation) and whereterritories suitable for breeding are limited. Although extrapairpaternity rates were only 14% of offspring and 25% of nests,they varied greatly among groups, ranging from 4% to 32% ofoffspring and from 7% to 60% of nests. These among-group differencesin extrapair paternity were not related to social/demographicfactors but instead to territory quality; extrapair paternitywas higher on lower quality territories (lower vegetation coverand grasshopper abundance) than on higher quality territories(higher vegetation cover and grasshopper abundance). These resultssuggest that even in a heterogeneous landscape where suitablebreeding territories are limited, subtle differences in habitatquality can have profound effects on reproductive decisionsand patterns of extrapair paternity. Understanding the interactionbetween spatial (habitat heterogeneity) and temporal (temporalvariability) environmental variation will be important for determininghow environmental and social factors drive avian reproductiveand mating decisions.     

No evidence for female kin association,indications for extragroup paternity,and sex‐biased dispersal patterns in wild western gorillas

Characterizing animal dispersal patterns and the rational behind individuals’ transfer choices is a long‐standing question of interest in evolutionary biology. In wild western gorillas (Gorilla gorilla), a one‐male polygynous species, previous genetic findings suggested that, when dispersing, females might favor groups with female kin to promote cooperation, resulting in higher‐than‐expected within‐group female relatedness. The extent of male dispersal remains unclear with studies showing conflicting results. To investigate male and female dispersal patterns and extragroup paternity, we analyzed long‐term field observations, including female spatial proximity data, together with genetic data (10 autosomal microsatellites) on individuals from a unique set of four habituated western gorilla groups, and four additional extragroup males (49 individuals in total). The majority of offspring (25 of 27) were sired by the group male. For two offspring, evidence for extragroup paternity was found. Contrarily to previous findings, adult females were not significantly more related within groups than across groups. Consistently, adult female relatedness within groups did not correlate with their spatial proximity inferred from behavioral data. Adult females were similarly related to adult males from their group than from other groups. Using R _ST statistics, we found significant genetic structure and a pattern of isolation by distance, indicating limited dispersal in this species. Comparing relatedness among females and among males revealed that males disperse farer than females, as expected in a polygamous species. Our study on habituated western gorillas shed light on the dispersal dynamics and reproductive behavior of this polygynous species and challenge some of the previous results based on unhabituated groups.     

Social status influences microhabitat selection: breeder and floater Eagle Owls Bubo bubo use different post sites

Social status can be reflected in many aspects of an individual’s behaviour and ecology, including habitat use and conspecific interactions. In territorial species where at least two social groups – breeding birds and non‐territorial floaters – are recognized, the diverse tasks associated with territorial ownership can lead territory holders to behave differently from the non‐territorial part of the population. Territory holders defend their breeding area and reproduce, whereas floating individuals are dispersing and lead a more transient life, during which they do not show any territorial behaviour even when settling in a more or less fixed area (known as the stop phase). As social interactions are based on visual and vocal cues, the use of specific sites for sending and/or receiving signals can be a crucial choice in an animal’s life. By analysing the post‐site selection of Eagle Owl Bubo bubo breeders and floaters during their nocturnal activity, we found that: (1) territory holders selected more visible and dominant posts than non‐territorial floaters; (2) the choice of posts made by floating individuals did not differ between the wandering and stop phases of dispersal; and (3) floating females intruded more frequently than floating males within a breeder’s home‐range. These findings highlight the fact that two social strategies are possible within the same species, depending on an individual’s social status and its related tasks. Breeders could take advantage of visible locations to declare their status as territory holders, whereas floaters could benefit from a more secretive life to wander unnoticed among occupied territories. This secretive life would help floaters to reduce the risks associated with conspecific aggression. Finally, the greater occurrence of floating females within breeders’ home‐ranges can be explained by the fact that female incursions in a breeder’s home‐range are less risky than male intrusions.     

Shared parentage and incest avoidance in the cooperatively breeding acorn woodpecker

Social groups of acorn woodpeckers (Melanerpes formicivorus) range in size from unaided pairs to 15 adults. Behavioural indicators of mate guarding, assumed incest avoidance and observations of egg-laying indicate that social organization ranges from monogamous pairs to groups with up to seven male and three female putative cobreeders plus up to 10 nonbreeding helpers. In addition, groups occasionally lack a putative breeder throughout the breeding season. Here we report results from multilocus DNA fingerprinting of 372 nestlings from 123 nests in groups with putative cobreeders of one or both sexes. No extra-group fertilizations were found. Putative cobreeding males within social groups shared paternity. However, the most reproductively successful male was, on average, almost three times as successful as the next most successful and additional males only occasionally sired offspring. In contrast, cobreeding females shared parentage equally. Helpers never bred incestuously when their opposite-sex parent (or another relative, such as their uncle) held breeding status in the group. However, during breeding male vacancies, 14 nestlings were produced when helper males bred incestuously with their mother. Both male and female helpers usually became successful cobreeders with their same-sex parent following replacement of the opposite-sex breeder(s) by unrelated individuals.     

The couple that sings together stays together: duetting,aggression and extra-pair paternity in a promiscuous bird species

When individuals mate outside the pair bond, males should employ behaviours such as aggression or vocal displays (e.g. duetting) that help assure paternity of the offspring they care for. We tested whether male paternity was associated with aggression or duetting in the red-backed fairy-wren, a species exhibiting high rates of extra-pair paternity. During simulated territorial intrusions, aggression and duetting were variable among and repeatable within males, suggesting behavioural consistency of individuals. Males with quicker and stronger duet responses were cuckolded less often than males with slower and weaker responses. In contrast, physical aggression was not correlated with male paternity. These results suggest that either acoustic mate guarding or male–female vocal negotiations via duetting lead to increased paternity assurance, whereas physical aggression does not.     

Territory configuration moderates the frequency of extra‐group mating in superb fairy‐wrens

The frequency of extra‐pair paternity (EPP) in socially monogamous birds varies substantially between and within species, but ecological drivers of this variation remain poorly understood. Habitat configuration could influence EPP by moderating access to extra‐pair mates, because species occupying territories in a clustered ‘honeycomb’ configuration have a larger pool of potential extra‐group mates in their immediate neighbourhood than those living in linearly arranged territories (e.g. along narrow strips of riparian or fragmented habitat). We exploited variation in the spatial arrangement of territories due to anthropogenic modification of habitat of the cooperatively breeding superb fairy‐wren Malurus cyaneus to test whether habitat configuration influenced the frequency of EPP. In this species, most paternity is obtained by males outside the social group [extra‐group paternity (EGP)]. We found that the frequency of EGP among groups living in linear strips of roadside vegetation (41% of 44 offspring) was lower than it was for groups living in clustered territories within continuous habitat (59% of 70 offspring). Differences in group size and pair relatedness did not explain differences in EGP associated with territory configuration, although the frequency of EGP was negatively correlated with pair relatedness. Our finding suggests that territory configuration can influence rates of EGP and that anthropogenic habitat fragmentation has the potential to limit access to extra‐pair mates, affecting mating systems and ultimately fitness.     

Extra-pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection

Sexual selection theory posits that ornamental traits can evolve if they provide individuals with an advantage in securing multiple mates. That male ornamentation occurs in many bird species in which males pair with a single female is therefore puzzling. It has been proposed that extra-pair mating can substantially increase the variance in reproductive success among males in monogamous species, thus increasing the potential for sexual selection. We documented the frequency of extra-pair paternity and examined its effect on variation in male reproductive success in the mountain bluebird Sialia currucoides , a socially monogamous songbird in which males possess brilliant plumage ornamentation. Extra-pair paternity was common in our Wyoming study population, with 72% of broods containing at least one extra-pair offspring. The standardized variance in actual male reproductive success (i.e., the total number of within-pair and extra-pair offspring sired) was more than seven times higher than the variation in apparent success (i.e., success assuming that no extra-pair mating occurred). Success at siring within-pair and extra-pair offspring both contributed to the variation in overall male reproductive success. Within-pair success, however, did not predict a male's level of extra-pair success, suggesting that males do not sacrifice within-pair paternity to gain extra-pair paternity. Calculation of the sexual selection (Bateman) gradient showed that males sire approximately two additional offspring for each extra-pair mate that we identified. Thus, in this sexually dichromatic species, extra-pair mating increases the variance in male reproductive success and provides the potential for sexual selection to act.     

Within‐population variation in social strategies characterize the social and mating system of an Australian lizard,Egernia whitii

The lizard genus Egernia has been suggested as an excellent model system for examining the evolution of sociality as it exhibits considerable diversity in social organization both between and within species. To date the majority of work examining the factors responsible for the evolution of sociality within Egernia has advocated a broad scale approach; identifying the social structure of specific species or populations and comparing the degree of sociality between them. However, we argue that significant advancements could also be gained by examining variation in social strategies within populations. Here we integrate a detailed, 3‐year, field‐based examination of social spacing and juvenile dispersal with molecular analyses of paternity to determine the social and mating system of a Tasmanian population of White's skink (Egernia whitii). We show that E. whitii live in small stable family groups consisting of an adult male, his female partner(s), as well as juvenile or sub‐adults individuals. In addition, while the mating system is characterized by considerable genetic monogamy, extra‐pair fertilizations are relatively common, with 34% of litters containing offspring sired by males from outside the social group. We also show that traits related to social organization (social group composition, group size, stability and the level of extra‐pair paternity) vary both between and within individuals. We suggest that ecological factors, such as habitat saturation, quality and availability, play a key role in maintaining between individual variation in social strategies, and that examining these individual level processes will allow us to more clearly understand variation in sociality among species.     

Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis)

We describe the development and initial application of a semiautomated parentage testing system in the Seychelles warbler (Acrocephalus sechellensis). This system used fluorescently labelled primers for 14 polymorphic microsatellite loci in two multiplex loading groups to genotype efficiently over 96% of the warbler population on Cousin island. When used in conjunction with the program CERVUS, this system provided sufficient power to assign maternity and paternity within the Seychelles warbler, despite the complications associated with its cooperative breeding system and a relatively low level of genetic variation. Parentage analyses showed that subordinate 'helper' females as well as the dominant 'primary' females laid eggs in communal nests, indicating that the Seychelles warbler has an intermediate level of female reproductive skew, in between the alternative extremes of helper-at-the-nest and joint nesting systems. Forty-four per cent of helpers bred successfully, accounting for 15% of all offspring. Forty per cent of young resulted from extra-group paternity.     

Microsatellite determination of male reproductive success in a natural population of the territorial ornate dragon lizard, Ctenophorus ornatus

It is now evident that the genetic mating system can be very different to the observed mating system. However, it is less well known what makes particular individuals more (or less) successful than expected from the observed system. In this study the observed territorial structure of a field population of the agamid lizard, Ctenophorus ornatus, was compared with the mating system as evidenced by microsatellite parentage assignment. This study also investigated whether any male traits predicted reproductive success. Sixty-five per cent of clutches were sired at least partially by a male other than the main territory-holding male and 35% of clutches were sired by a male with no overlap of the female's territory. Multiple paternity was moderately frequent at 25% of clutches. Male chest patch size predicted territory size and the number of females in the territory, but did not predict reproductive success. Instead, male head depth and body size were independently related to the number of offspring sired. As male head depth also predicted the number of females in a territory, these males are likely to be gaining increased reproductive success as a consequence of the higher number of females in their territories. Larger body size males, however, did not have a greater number of females in their territory and instead had more extra-territorial copulations. Whether these extra-territorial copulations are due to female choice or success in male competition is unknown.     

社会性单配制鸟类婚外父权的发生和影响因素

一雌一雄单配制鸟类中,雌性个体与配偶外雄性发生交配的行为称为婚外交配,继而导致了婚外受精产生婚外子代的现象称为产生了婚外父权。婚外父权广泛存在于鸟类中,针对其发生和影响因素已经成为了鸟类行为生态学研究的热点。本文收集了近十年社会性单配制鸟类婚外父权方面的研究文献,从婚外父权的发生及其影响因素两个方面综述了单配制鸟类婚外父权的研究进展。婚外父权发生原因的探讨主要包括：1、从两性的角度探讨雌雄两性在婚外行为中不同的进化繁殖策略。雄性策略旨在增加自身的繁殖输出;有关雌性策略则提出了确保受精假说、食物供给假说、遗传利益假说等,但目前尚存争议;2、在遗传利益假说中较常见的又分为3个假说：“优秀基因”假说、“遗传相容性”假说和“遗传多样性”假说,该三种假说是针对雌性从遗传方面获得的利益而提出的,不断有报道指出雌性配偶选择会被潜在的雄性遗传特性所影响;3、非遗传利益——母系效应影响婚外父权的进化。一些研究指出遗传质量参数,如体重、身体大小、存活率和免疫应答等方面可能会存在母系效应。婚外父权发生的影响因素这里主要指环境因素,包括繁殖同步性、繁殖密度、栖息地环境、产卵及孵化时机等。由于物种不同,受到环境压力不同,导致婚外父权发生率千差万别。最后本文针对未来的研究方向做出了展望。尽管近十年的研究进一步解释了鸟类婚外父权现象,但是该领域仍然存在并且产生了许多新的未解决的问题,而相关实验操作和理论的完善是深入探讨这些问题的关键。