Extra-pair Fertilizations Research Articles

Sperm competition in birds.

Sperm competition in birds occurs when a female is inseminated by more than one male during a single breeding cycle. Despite most birds being socially monogamous, sperm competition is widespread and results in frequent extra-pair paternity. Sperm competition is a fundamental part of sexual selection since it results in differential reproductive success among males. 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 but, by controlling whether copulations are successful, they probably determine its frequency and extent. Despite this, the evolutionary benefits females acquire from extra-pair fertilizations are poorly understood. Experiments in which females are inseminated with equal numbers of spermatozoa from two males usually show last male sperm precedence. Understanding the mechanism of sperm competition requires understanding of why the last male to inseminate a female fertilizes a disproportionate number of eggs. The data from sperm competition studies on the domestic fowl, turkeys and zebra finches are consistent only with a passive sperm loss model of sperm competition. The mechanism is as follows: after insemination, spermatozoa enter the sperm storage tubules located in the oviduct, from which they are lost at a constant rate over days or weeks. All else being equal, the interval between two inseminations determines the probability of fertilization: the second of two inseminations fertilizes most eggs simply because, by the time fertilization occurs, fewer of these spermatozoa have been lost. Other factors also affect the outcome of sperm competition: the timing of insemination relative to oviposition, the differential fertilizing capacity of males and differences in the numbers of spermatozoa inseminated; as a consequence, last male sperm precedence is not automatic. On the basis of the mechanism of sperm competition, the optimal strategy for both males and females to maximize their likelihood of extra-pair fertilization is to copulate with an extra-pair partner as close as possible to the onset of oviposition.

Sperm competition in birds

Sperm competition in birds occurs when a female is inseminated by more than one male during a single breeding cycle. Despite most birds being socially monogamous, sperm competition is widespread and results in frequent extra-pair paternity. Sperm competition is a fundamental part of sexual selection since it results in differential reproductive success among males. 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 but, by controlling whether copulations are successful, they probably determine its frequency and extent. Despite this, the evolutionary benefits females acquire from extra-pair fertilizations are poorly understood. Experiments in which females are inseminated with equal numbers of spermatozoa from two males usually show last male sperm precedence. Understanding the mechanism of sperm competition requires understanding of why the last male to inseminate a female fertilizes a disproportionate number of eggs. The data from sperm competition studies on the domestic fowl, turkeys and zebra finches are consistent only with a passive sperm loss model of sperm competition. The mechanism is as follows: after insemination, spermatozoa enter the sperm storage tubules located in the oviduct, from which they are lost at a constant rate over days or weeks. All else being equal, the interval between two inseminations determines the probability of fertilization: the second of two inseminations fertilizes most eggs simply because, by the time fertilization occurs, fewer of these spermatozoa have been lost. Other factors also affect the outcome of sperm competition: the timing of insemination relative to oviposition, the differential fertilizing capacity of males and differences in the numbers of spermatozoa inseminated; as a consequence, last male sperm precedence is not automatic. On the basis of the mechanism of sperm competition, the optimal strategy for both males and females to maximize their likelihood of extra-pair fertilization is to copulate with an extra-pair partner as close as possible to the onset of oviposition.

Sex-role reversal and the absence of extra-pair fertilization in Wilson's phalaropes

Extra-pair fertilizations are common in birds, which has led to great interest in how this phenomenon is regulated at a proximate level and how extra-pair fertilizations, and extra-pair fertilization avoidance, shape avian social systems. In Wilson's phalaropes,Phalaropus tricolor, incubation and brood-rearing is performed exclusively by males. Males are able to rear only a single brood of four during a breeding season. This suggests that males have a high level of paternity in clutches and broods under their care and, thus, that extra-pair fertilizations are infrequent. In contrast, female social dominance, lack of territoriality and frequent interactions among breeding adults suggest that both males and females have the opportunity to engage in extra-pair copulations. Using DNA fingerprint band-sharing between putative parents and offspring, we found no evidence of extra-pair fertilizations among 51 offspring from 17 families of phalaropes. Copulation disruption by non-copulatory adults, ability of females to reject copulation attempts and potential fitness benefits to females by avoiding extra-pair fertilizations were sufficient to explain the absence of extra-pair fertilizations in Wilson's phalaropes. We propose that sex-role reversal affects the relative costs and benefits to females of seeking extra-pair fertilizations. At the time of clutch completion, females have invested particularly heavily in their clutches due to intense competition among females to gain and keep a mate during the pre-laying and laying periods. After clutch completion, nest success requires significant male parental care. Benefits to females in gaining extra-pair fertilizations may be offset by the risk of losing male parental care.

Behavioural correlates of testosterone and seasonal changes of steroids in red-winged blackbirds

I studied the relationship between behaviour and plasma testosterone level (T) and the seasonal changes in T and plasma corticosterone levels (B) in male red-winged blackbirds,Agelaius phoeniceus. I measured T and B using radioimmunoassay, and on the day after taking blood, I observed each male's behaviour for 60min. The time that males spent conspicuously perched and the number of songs were positively correlated with T, but the proportion of time spent conspicuously perched and the frequency of song were not correlated with T. The frequency of aggressive encounters, sexual chases, epaulet exposure when singing and flights within the territory were positively correlated with T, suggesting a direct role for circulating testosterone influencing male aggressive behaviour. Both T and B increased early in the breeding season, peaked when the first females were receptive, and decreased through the remainder of the breeding season. Late in the season, the presence of a receptive female caused males to have increased T. The peak in T when the first females were receptive, the positive correlation between aggression and T, and the response to a receptive female with increased T support predictions of the challenge hypothesis. T was positively correlated with B, suggesting a cost to the males of maintaining high T. When a receptive female was present on the male's territory, T was negatively correlated with date. Male red-winged blackbirds in Indiana may respond less to receptive females late in the season when benefits associated with protecting paternity and gaining extra-pair fertilizations decrease.

Extra-pair mating effort of male hooded warblers,Wilsonia citrina

Few researchers have been able to quantify the time or effort expended by male birds in seeking extra-pair copulations with neighbouring females. In this study, we radio-tracked male hooded warblers, to determine the frequency and duration of intrusions onto neighbouring territories. Extra-pair fertilizations are common in hooded warblers, with 35% of females producing extra-pair young. Males intruded onto territories where females were nest building more often than expected by chance and approached females during most intrusions (78%), suggesting that these intrusions were extra-pair copulation attempts. Almost all intrusions (96%) were to adjacent territories, and males made an average±seof 0.4±0.2 forays/h and spent 4.7±2.6% of their time off-territory. Males were involved in fights or chases with the resident male in 21% of intrusions, but were apparently undetected during most intrusions. Males with high intrusion effort onto neighbouring territories had the lowest rate of intrusions onto their own territory by other radio-tracked males. Males varied extensively in their intrusion effort, but this was not significantly correlated with male body mass, age or song rate. The percentage of time spent intruding onto other territories was small (0–8%), so males probably do not face strong trade-offs between making extra-pair copulation forays and other activities like mate guarding and feeding offspring.

Breeding synchrony and extrapair fertilizations in two populations of red-winged blackbirds

We tested the relationship between synchrony of breeding and the frequency of extrapair fertilizations (EPFs) in two populations of red-winged blackbirds known to differ in female extrapair behavior. We found no association between the number of simultaneously fertilizable females (temporal neighbors) and EPF rate in either population, although a significant difference between populations in the direction of this relationship (positive where females initiated extrapair copulations and negative where males initiated them) suggested a modest difference in the influence of synchrony. Males losing offspring to EPFs tended to have more fertilizable females at that time than the actual sires in some analyses but not in others. We also tested several assumptions underlying two competing hypotheses for the effects of synchrony. We found no evidence that females pursued extrapair copulations more often when other females were synchronous. Rather, females were more likely to gain EPFs with extrapair males whose social mates were not yet building their nests. Synchrony also did not consistently affect male pursuit of extrapair copulations or achievement of EPFs. These results suggest that timing of breeding has some effects on extrapair activity, but that those effects are both relatively weak and influenced by other factors that vary between years or populations.

Extrapair paternity, inclusive fitness, and within‐group benefits of helping in western bluebirds

In central coastal California, USA, 3–16% of western bluebird (Sialia mexicana) pairs have adult male helpers at the nest. Demographic data on a colour‐ringed population over a 13‐year period indicate that helpers gain a small indirect fitness benefit through increases in the number of young fledged from nests of close kin. A small proportion of adult helpers (16%) that were able to breed and help simultaneously had higher annual inclusive fitness than males that only bred. These males comprised such a minor proportion of helpers that the mean fitness of helpers was still lower than the mean fitness of independent breeders. We used DNA fingerprinting to determine whether extrapair fertilizations alter within‐group benefits enough to tip the balance in favour of helping behaviour. Overall, 19% of 207 offspring were sired by males other than their social father and extrapair fertilizations occurred in 45% of 51 nests. Intraspecific brood parasitism was rare so that mean mother‐nestling relatedness approximated the expected value of 0.5. Extrapair paternity reduced putative father‐offspring relatedness to 0.38. Mean helper‐nestling relatedness was 0.41 for helpers assisting one or both parents and 0.28 for helpers aiding their brothers. Helpers rarely sired offspring in the nests at which they helped. Helping was not conditional on paternity and helpers were not significantly more closely related to offspring in their parents’ nests than to offspring in their own nests. Although helpers may derive extracurricular benefits if helping increases their own or their father's opportunities for extrapair fertilizations, within‐nest inclusive fitness benefits of helping do not compensate males for failing to breed. Breeding failure and constraints on breeding are the most likely explanations for why most helpers help.

Costs and Benefits of Extra-Group Paternity in Superb Fairy-Wrens

One of the most extreme examples of conflict between the sexes occurs in the Superb Fairy-wren {Malurus cyaneus), a cooperatively breeding bird in which 72% of nestlings were produced by extra-pair fertilizations. Males that gained extra-pair paternity were almost exclusively dominant breeding males out- side the group and not helpers. Group size had a significant effect on the number of young sired by males on their own territory. Males breeding in a pair (no helpers) sired more young (41%, 71/175 young) and provided more parental care (42% of feeding visits) than dominant breeding males that lived in groups with helpers (19%, 56/292 young; 25% of feeding visits). This pattern of extra-group paternity was a result of female choice and control of fertilization. When females lived in a group, helpers compensated for the lower parental assistance of the dominant breeding male, so all offspring were provisioned fully and there was no cost to the female or male in terms of reduced nestling survival. Thus, the mate choice of females with helpers was not constrained by the importance of male parental assistance. In unassisted pairs, females had no alternative source of pa- rental assistance and may have allowed their mates greater paternity to ensure the assistance of the mates in providing parental care. The reduced workload of dom- inant breeding males in groups did not increase their survival; rather, it allowed them more time to engage in courtship displays to females on other territories. This increased display rate of males in groups was associated with a greater likelihood of gaining extra-group fertilizations, and it may have compensated males in groups for their lower within-pair paternity. The release of females from the constraint of male parental care was due to helpers, whereas the reduction in male parental care was most likely the result of a paternity cue and not simply the presence of helpers per se. After controlling statistically for group size, males provided less parental care when they had lower paternity. Thus, a detailed knowl- edge of the alternatives available to females (other sources of parental assistance) and males (opportunities for extra-pair matings) may be necessary to understand male and female reproductive strategies.

Genetic monogamy in blue-headed vireos and a comparison with a sympatric vireo with extrapair paternity

Based on the breeding synchrony hypothesis, we predicted, in two congeners that nest in simiilar habitat but differ in nesting synchrony, that blue-headed vireos (Vireo solitarius) would have fewer extrapair fertilizations (EPFs) thaii red-eyed vireos (V. olivaceus EPFs were rare in blue-headed vireos (1/37 nestlings), but common in red-eyed vireos (11/19 nestlings). We studied the behavior of blue-headed vireos to determine what factors could promote genetic monogamy. We found no evidence that males mate guarded to prevent extrapair copulations from occurring. Males did not follow fertile mates closely when mates left the nest (14–25% of female departures) and, during the egg-laying period, males were often alone on the nest (22.3 mm/h). Female blue-headed vireos, but not red-eyed vireos, obtain direct benefits from social mates such as nest building and incubation (49.1% of the total), and they assess male quality long before becoming fertile. Female blue-headed vireos spent more time incubating when their mates had low incubation effort. Furthermore, male incubation effort was positively correlated with nest survival during incubation. We discuss the evolution of genetic monogamy and sex role convergence in blue-headed vireos in relation to asynchronous breeding.

Emerging Themes and Questions in the Study of Avian Reproductive Tactics

Many researchers have explored the ramifications of the idea that extra-pair copulation (EPC) is a male reproductive tactic to obtain parentage while avoiding parental investment since this concept was advanced by Trivers in 1972. Consortship between males and their fertile mates has been interpreted almost exclusively in terms of mate guarding by males. Females have been thought to benefit little, if at all, from extra-pair activities. This mindset has persisted and influences our interpretation of patterns of reproductive success revealed by molecular markers. Here we briefly trace the historical development of this line of reasoning and the newer, contrasting view well represented in this volume that females as well as males have EPC tactics. We identify specific contributions made by authors in this volume, contrast their approaches, and discuss the implications of their results for the understanding of avian mating systems and the role of sexual selection in avian social evolution. Finally, we illustrate the richness of this collection of papers by expanding on key points. This volume had its origins in a symposium on Avian Tactics for Extra-Pair Mating organized by Patty Parker at the request of Thomas C. Grubb for the 1995 AOU meeting in Cincinnati, Ohio. Cognizant of the increasing number of substantial data sets showing that rates of extra-pair fertilization (EPF) are commonly much higher than was expected even a few years previously, Patty invited participants with such data sets, fully expecting to find that patterns of EPF would be interpreted in a variety of ways. What emerged in the symposium, however, was a clear and compelling empirical consensus: acquisition of multiple genetic mates is a female reproductive tactic in avian species having a diversity of social mating systems (monogamy, polygyny, promiscuity) and social organizations (cooperative breeders, territorial species, gregarious and colonial species). This consensus is reinforced by several recent papers (e.g., Gowaty and Bridges 1991; Kempenaers et al. 1992; Lifjeld and Robertson 1992; Wagner 1992; Burley et al. 1994, 1996; Lifjeld et al. 1994; Stutchbury et al. 1994). This idea provides a sharp contrast to the prevailing view, briefly discussed below as well as by several contributors to this volume (Johnson and Burley, Chapter 2; Ketterson et al., Chapter 4; Stutchbury and Neudorf, Chapter 5), that selection on males is the

The Relative Impact of Extra-Pair Fertilizations on Variation in Male and Female Reproductive Success in Dark-Eyed Juncos (Junco hyemalis)

The Relative Impact of Extra-Pair Fertilizations on Variation in Male and Female Reproductive Success in Dark-Eyed Juncos (Junco hyemalis)

Paternal care declines with increased opportunity for extra–pair matings in fairy martins

Following the discovery that extra-pair fertilizations are common in many birds, it has been predicted that male participation in parental care may be influenced by their opportunity for extra-pair copulations. However, such a trade-off between male contribution to parental care and the availability of fertile females has not been confirmed. Here we use a novel remote monitoring technique to show that participation in incubation by male fairy martins, Hirundo ariel, declines with the increasing availability of fertile females in the breeding colonies. Furthermore, male contribution to incubation is most responsive to change in the availability of fertile females in the early morning, when most copulations occur, and also if their clutches are smaller than average. Both of these patterns support the presence of a trade-off between parental and extra-pair copulation effort. We suggest that this trade-off may be widespread among the 90% of bird species where males contribute to parental care.

Testosterone affects reproductive success by influencing extra–pair fertilizations in male dark–eyed juncos (Aves:Junco hyemalis)

Monogamous male birds typically allocate less effort to courtship and more to parental behaviour than males of polygynous species. The seasonal pattern of testosterone (T) secretion varies accordin...

Extra-pair paternity and tail ornamentation in the barn swallow Hirundo rustica

Females of socially monogamous species may copulate with attractive non-mates to obtain access to the genes of such males, and a preference for attractive copulation partners may result in sexual selection. Extra-pair copulations are common in the socially monogamous barn swallow Hirundorustica, and a 2-year study of paternity using multi-locus DNA fingerprinting demonstrated that 33% of 63 broods and 28% of 261 offspring were sired by extra-pair males. The frequency of extra-pair offspring within broods was highly skewed with the majority of all broods having either no extra-pair offspring or only extra-pair offspring. Individual pairs were consistent in their frequency of extra-pair paternity among broods, and the repeatability of extra-pair paternity of multiple broods of the same female was statistically significant. The proportion of extra-pair offspring was negatively related to the tail length of the male attending the nest. Behavioural observations showed that extra-pair fertilizations were more likely in broods raised by females that had been observed to engage in extra-pair copulations. The frequency of extra-pair offspring was unrelated to the intensity of two male paternity guards, mate guarding and the rate of intra-pair copulations. In an analysis of extra-pair paternity and male parental care in different broods of the same male, male barn swallows fed their offspring relatively less frequently if the brood contained more extra-pair offspring. Therefore, female barn swallows pursue extra-pair copulations with attractive males, which may result in sexual selection, even though extra-pair paternity is costly for females due to the reduction of paternal care by their social mates.

Isolation of microsatellite DNA markers from a passerine bird, Dendroica petechia (the yellow warbler), and their use in population studies.

We describe the isolation and genetic characterization of five microsatellite loci in a passerine bird, the yellow warbler Dendroica petechia, and assess their use for various types of population-level analysis using data from two breeding populations. All five loci show levels of variability comparable to those observed in other vertebrates (Hexp = 0.388-0.989). One locus, Dp mu 05, is highly variable with 46 alleles detected in 41 individuals. All loci appeared to segregate in a Mendelian fashion as judged by patterns of inheritance in known families. However, one locus showed a significant heterozygote deficiency in one population suggesting the possible presence of null alleles at this locus. These markers provide a highly accurate system for determination of parentage in this species: the probability of detecting extrapair fertilization by males given known maternity was 0.999 in each of two separate populations. Comparison of allele frequencies and genetic distances between the two populations showed no evidence for significant differences in allele frequencies at individual loci, whereas the overall genetic distance and FST-value are significantly different from zero suggesting weak differentiation. Finally, cross-species amplification experiments showed that at least one locus appears to amplify products in a wide range of birds including nonpasserine species. Thus, our results demonstrate that these loci will provide a useful set of genetic information for addressing a wide range of population-level analyses in this and other bird species.

Isolation of microsatellite DNA markers from a passerine bird, Dendroica petechia (the yellow warbler), and their use in population studies

We describe the isolation and genetic characterization of five microsatellite loci in a passerine bird, the yellow warbler Dendroica petechia, and assess their use for various types of population-level analysis using data from two breeding populations. All five loci show levels of variability comparable to those observed in other vertebrates (Hexp = 0.388 – 0.989). One locus, Dpµ05, is highly variable with 46 alleles detected in 41 individuals. All loci appeared to segregate in a Mendelian fashion as judged by patterns of inheritance in known families. However, one locus showed a significant heterozygote deficiency in one population suggesting the possible presence of null alleles at this locus. These markers provide a highly accurate system for determination of parentage in this species: the probability of detecting extrapair fertilization by males given known maternity was 0.999 in each of two separate populations. Comparison of allele frequencies and genetic distances between the two populations showed no evidence for significant differences in allele frequencies at individual loci, whereas the overall genetic distance and FST-value are significantly different from zero suggesting weak differentiation. Finally, cross-species amplification experiments showed that at least one locus appears to amplify products in a wide range of birds including nonpasserine species. Thus, our results demonstrate that these loci will provide a useful set of genetic information for addressing a wide range of population-level analyses in this and other bird species.

Density and extra-pair fertilizations in birds: a comparative analysis

Moller and Birkhead (1992, 1993) reported that extra-pair copulations (EPCs) occur more frequently in colonial than dispersed nesting birds. We comprehensively reviewed published data to investigate how breeding density affects extra-pair fertilizations (EPFs). Within species EPFs appeared to increase with density: two of three studies on colonial breeders and six of eight on dispersed nesters showed increases in EPFs with increasing density. However, comparisons among species (n = 72) revealed no evidence that EPF frequencies correlated with (1) nesting dispersion, (2) local breeding density, or (3) breeding synchrony, even when each of these variables in turn was held constant and phylogenetic relationships were taken into account via contrast analyses. Methodological and biological reasons for the disparity between observational studies of EPCs and molecular genetic analyses of EPFs are discussed.

Song rates of dark-eyed juncos do not increase when females are fertile

Frequency of singing by birds may vary with reproductive stage in ways that reflect variation in the functions of song in intersexual and intrasexual communication. In dark-eyed juncos (Junco hyemalis) high-amplitude song is produced only by males. To investigate the function of this song, we tested whether fertility of females affected singing by their mates or by neighboring males. Using focal observations, song censuses, and radiotracking data, we determined whether song production varied between and among periods when females were fertile and non-fertile. Our findings show that males do not increase song production when their mates are fertile, nor do they increase song production when neighboring females are fertile. These results suggest that male juncos do not signal their intent to defend territories (or mates) more when females are fertile and that they do not use song to advertise to specific potential participants in extra-pair fertilizations.

Low Frequency of Extra-Pair Fertilizations in the Great Tit Parus major Revealed by DNA Fingerprinting

Multilocus DNA fingerprinting was used to estimate the frequency of extra-pair fertilizations in a low density, island population of Great Tits Parus major. A total of 69 pairs and 516 offspring from 82 breeding attempts were examined. Only 18 offspring (3.5%) in seven different nests were not fathered by the attending male. The sample included one brood in which all nine chicks were fathered by an extra-pair male. One chick from a nest of eight was the result of intra-specific brood parasitism. Three chicks from a brood of nine could be matched with the male but not with the female. Observations at this nestbox suggested that mate switching had occurred during the laying period. The percentage of extra-pair fertilizations did not differ between first clutches and (experimentally induced) replacement clutches. Females mated to small males were more likely to have extra-pair young in the nest. Because both extra-pair paternity and intraspecific brood parasitism are rare in this population, a reliable measure of reproductive success can be obtained by counting the number of offspring. [KEYWORDS: Intraspecific brood parasitism; mixed reproductive strategies; conspecific nest parasitism; eastern bluebirds; genetic similarity; female preference; sperm competition; hatching failure; sexual selection; tree swallows]

Characterization of microsatellite loci from the socially monogamous lizard Tiliqua rugosa using a PCR-based isolation technique.

The sleepy lizard Tiliqua rugosa is a large, omnivorous, viviparous skink with a wide distribution across southern Australia. Behavioural studies have shown that sleepy lizards are socially monogamous with pair fidelity over more than one mating season (Bull 1994). Social monogamy does not necessarily imply sexual monogamy and genetic analyses have revealed extra-pair fertilizations in many apparently monogamous species (Westneat & Webster 1994). In this paper we report the characterization of polymorphic microsatellite loci from T. rugosa and briefly discuss their potential use for testing whether T. rugosa is sexually monogamous. We have used a modified version of the PCR-based