Rates Of Extra-pair Fertilization Research Articles

Using Microsatellite DNA to Understand Bobwhite Behavior and Population Structure (Post Abstract)

Northern bobwhite (Colinus virginianus) have a flexible mating system with varying degrees of parental investment in offspring. Questions of relatedness of mates and the dynamics of covey membership have not been answered. It is not known how different patterns of mating systems impact productivity of bobwhite populations. In addition to behaviors, the genetic structure of bobwhite populations likely varies across landscapes, and may depend on the distribution and abundance of habitat types. These issues have critical conservation and management implications, such as the impact of habitat fragmentation on gene flow. Recent advances in molecular techniques provide an opportunity to investigate these questions through examination of small, repetitive, highly variable regions of DNA known as microsatellites. Microsatellites provide the fine-scale resolution needed to objectively understand certain population structures and reproductive strategies. Microsatellite analysis techniques have been used successfully to research relatedness and extra-pair paternity of a number of species. Therefore, we have begun to investigate the genetic basis for many northern bobwhite behaviors related to reproduction. Our primary objectives are to determine: (1) relatedness of individuals within coveys and groups over time, (2) relatedness between reproductive pairs relative to random pairings, (3) relatedness of chicks in broods, (4) rates of extrapair fertilization, (5) rates of intra-specific nest parasitism, and (6) the relatedness of incubating birds to their eggs. To do so, we have developed a series of microsatellite markers for northern bobwhites. We radiomarked approximately 75% of bobwhites on our study area at Tall Timbers Research Station. We collected body feathers from adults and 1.5 mm patagial micro-biopsies from each chick (4 days old) found brooding with radiomarked adults for microsatellite analysis. We are determining relatedness and parentage, based on these microsatellite data, using programs RELATEDNESS and CERVUS. Additionally, we are testing our tissue collection techniques on a pen-reared population of bobwhites to determine the efficiency of DNA amplification via the polymerase chain reaction for 4 tissue collection techniques: patagial micro-biopsy, down and feather shaft, egg tooth, and egg membrane. Additionally, we are pairing pen-reared adult hens and males for different periods of time to determine the presence of sperm storage and test for evidence of sperm competition. Further, we are crossing individuals of known relatedness over several generations to test the accuracy of paternity inferences calculated by CERVUS with respect to bobwhite microsatellite data. Finally, by collecting feathers from hunterkilled bobwhites throughout the Red Hills and the southeast, we will compare the genetic structure of the bobwhite population(s) of the Red Hills, likely the last panmictic population in the southeast, to more isolated, declining populations. In our poster we present a detailed description of this research along with first year results.

The effects of anthropogenic alteration of nesting habitat on rates of extra‐pair fertilization and intraspecific brood parasitism in Canada Geese Branta canadensis

Parentage studies have shown that alternative reproductive strategies are widespread in many avian taxa that were once thought to be monogamous. Recent anthropogenically mediated habitat change may have disrupted ecological factors, such as breeding density, which have given rise to inter‐ and intraspecific variation in the frequency of extra‐pair fertilization (EPF) and intraspecific brood parasitism (IBP). We used genetic analyses to quantify the incidence of alternative reproductive strategies exhibited within clutches of Canada Geese Branta canadensis maxima nesting in high‐ and low‐density situations in and around urban areas in southern Michigan, USA. We tested the hypothesis that high nesting density would increase the frequency of EPF and IBP. There were no significant differences in rates of EPF and IBP clutches (14 and 26% of clutches, respectively) from nests in high‐density (21.7% EPF, 21.7% IBP) vs. low‐density (5.3% EPF, 31.6% IBP) areas, although high‐density sites had a fourfold higher rate of EPF. Rates of EPF and IBP in high‐density urban areas in Michigan were comparable to rates observed in other species nesting under different ecological conditions. Levels of relatedness between host and parasitic females were higher than expected by chance, suggesting that related females are more tolerant of one another and that host females could gain inclusive fitness benefits from rearing parasitic offspring. Our study highlights the importance of understanding the different costs and benefits associated with alternative behavioural repertoires that may vary as habitats and associated selection pressures are increasingly modified by human activities.

Breeding Strategies of a Socially Monogamous Neotropical Passerine: Extra-Pair Fertilizations, Behavior, and Morphology

AbstractBlue-black Grassquits (Volatinia jacarina) are small, granivorous, Neotropical birds that are abundant in central Brazil. During the reproductive season, the socially monogamous males acquire a blue-black plumage and defend very small, clustered territories that resemble leks. They execute a conspicuous courtship display that consists of a leap, revealing white under-wing patches, synchronized with a vocalization. We collected data on the morphology and behavior of banded males and characteristics of their territories to determine how these factors may influence acquisition of mates and nesting. For a second group of birds in the area, we used microsatellite genotyping to test the breeding synchrony hypothesis, which predicts that tropical species that breed synchronously should exhibit high rates of extra-pair fertilization (EPF). We found that males that successfully formed a pair bond differed from unsuccessful males in their behavior, but not in morphological attributes or territory features. Successful males spent more time in their territories, executed displays for longer periods and at greater rates, and their display leaps were higher. These results point to the greater importance of behavior relative to other factors in the successful reproduction of Blue-black Grassquit males. In the second group of birds, EPFs occurred in 63% of 11 nests and involved 50% of the 20 chicks sampled. This exceptionally high incidence of EPF in the small sample analyzed occurred in diverse contexts, including intraspecific parasitism and quasi-parasitism, a rare type of maternity loss where the resident female is parasitized by other females that were fertilized by the resident male. A short and highly synchronized breeding season, clustered breeding in small territories, and granivorous habits may contribute to the high rates of EPF in this tropical species.

The Strength of Direct Selection against Female Promiscuity Is Associated with Rates of Extrapair Fertilizations in Socially Monogamous Songbirds

A costs-benefits approach has frequently been used to understand the evolutionary origin and maintenance of promiscuity in animal populations. Recent meta-analyses suggest that direct costs to unfaithful females outweigh indirect benefits from infidelity in socially monogamous songbirds, suggesting that in this taxa, extrapair fertilization (EPF) evolved primarily as a self-interest male tactic. Here we present results of comparative analysis to show that standardized selection gradients acting against female infidelity (direct costs of promiscuity) explain variation in EPF rates at an interspecific level in passerines. This result confirms that costs to females resulting from reduced parental care from cheated males constrain promiscuity in this group. Our data indicate that females exert resistance over EPFs when the costs of infidelity are high and, conversely, that the rate of EPFs increases when selection on females to defend themselves against EPF attempts by males is weak and costs of infidelity are low.

Social and Genetic Monogamy in Territorial and Loosely Colonial Populations of Phainopepla (Phainopepla Nitens)

Abstract We observed courtship and copulatory behavior in two populations of Phainopeplas (Phainopepla nitens) with contrasting social systems and used multilocus DNA fingerprinting to assess rates of extrapair fertilization (EPF). Phainopeplas from both territorial and loosely colonial populations copulated infrequently (≤2 times per day). No extrapair copulations (EPCs) were observed in either population. We found no evidence of EPFs in 48 nestlings from 25 nests. Thus, Phainopeplas appear to be both socially and genetically monogamous. However, Phainopeplas are not monogamous over their lifetimes—they do not retain mates from year to year and appear to switch mates between breeding localities within the same year. Compressed breeding seasons, geographically shifting food resources, and widespread breeding failures may favor monogamy during any given breeding attempt while allowing opportunities to switch mates between breeding localities and years.

GENETIC EVIDENCE FOR EXTRAPAIR PATERNITY IN THE TUFTED TITMOUSE

Abstract Until now, there have been no reports of extrapair parentage in Tufted Titmice (Baeolophus bicolor). During 1995–1998, we used multilocus minisatellite DNA fingerprinting to estimate paternity and degree of relatedness in eight central Ohio broods of this socially monogamous species. Our results suggest a rather low rate of extrapair fertilization in the study population; three of 34 nestlings could not be attributed to the attending male. Of the three extrapair offspring, two represented the entire brood in a nest attended by their mother and a nonparental male that appeared to be a close relative of the mother.

Genetic paternity analyses in Little Owls (Athene noctua): does the high rate of paternal care select against extra-pair young?

Previous studies have shown that extra-pair fertilizations are much less frequent in Non-Passeriformes, especially in raptors, than in Passeriformes. Low breeding densities, high breeding synchrony and high rates of paternal effort have been discussed as possible causes of these low extra-pair fertilization rates. Using DNA fingerprinting, we studied the mating system of Little Owls (Athene noctua) in a population of relatively high breeding density and comparatively low breeding synchrony. We found no cases of extra-pair fertilization among 53 nestlings of 16 breeding pairs. We conclude that paternal effort is probably the most important factor in preventing extra-pair fertilizations in Little Owls.

High frequency of extrapair fertilization in a plural breeding bird, the Mexican jay, revealed by DNA microsatellites

We used tetra-nucleotide microsatellite DNA typing to estimate the frequency of extrapair fertilization (EPF) in a plural breeding species, the Mexican jay, Aphelocoma ultramarina, in Arizona. We found EPF in 32 of 51 complete broods (63%) and 55 of 139 nestlings (40%) for which the putative father had been identified (one of the highest rates of EPF known for birds). At least 96.1% of EPF fathers came from within the group. This is by far the highest known within-group EPF rate among socially monogamous, communally rearing species. Most (70%) males of breeding age (3+ years) had no genetic paternity in a given year. Social fathers (i.e. those with nests and mated females) rarely obtained EPFs; of 25 social fathers, 23 had young in only one nest and only two had young in two nests by virtue of EPF. Of the 27 males known to be EPF fathers without a nest of their own, none had young in more than one nest. Only 7% of EPF fathers had their own broods reaching banding age (day 14), compared with 29.7% of social fathers. The proportion of EPF young was significantly larger in smaller broods. Breeding females in all age classes were equally likely to have EPF young.

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.

Species Differences in Male Parental Care in Birds: A Reexamination of Correlates with Paternity

Avian species differ markedly in the extent to which males contribute to pre- hatching and posthatching parental care. In a recent comparative study, Moller and Birkhead (1993) concluded that diversity in male parental care was associated with differences among species in extrapair paternity. Specifically, their results showed a significant inverse rela- tionship between extrapair paternity and male contributions to feeding of nestlings. We used a revised and updated data set in an attempt to replicate their study. In contrast to their results, we found no evidence that the evolution of male posthatching care was strongly cor- related with paternity. Instead, our results showed that male participation in incubation tends to be negatively associated with extrapair fertilization rates, thereby providing ten- tative support for Ketterson and Nolan's (1994) hypothesis that this particular form of pa- rental care may be especially restrictive to male extrapair mating activities. Received 15 Sep-

Breeding synchrony and EPF rates: the key to a can of worms?

Given that roughly 95% of bird species are classified as ‘monogamous’1, some might claim that the class Aves is short on mating system diversity. Whatever the group might lack in this respect, however, is offset by rather impressive species differences in the prevalence of covert matings by females. By a recent count2, extra-pair fertilization (EPF) rates range from 0 to 76% across avian species, with the mean for all species at about 13%.

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

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

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

Increased opportunities for cuckoldry may be why dominant male fairy-wrens tolerate helpers

The highest known rates of extra-pair fertilization (76%) occur in the superb fairy-wren ( Malurus cyaneus) , a bird that lives in both breeding pairs and in cooperative groups where 2-5 males assist a single female. Males living in groups are cuckolded more often than males in pairs, apparently because females can rely on helpers as an alternative source of care, and so do not need to allow their mate fertilizations. It is therefore unclear why dominant males tolerate helpers. Here we show that dominant males with helpers provide less parental care during the nestling period, and use this reduced workload to make extra-territorial forays which are used to court extra-group females. DNA fingerprinting suggests that this increased display rate provides them with an advantage in obtaining extra-group copulations. These data suggest that within-pair and extra-pair paternity will not always be positively correlated.

Extra-pair relations in zebra finches: differential male success results from female tactics

Abstract. Extra-pair courtship and copulatory patterns were examined in a freely breeding laboratory population of wild-type, domesticated zebra finches, Taeniopygia guttata. Prior to release into the experimental aviary, each male received either two red bands (shown previously to be attractive in heterosexual tests) or two green bands (unattractive to females) as part of a unique combination of four leg bands; the remaining two bands were of neutral colours. Females received neutral combinations. Bill colour, which also affects heterosexual attractiveness, was also scored. Bill colour had only minor effects here, but band colour effects were substantial. Red-banded males participated in unforced extra-pair copulations more commonly than did green-banded males. Band colour did not influence male participation in forced extra-pair copulations. Mates of red-banded males (red-mated females) deterred extra-pair courtship more than green-mated females; green-mated females participated in extra-pair courtship and extra-pair copulation more frequently. Results indicate that females displayed active choice of extra-pair copulatory partners and employed conditional tactics for obtaining these partners. Males showed little differentiation in extra-pair tactics based on attractiveness or mating status. However, assuming that rates of extra-pair fertilization are proportional to rates of extra-pair copulation, red-banded males would appear to have both higher paternity confidence and greater success in obtaining extra-pair fertilizations.

Extra-pair paternity in monogamous tree swallows

Abstract. Multilocus DNA fingerprinting of offspring of monogamous pairs of tree swallows, Tachycineta bicolor, revealed that 50% (8/16) of broods contained young sired by extra-pair males, totalling 38% (33/86) of all offspring analysed. No young resulted from intraspecific brood parasitism. The distribution of extra-pair paternity showed a bimodal pattern; either none or many illegitimate young per brood. Thirty-three per cent of illegitimate offspring were sired by three to five nearest male neighbours. Females copulated frequently with their own mate at their own box, but they were never seen copulating with other males. Hence, there was a striking contrast between the rate of extra-pair copulation and the rate of extra-pair fertilization. There was no relationship between the pair copulation rate and the proportion of illegitimate young in a brood, suggesting that males cannot use the number of copulations performed with their mate as a reliable cue to their share of paternity. Males provisioned their young at nearly the same rate as did females, and males with illegitimate offspring in their nest did not reduce provisioning effort compared to males with only legitimate offspring. Hence, females did not suffer any apparent costs of promiscuity. It is argued that females control the sperm transfer success of copulations. Because females do not receive anything other than sperm from extra-pair copulation, the promiscuous behaviour is probably driven by some genetic factors enhancing female fitness. Although the data presented seem consistent with female choice for male genetic quality, there were no detectable phenotypic characteristics of males with high fertilization success.