Extra-pair Fertilizations Research Articles

High levels of extra-pair paternity in an isolated, low-density, island population of tree swallows (Tachycineta bicolor).

Molecular genetic studies have suggested that apparently nonbreeding males ('floaters') may account for a significant proportion of extra-pair paternity (EPP) in avian populations. Attempts to determine the influence of breeding density on EPP are therefore confounded by the presence of a subpopulation of floaters whose numbers are difficult to estimate. To study EPP in a tree swallow (Tachycineta bicolor) population with few floaters, we chose a nestbox grid on an island with an excess of available breeding sites and very few floaters. We obtained DNA samples from 13 complete families and performed DNA profiling on them using four microsatellite loci. For comparison, we also obtained a sample of 58 extra-pair young (EPY) from a mainland population typed at five microsatellite loci. Paternity assignments among resident males in both populations were made using the microsatellite profiles and a likelihood-based statistical method. Of the 67 island nestlings typed, we found 37 (55%) nestlings from 11 (85%) different nests that were EPY. The proportion of nestlings that were EPY and the proportion of broods containing EPY did not differ significantly between island and mainland populations studied previously. There was no significant difference between island and mainland populations in the proportion of extra-pair paternities assigned among neighbouring resident males. Male breeding density does not appear to affect the ability of female tree swallows to obtain extra-pair fertilizations, at least over the range of densities studied so far. The rate of EPP has remained remarkably consistent over many years, studies and populations implying an important role of active female choice in determining EPP.

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.

No Evidence for Effects of Breeding Density and Male Removal on Extrapair Paternity in the Pied Flycatcher

Abstract Molecular methods have brought new insight to the study of mating patterns. Extrapair fertilizations (EPF) have proven to be widespread among bird species irrespective of social relationships. Ecological factors, such as breeding density and synchrony, have been suggested as contributors to variation in EPF rates. Absence of a male during the female fertile period may also increase the probability of EPFs. In this study, we examined experimentally whether breeding density and male absence before egg-laying influence the EPF rate in Pied Flycatchers (Ficedula hypoleuca). DNA fingerprinting revealed that 4.4% (10/225) of nestlings were the result of EPFs and 7.0% (3/43) of broods included at least one offspring sired by a male other than that attending the nest. We did not find any evidence of higher EPF rate with higher breeding density as stated by the density hypothesis. Contrary to expectation, EPFs were more frequent, though not quite statistically significantly, at low breeding density: all three EPF nests were found in low-breeding-density areas. There was no evidence that EPF rate was affected by a 4 h male removal. In all cases of EPF, an old female was mated with a yearling male, which suggests that older females mated with browner yearling males may have adjusted their initial mate choice through EPCs to acquire indirect genetic benefits. Pied Flycatcher females may be constrained to accept a mate of lower than preferred quality, especially at low breeding density, due to the cost of searching for alternative males.

NO EVIDENCE FOR EFFECTS OF BREEDING DENSITY AND MALE REMOVAL ON EXTRAPAIR PATERNITY IN THE PIED FLYCATCHER

Abstract Molecular methods have brought new insight to the study of mating patterns. Extrapair fertilizations (EPF) have proven to be widespread among bird species irrespective of social relationships. Ecological factors, such as breeding density and synchrony, have been suggested as contributors to variation in EPF rates. Absence of a male during the female fertile period may also increase the probability of EPFs. In this study, we examined experimentally whether breeding density and male absence before egg-laying influence the EPF rate in Pied Flycatchers (Ficedula hypoleuca). DNA fingerprinting revealed that 4.4% (10/225) of nestlings were the result of EPFs and 7.0% (3/43) of broods included at least one offspring sired by a male other than that attending the nest. We did not find any evidence of higher EPF rate with higher breeding density as stated by the density hypothesis. Contrary to expectation, EPFs were more frequent, though not quite statistically significantly, at low breeding density: all t...

Does Red-Cockaded Woodpecker Excavation of Resin Wells Increase Risk of Bark Beetle Infestation of Cavity Trees?

WEATHERHEAD, P. J., AND S. B. McRAE. 1990. Brood care in American Robins: Implications for mixed reproductive strategies by females. Animal Behaviour 39:1179-1188. WESTNEAT, D. F. 1987. Extrapair fertilizations in a predominantly monogamous bird: Genetic evidence. Animal Behaviour 35:877-886. WESTNEAT, D. F. 1990. Genetic parentage in the Indigo Bunting: A study using DNA fingerprinting. Behavioral Ecology and Sociobiology 27:6776. WESTNEAT, D. F., AND E. M. GRAY. 1998. Breeding synchrony and extrapair fertilizations in two populations of Red-winged Blackbirds. Behavioral Ecology 9:456-464. WESTNEAT, D. F., AND P. W. SHERMAN. 1997. Density and extra-pair fertilizations in birds: A comparative analysis. Behavioral Ecology and Sociobiology 41:205-215. WESTNEAT, D. F., P. W. SHERMAN, AND M. L. MORTON. 1990. The ecology and evolution of extra-pair copulations in birds. Current Ornithology 7: 331-369.

MALE CHARACTERISTICS AND FERTILISATION SUCCESS IN BLUETHROATS

Abstract Extra-pair copulations (EPCs) can create or intensify sexual selection and, provided that fertilisation success is related to phenotypic traits, help explain sexual dimorphism in socially monogamous species. Previous experimental manipulations of the ornamental coloration in male bluethroats, Luscinia s. svecica, have shown effects on their social mating success, mate-guarding behaviour, and within-pair- and extra-pair paternity. This study investigates the relationship between male characteristics (reflectance of the blue throat feathers, width of the chestnut breast band, wing length, body condition and age) and fertilisation success under natural, non-experimental conditions. Combining three breeding seasons, 29% of 720 offspring were sired by extra-pair males and 54% of 136 nests contained one or more extra-pair offspring. The chroma (spectral purity) of the blue throat feathers and the width of the chestnut band were positively related to paternity in own nest, and for blue chroma this translated into a significantly positive relation with total fertilisation success. This suggests that differential within-pair paternity success exerts directional selection on the colour signal. None of the throat colour measures or morphological traits were significantly related to overall extra-pair fertilisation (EPF) success. However, restricting the analysis to males with one or more EPFs, there was a positive relation between amount of extra-pair paternity and blue chroma. Old males were more successful than young ones in achieving EPFs. Pairwise comparisons showed no plumage differences between cuckolded males and the males that cuckolded them. The absence of phenotypic correlates of male EPC-success agrees with our recent finding that females improve offspring quality through individual choice of EPC partners with 'compatible genes' rather than 'good genes' in an absolute sense. Our results indicate that experiments where traits are manipulated outside the natural range should be interpreted with caution, and illustrate the importance of a dual approach (experimental and correlative) in studies of sexual selection in the wild.

MORPHOLOGICAL HERITABILITY IN A HYBRID BUNTING COMPLEX: NESOSPIZA AT INACCESSIBLE ISLAND

Abstract Juvenile Nesospiza buntings measured 7–11 weeks after hatching were compared with the sizes of their parents to estimate the heritability (h2) of six external morphological characters. There was no evidence of size selection before juveniles were seven weeks old, but some additional growth in bill size probably occurred after this age. All characters had significant heritabilities among Tristan Buntings (N. acunhae; h2 = 0.66–0.95) and hybrids with Wilkins' Buntings (N. wilkinsi; h2 = 0.62–0.93). Positive heritabilities also were found within color morphs of the Tristan Bunting, although not all regressions were significant. Hybrid offspring generally were intermediate in size between their parents' phenotypes, but one hybrid pair had an unusually small offspring, possibly the result of an extra-pair fertilization. Differences between h2 estimates from sib-sib and parent-offspring regressions suggest that environmental factors contribute to morphological variability, but the large heritable compo...

EGG HATCHABILITY INCREASES WITH COLONY SIZE IN CLIFF SWALLOWS

Abstract The percentage of otherwise successful nests containing ≥ 1 unhatched egg in Cliff Swallows (Petrochelidon pyrrhonota) varied inversely with colony size in southwestern Nebraska. Colony-site characteristics other than colony size had no significant effect on egg hatchability. The incidence of unhatched eggs at a colony site did not vary significantly with year, mean date of first egg laying, mean incubation period, extent of ectoparasitism, or mean body mass of nestlings or adults. This suggests that increased hatching failure in smaller colonies was unrelated to ectoparasitism by fleas and cimicid bugs, foraging success, or egg inattendance. Furthermore, because reproductive interference and incidence of brood parasitism do not increase in smaller colonies, these variables seem unlikely to account for the relationship between egg hatchability and colony size. More frequent matings between genetically similar individuals and reduced opportunities for females to seek extrapair fertilizations with ...

Male boobies expel eggs when paternity is in doubt

We analyzed the effect of increased risk of cuckoldry on male parental investment in eggs in the colonial blue-footed booby (Sula nebouxii). Seventeen experimental males were removed from the nesting territory for 10–12 h on a single day, 1–5 days before laying (females’ supposed fertile period SFP), and 17 control males were removed for the same amount of time on a single day, 7–29 days before laying (before the SFP). These removals were intended to simulate extended absence from the nest on a foraging excursion. Female extrapair courtship and copulation rates did not increase during the removal of the social mate, and there was no evidence that experimental and control males differed quantitatively in incubation or defense of the clutch. However, 43% of experimental males expelled the first-laid egg from the nest, whereas no control male did so. Apparently, male boobies drastically reduce parental investment in eggs with a presumed elevated probability of extrapair fertilization by destroying them.

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.

Extra-pair paternity in waved albatrosses.

We estimated the rate of extra-pair fertilizations (EPFs) in waved albatrosses (Phoebastria irrorata) on Isla Española, Galápagos, Ecuador, using multilocus minisatellite DNA fingerprinting. Waved albatrosses are socially monogamous, long-lived seabirds whose main population is on Española. Aggressive extra-pair copulation (EPC) attempts have been observed in the breeding colony during the days preceding egg-laying. Our genetic analyses of 16 families (single chicks and their attending parents) revealed evidence of EPFs in four families. In all cases males were the excluded parent. These data suggest that waved albatrosses have an unusually high rate of EPF relative to taxa with similar life histories. Future behavioural observations will determine the extent to which forced vs. unforced EPCs contribute to this high EPF rate.

Genetic Relationships of Cory's Shearwater: Parentage, Mating Assortment, and Geographic Differentiation Revealed by DNA Fingerprinting

AbstractWe used DNA fingerprinting to assess genetic structure of populations in Cory's Shearwater (Calonectris diomedea). We analyzed mates and parent-offspring relationships, as well as the amount and distribution of genetic variation within and among populations, from the level of subcolony to subspecies. We found no evidence of extrapair fertilization, confirming that the genetic breeding system matches the social system that has been observed in the species. Mates were closely related, and the level of genetic relatedness within populations was within the range usually found in inbred populations. In contrast to previous studies based on allozymes and mtDNA polymorphism, DNA fingerprinting using microsatellites revealed consistent levels of genetic differentiation among populations. However, analyzing the two subspecies separately revealed that the pattern of genetic variation among populations did not support the model of isolation by distance. Natal dispersal, as well as historic and/or demographic events, probably contributed to shape the genetic structure of populations in the species.

Frequencies of multiple paternity in three Acrocephalus species (Aves Sylviidae) with different mating systems (A. palustris, A. arundinaceus, A. paludicola)

Genetic parentage was determined by DNA-fingerprinting with multilocus probes and microsatellite PCR in three Acrocephalus species with different mating systems: the socially monogamous marsh warbler (A. palustris), the polygynous great reed warbler (A. arundinaceus) and the promiscuous aquatic warbler (A. paludicola). The amount of extra-pair paternity (EPP)/multiple paternity (MP) was then related to ecological parameters (increasing productivity) and parental care (decreasing male participation) of Acrocephalus species. Marsh warblers (33 broods, 131 young plus putative parents) were studied over 3 years in a German population. No case of social polygyny but four extrapair young (EPY) were detected in three socially monogamous broods. The low frequency of extra-pair fertilization (EPF, 9.1% of broods, 3.1% of offspring) may be best attributed to intense male mate-guarding and restrictions on mate assessment due to an extremely short breeding window. The rate of social polygyny in a German great reed warbler population varied between 8 and 35% of males during a 5-year period. In 48 broods (27 monogamous and 21 polygynous males) with 194 young, 5 nests (3 of polygynous, 2 of monogamous males) with 19 EPY were recorded: EPF-rates are 10.4% of broods and 9.8% of offspring. In none of the nests were neighbouring males the genetic fathers, but in 2 nests, “bachelor” males from distant territories had sired the offspring. The EPP-rate in this species seems to be related to an incomplete correlation between male and territory characteristics leaving some females to correct their choice. Aquatic warblers were studied during three years in a Polish population. In each of the years, MP was recorded in more than half of a total of 75 broods (mean 76%). The proportion out of 340 young sired by one to five “additional” males varied between 25 and 57% (mean 39.1%). Food resources are neither critical nor economically defendable in the species' habitat and paternity assurance behaviours of males and female choice are yet not fully understood.

Badge Size and Extra-Pair Fertilizations in the House Sparrow

AbstractFor House Sparrows, Passer domesticus, it has been proposed that the size of a male's throat badge correlates with his success in avoiding cuckoldry as well as obtaining extra-pair copulations (EPCs), and that females gain indirect (genetic) benefits from EPCs with large-badged males. Alternatively, female House Sparrows may engage in EPCs as a guard against their social mate's infertility. We used multi-locus DNA fingerprinting to examine paternity and found that among 41 broods and 136 offspring, 20% of the offspring were attributable to extra-pair fertilizations (EPFs). Forty-one percent of the 34 males were cuckolded; however, large-badged males were as likely to be cuckolded as small-badged males. Moreover, we found no evidence that large-badged males were inherently superior to small-badged males in terms of survivorship. We compared the prevalence of unhatched eggs in broods with and without extra-pair offspring to determine whether EPFs are associated with hatching failure. Although we detected no association between hatch failure and EPFs, enhanced fertility remains a plausible EPC benefit to females, but experimental approaches may be required to evaluate its significance.

Low frequency of extra-pair fertilisations in House Sparrows breeding at high density

The importance that the density of breeders has on the opportunity for extra-pair fertilisations (EPFs) is controversial. Some evidence supports the idea that population density and frequency of extra-pair paternity are positively associated, whereas other work does not. In the present paper we estimate EPF frequency in a dense House Sparrow Passer domesticus colony. We detected extra-pair nestlings in 9.3% of 54 broods studied, and 7% of 171 nestlings were sired by extra-pair fathers. The number of clutches laid per female, the change of male or female between two consecutive breeding attempts and the age of the partners showed no association with the presence or absence of extra-pair fertilisations. Morphometric variables of paired males and females did not discriminate broods with EPFs from those without. We detected a single case of a female laying a “parasitic” egg in the nest of a male that in a previous breeding attempt was the extra-pair genetic father of her entire brood. The frequency of extra-pair fertilisation recorded in this study was low compared with that in other House Sparrow populations breeding at lower densities, or other species that breed in colonies. This result does not support the claim that EPF frequency is associated with population density. We propose, as an explanation for this result, that under high intra-sexual competition for nest sites (1) males may have limited opportunities to search for females for extra-pair copulations and (2) the high quality of male nest-owners may reduce female propensity to search for additional sexual partners.

Strict monogamy in a semi‐colonial passerine: the Jackdaw Corvus monedula

In this study we used DNA fingerprinting to provide an accurate measure of paternity in a nest‐box colony of Jackdaws. The species is a semi‐colonial, socially monogamous passerine which establishes long‐term pair bonds. Parents raise a single annual brood in which 50% brood reduction is commonplace. However, nest sites are a limited resource, non‐breeding adults are also common around colonies and males are frequently separated from their incubating females during the fertile egg‐laying period so that opportunities arise for extra‐pair copulation. The parentage analysis, however, revealed no cases of extra‐pair fertilisation (EPF) or intra‐specific brood parasitism. Therefore fledgling output or survival is likely to be a good measure of individual reproductive success in this species. The lack of EPFs is not explained by nesting synchrony and we discuss the relative costs and benefits to females of seeking EPFs; the likelihood that paternal care and a life‐history strategy similar to many long‐lived non‐passerines may also constrain the species to monogamy.

Badge Size and Extra-Pair Fertilizations in the House Sparrow

Badge Size and Extra-Pair Fertilizations in the House Sparrow

Genetic evidence for mixed parentage in nests of the emu ( Dromaius novaehollandiae )

Parentage in emus (Dromaius novaehollandiae) was examined by microsatellite analysis using four independent loci. Of 106 chicks sampled in one breeding season from 18 nests, 54 (51%) were not fathered by the nesting male, 12 (11%) were not from the observed mate of the sitting male, and 9 (8%) represented intra-specific brood parasitism, having no alleles in common with either nest parent. Some males (11%) fathered all chicks in their nests, but the majority showed high levels of cuckoldry. Those males commencing incubation earliest in the season tended to have the highest levels of paternity in their own nests. These results reveal a high frequency of extra-pair fertilisations and resultant cuckoldry in a predominantly socially monogamous bird and support recent reports which have described the emu mating system as a complexity of polyandrous, promiscuous and monogamous behaviour. Parentage assignment of chicks resulting from extra-pair fertilisations revealed an evenly scattered pattern of paternity that did not show any particular male dominance in reproductive success. These results lead to a reassessment of behavioural observations of emus, the consequences of parentage distribution, and theories about mating systems and sexual selection. The frequency of extra-pair copulations and intra-specific brood parasitism suggests patterns of descent that differ greatly from those implied by social monogamy.

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.

Male mating strategies and the mating system of great-tailed grackles

Great-tailed grackles (Quiscalus mexicanus) are sexually dimorphic, dichromatic, colonially nesting blackbirds. In this study, males pursued three basic types of conditional mating strategies, each of which employed a different set of mating tactics. Territorial males defended one or more trees in which several females nested. They achieved reproductive success by siring the offspring of their social mates and through extrapair fertilization. Resident males lived in the colony but did not defend territories or have social mates. Transient males passed through the colony, staying no more than a few days, and probably visited more than one colony. Residents appeared to queue for access to territories, but transients did not. Residents and transients gained all paternity through extrapair fertilizations and provided no parental care. Territorial males sired the majority of offspring, but residents and transients also sired small numbers of nestlings. Territorial males were larger and had longer tails than nonterritorial males. The number of social mates was related to body size, and males that sired nestlings were heavier and had longer tails than males with no genetic reproductive success. Males that gained paternity through extrapair fertilization were heavier and had longer tails than males that did not. The mating system of great-tailed grackles can best be categorized as “non-faithful-female frank polygyny.”