Low frequency of extrapair paternity in the polygynous great reed warbler, Acrocephalus arundinaceus

We carried out DNA fingerprinting on 553 young (130 broods)great reed warblers (Acrocephalus arundnaceus) in 1987–1991.In the study population, where 40% of the males become polygynous,there was a low frequency of extrapair fertilizations (EPF).When data from all five years were pooled, 3.1% of the youngwere sired by extrapair males (EPF-males) and 5.4% of the broodscontained extrapair young. We found no cases of extrapair maternity;young with 6–17 mismatched DNA bands (n= 17) had highband sharing with their putative mothers (range = 0.52–0.72)but low band sharing with their putative fathers (range = 0.24–0.40).In broods exposed to EPF, on average 53% of the young were siredby EPF-males. We found the genetic father to each of the illegitimateyoung. In all cases the same EPF-male sired all extrapair youngin a brood. Broods containing EPF-young tended to be initiatedlate during the breeding season. Breeding attempts were ratherevenly distributed over two months, thus this breeding asynchronywould have facilitated EPFs. There was no difference in EPFfrequency between broods where the pair males had left theirfemales unguarded during parts of their fertile periods andbroods where males guarded throughout the fertile periods. Nestswith extrapair young had significantly shorter mean distanceto the closest male neighbor and more male neighbors within100 m than nests without extrapair young. We found no indicationthat females engaged in EPF to get parental care from the EPF-males,or because they were forced to copulate with extrapair males.The low frequency of EPF suggested that females did not seekgenetic diversity to their brood. We cannot rule out the possibilitythat females engaged in EPF to insure fertility. However, datasupporting this hypothesis were weak. Instead, our data supportthe conclusion that females engaged in EPF to increase the geneticquality of their offspring, and that females may have used malesong repertoire size as a cue when choosing EPF partners.     

Ecological, social, and genetic contingency of extrapair behavior in a socially monogamous bird

Extrapair mating strategies are common among socially monogamous birds, but vary widely across ecological and social contexts in which breeding occurs. This variation is thought to reflect a compromise between the direct costs of mates' extrapair behavior and indirect benefits of extrapair fertilizations (EPF) to offspring fitness. However, in most free-living populations, the complete spatial and temporal distribution of mating attempts, genetic characteristics of available mates, and their relative contribution to EPF strategies are difficult to assess. Here we examined prevalence of EPF in relation to breeding density, synchrony, and genetic variability of available mates in a wild population of house finches Carpodacus mexicanus where all breeding attempts are known and all offspring are genotyped. We found that 15% of 59 nests contained extra-pair offspring and 9% of 212 offspring were sired by extra-pair males. We show experimentally that paired males and females avoided EPF displays in the presence of their social partners, revealing direct selection against EPF behavior. However, at the population level, the occurrence of EPF did not vary with nests dispersion, initiation date, synchrony, or with distance between the nests of extrapair partners. Instead, the occurrence of EPF closely covaried with genetic relatedness of a pool of available mates and offspring of genetically dissimilar mating tended to be resistant to a novel pathogen. These results corroborate findings that, in this population, strong fitness benefits of EPF are specific to each individual, thus highlighting the ecological, social, and genetic contingency of costs and benefits of an individual's extrapair behaviors.     

Extrapair paternity in the great tit (Parus major): a test of the "good genes" hypothesis

In 1993 and 1994 we determined the frequency of extrapair paternityin broods of great tits, Parus major using multilocus DNA fingerprinting.We found no instances of intraspecific brood parasitism, but40% of broods (31/78) contained extrapair-fathered young and83% of offspring (58/681) were xtrapair We identified the geneticfathers of 60% of the extrapair nestlings (35/ 58). Males withfull and lost paternity did not differ significantly in traitsthat have been suggested to indicate male quality, nor did thegenetic and social fathers of extrapair offspring. In 1993,cuckolded males sired more offspring that recruited to the subsequentbreeding season than males with full paternity. Moreover, eventhough genetic fathers of extrapair young (EPY) sired more fledglingsthan the males they cuckolded, genetic and social fathers ofEPY did not differ in the number of recruits sired. Also, theEPY of a brood did not survive better than their half sibs.Thus, our results do not supportthe hypothesis that femaleschoose better quality males for extrapair matings ("good genes"hypothesis). Further, the level of extrapair paternity differedmarkedly between the two years. Our data show that females areconstrained in their extrapair activities by the availabilityof extrapair mates. This is at least partly due to yearly differencesin breeding synchrony.     

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

Based on the breeding synchrony hypothesis, we predicted, intwo congeners that nest in simiilar habitat but differ in nestingsynchrony, that blue-headed vireos (Vireo solitarius) wouldhave 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 studiedthe behavior of blue-headed vireos to determine what factorscould promote genetic monogamy. We found no evidence that malesmate guarded to prevent extrapair copulations from occurring.Males did not follow fertile mates closely when mates left thenest (14–25% of female departures) and, during the egg-layingperiod, males were often alone on the nest (22.3 mm/h). Femaleblue-headed vireos, but not red-eyed vireos, obtain direct benefitsfrom social mates such as nest building and incubation (49.1%of the total), and they assess male quality long before becomingfertile. Female blue-headed vireos spent more time incubatingwhen their mates had low incubation effort. Furthermore, maleincubation effort was positively correlated with nest survivalduring incubation. We discuss the evolution of genetic monogamyand sex role convergence in blue-headed vireos in relation toasynchronous breeding.     

Genetic similarity, extrapair paternity, and offspring quality in Savannah sparrows (Passerculus sandwichensis)

The occurrence of extrapair paternity (EPP) in birds is oftenattributed to the action of good-genes sexual selection wherebyfemales "trade up" on male genetic quality by allocating fertilizationsto males with better genes than those possessed by their socialmate. To date, most studies of EPP in birds focus on absolutemeasures of male quality as a criterion for female choice, althoughmultiple mating by females in other taxa is more commonly ascribedto benefits associated with the individual optimization of offspringgenotypes. Here, we examine whether the genetic similarity ofsocial mates predicts female mating patterns in a populationof Savannah sparrows (Passerculus sandwichensis) where as manyas 70% of adults produce extrapair young (EPY). We considerthe influence of genetic similarity across all stages of a female'sdecision-making process, from pair formation through the decisionto produce EPY, to the allocation of fertilizations to specificextrapair sires. In a 4-year study of 175 males, 206 females,and 506 offspring, females were more likely to produce EPY whenpaired to genetically similar males, but they did not appearto be influenced by the size, age, mass, individual heterozygosity,and genetic diversity of their social mates. In paired comparisons,females were almost twice as likely to decrease their geneticsimilarity to males when producing EPY as they were to increaseit. Nonetheless, females did not select especially dissimilarmales when mating outside the pair-bond nor did they pair disassortativelywith respect to genetic similarity. Relative measures of malequality may influence mating patterns in birds, but only atsome points in a female's decision-making process.     

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. Territorialmales defended one or more trees in which several females nested.They achieved reproductive success by siring the offspringof their social mates and through extrapair fertilization.Resident males lived in the colony but did not defend territoriesor have social mates. Transient males passed through the colony, staying no more than a few days, and probably visited more thanone colony. Residents appeared to queue for access to territories,but transients did not. Residents and transients gained allpaternity through extrapair fertilizations and provided noparental 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 nonterritorialmales. The number of social mates was related to body size,and males that sired nestlings were heavier and had longertails than males with no genetic reproductive success. Malesthat gained paternity through extrapair fertilization wereheavier and had longer tails than males that did not. The matingsystem of great-tailed grackles can best be categorized as "non-faithful-female frank polygyny."     

Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity

Sexual conflict between males and females over mating is common. Females that copulate with extrapair mates outside the pair-bond may gain (i) direct benefits such as resources or increased paternal care, (ii) indirect genetic benefits for their offspring, or (iii) insurance against infertility in their own social mate. Few studies have been able to demonstrate the different contexts in which females receive varying types of benefits from extrapair mates. Here, I examined sexual conflict, female extrapair mate choice, and patterns of extrapair paternity in the cooperatively breeding superb starling Lamprotornis superbus using microsatellite markers. Although extrapair paternity was lower than many other avian cooperative breeders (14% of offspring and 25% of nests), females exhibited two distinct mating patterns: half of the extrapair fertilizations were with males from inside the group, whereas half were with males from outside the group. Females with few potential helpers copulated with extrapair mates from within their group and thereby gained direct benefits in the form of additional helpers at the nest, whereas females paired to mates that were relatively less heterozygous than themselves copulated with extrapair mates from outside the group and thereby gained indirect genetic benefits in the form of increased offspring heterozygosity. Females did not appear to gain fertility insurance from copulating with extrapair mates. This is the first study to show that individuals from the same population mate with extrapair males and gain both direct and indirect benefits, but that they do so in different contexts.     

Sexual selection and extrapair fertilization in a socially monogamous passerine, the zebra finch (Taeniopygia gullata)

We investigated paternal exclusion rate (the percentage of youngreared by a male that were not his genetic offspring), and behavioraland reproductive variables influencing this rate, in a freelybreeding laboratory population of zebra finches (Tae-niopygiaguttala castanotis), a socially monogamous grassfinch. Priorto the experiment, each male founder was fitted with eithertwo red bands (creating a phenotype previously demonstratedto be attractive to females) or two green bands (unattractiveto females) as part of a unique combination of four leg bands.The overall paternal exclusion rate was 28%, as determined bymultilocus, minisatellite DNA fingerprinting of 278 offspringreared by 26 males and their mates. Mean exclusion rates were16% and 40% for red- and green-banded males, respectively. Exclusionrates were directly proportional to rates of female participationin unforced extrapair copulations (UEPCs) with red-banded malesthat occurred when females were fertile. Rates of fertile, forcedextrapair copulations (FEPCs) and fertile UEPCs involving green-bandedmales either failed to influence exclusion rate or varied inverselywith exclusion rate, indicating that extrapair fertilization(EPF) is under female control. Effort devoted by males to seekingEPFs increased exclusion rate. Results suggest that males placegreater effort into seeking fertile versus infertile EPCs andthat unattractive males accrue fitness gains through high parentalinvestment (PI), whereas attractive males benefit through decreasedPI and increased allocation to EPF.     

The use of extrapair copulations for mate appraisal by razorbills, Alca torda

Razorbills (Alca Undo) engaged in extrapair copulations (EPCs)during two phases of their breeding cycle when fertilizationof eggs was not possible, suggesting that EPCs provide nongeneticbenefits. Females actively pursued extrapair mountings afterthey completed egg laying, the first monogamous species reportedto do so. Mountings were performed in mating arenas outsideof the breeding colony, where attendance by postlaying femalesindicated that they sought encounters with extrapair males whiletheir mates were incubating. Postlaying females always successfullyresisted insemination yet positioned themselves to receive mountings.These findings support the hypothesis that resistance to inseminationis a ploy used by females to appraise males. At the end of thebreeding cycle, when males escorted the fledgling to sea, femalesremained at the colony where they consorted and sometimes copulatedwith other males. Nonfertilizable extrapair copulations mayserve two social functions for razorbills: female appraisalof males for future fertilizable EPCs and the appraisal andacquisition of new mates by both sexes.     

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. Copyright 2000 The Association for the Study of Animal Behaviour.     

Mate fidelity and parentage in Cory's shearwater Calonectris diomedea - field studies and DNA fingerprinting

Field studies on Cory's shearwater Calonectris diomedea , which were carried out in a breeding colony in the Aegean Sea between 1989 and 1993, revealed that almost all breeding mates stay together over many consecutive years. Mates usually changed when one partner disappeared (e.g. through death), whereas 'divorce' occurred at a rate of 2.7%. Since birds are nesting at very close quarters, the potential for extrapair copulation (EPC) and subsequent extrapair fertilization (EPF) seems to be high. Multilocus DNA fingerprints were used to determine the true parentage of 46 offspring (broods contain a single chick only) from 29 pairs (few pairs were studied in two and three successive years). There were no cases of extrapair paternity.     

Effects of breeding density, synchrony, and experience on extrapair paternity in tree swallows

Breeding density, synchrony, and experience are expected toinfluence the frequency of extrapair paternity in birds. UsingDNA fingerprinting, we examined the effect of these factorson tree swallows nesting at relatively high (grids of nest-boxes)and low (solitary boxes at least 100 m from the nearest neighbor)densities and in relatively synchronous (Alberta) and asynchronous(Ontario) populations in Canada. The mean percentage of extrapairoffspring per nest did not differ significantly between birdsnesting in grids (43%, n = 22 families) and solitary boxes (57%,n = 12 families). Similarly, there was no significant differencein the mean percentage of extrapair offspring per nest betweenrelatively synchronous (60%, n = 12 Alberta families) and asynchronous(41%, n = 22 Ontario families) populations. We also found noconsistent pattern between extrapair paternity and breedingexperience among seven males and seven females examined overtwo to three breeding seasons. Female tree swallows can influencethe fertilization success of extrapair males by active selectionand rejection of copulation partners. We suggest that this abilitylimits the predicted effect of various ecological factors onthe frequency of extrapair paternity     

GENETIC SIMILARITY BETWEEN PARENTS PREDICTS HATCHING FAILURE: NONINCESTUOUS INBREEDING IN THE GREAT REED WARBLER?

The DNA-fingerprinting technique was used to find the true pedigrees and to detect the overall genetic similarity between mates of great reed warblers (Acrocephalus arundinaceus) at an isolated breeding site in Sweden. The study covered 4 yr preceded by 3 yr when almost all adults and nestlings in the study area had been banded. DNA fingerprinting revealed that the putative father had sired 97% of the young (N = 455). The mate's genetic similarity, revealed as the proportion of bands shared in restriction fragment length polymorphism (RFLP) patterns, was high compared with other species of wild birds. Also, band sharing was higher between mates native to the area than between pairs in which the female was experimentally introduced from a distant breeding site. Hatching success of eggs was negatively correlated with the degree of genetic similarity between the mates, whereas pedigree data, up to the level of great-grandparents, clearly demonstrated an absence of close inbreeding. These are the first data showing a significant fitness cost associated with the choice of a mate that has high genetic similarity, even if it is not a close kin. This cost might be caused by generalized negative consequences of genomewide inbreeding in the present study, possibly accentuated by recent population bottlenecks.     

Indiscriminate polyandry and male parental effort

Extrapair paternity involves cooperation between mated females and extrapair males. On the other hand, mated males exhibit a spectrum of anti-cuckolding strategies. Hence, extrapair attributes of diverse species and populations reported in the literature are particular solutions of evolutionary games involving gender-specific cuckolding/anti-cuckolding strategies. Here we use game theoretical methods to study the effect of male paternal effort conserving strategies in situations where females seek extrapair fertilizations (EPF) for reasons of genetic compatibility and/or in pursuit of genetic diversity for their offspring. In such cases, females cannot make a pre-copulatory selection of the optimal genetic partners, and therefore combine promiscuous copulation with the use of in copula and/or post-copulatory selection mechanisms to optimize the genetic endowment of their offspring—indiscriminate polyandry. Our results indicate that, when indiscriminate polygamy is constrained by the availability of extrapair male partners, there are three possible (parameter regime wise) evolutionary stable strategy solutions. (1) All females seek EPF, while all males restrict parental care. (2) All females seek EPF, while all males are unconditionally parental. (3) Females use a combination strategy where pursuit of EPF is mixed—on either a population, or an individual level—with genetic monogamy, while all males use a conditional paternal care strategy, which involves adjusting their parental efforts according to their certainty of paternity.     

The effectiveness of mate guarding by male black-throated blue warblers

In many socially monogamous birds, males maintain close proximityto their mates during the fertile period. This is often consideredan effort on the male's part to prevent other males from copulatingwith his mate, but other functions have been suggested andthe effectiveness of males in preventing extrapair fertilizationshas come into question. Moreover, it is unclear whether mateguarding conflicts with other male activities, particularlythe pursuit of extrapair fertilizations. We examined mate guardingby male black-throated blue warblers (Dendroica caerulescens).Behavioral observations showed that males that guarded theirmates more closely were less likely to have extrapair youngin their nests. Moreover, the experimental detention of a malefor 1 h during the fertility risk period increased the probabilitythat a brood would contain extrapair young. Thus, male mate guarding was effective in reducing the risk of extrapair fertilization.Males with many opportunities for extrapair copulations appearedto guard their mates less and consequently had more extrapairyoung in their broods than males with few such opportunities.This suggests that mate guarding may conflict with the pursuitof extrapair fertilizations.     

Do male ornaments signal immunity in the common yellowthroat?

Male ornaments may advertise genetic benefits to females choosingmates. These benefits may come in the form of genes for resistanceto parasites and disease. Thus, females that prefer more ornamentedmales as mates may receive genes for enhanced immune systemfunction for their offspring. The common yellowthroat (Geothlypistrichas) is the only species to date in which a male plumageornament (size of the black facial mask) is known to be relatedto extrapair mating, and extrapair young are more immunocompetentthan their within-pair half-sibs (at least in colder years).To investigate whether male mask size signals superior immunefunction, we examined male ornaments (mask and bib size andcolor) in relation to measures of overall health (hematocrit)and immune system function (plasma immunoglobulin G [IgG] concentrationand cutaneous immune activity). We also investigated the rolethat testosterone may play in mediating the relationship betweenornaments and immunity. Male mask size was correlated positivelywith IgG level, suggesting that male mask size may indicatehumoral immunity. However, mask size was correlated negativelywith hematocrit and cutaneous immune activity (our measure ofnestling immunocompetence). Bib size and color were not relatedto these indices of immune function or health. Plasma testosteronelevel was neither related to immune function or health nor tothe expression of male ornaments. These results suggest thatthere might be a trade-off between immune system components,as well as between immunity and the production or advertisementof male ornaments.     

Extra-pair fertilizations in Tree Sparrows Passer montanus

Females of socially monogamous bird species frequently accept or solicit copulations from males other than their social mates. At the interspecific level, it has been proposed that species with few or no sexual plumage differences have lower levels of extra-pair fertilizations (EPFs) than more dichromatic species. This is because it is easier for females to assess the quality of extra-pair mates in dichromatic than monochromatic species. To test this, by using genetic profiling, we compared the occurrence of extra-pair young in nests of Tree Sparrows Passer montanus , a monochromatic species, in Switzerland and Spain, with published estimates for the House Sparrow Passer domesticus , a closely related dichromatic species. We found that 25% (10/40) of Tree Sparrow broods in Spain and 23% (8/35) in Switzerland had at least one extra-pair offspring, and that 8% (12/151) of nestlings in Spain and 10% (12/114) in Switzerland were sired by extra-pair mates. These proportions did not differ significantly between the two populations. Tree Sparrow EPF rates did not differ significantly from available data for the House Sparrow, either in the proportion of broods with EPF young (24%, 18/75 in Tree vs. 26%, 92/359 in House Sparrows) or the overall proportion of extra-pair young (9%, 24/265 in Tree vs. 11%, 142/1110 in House Sparrows). Our results suggest that a close taxonomic relationship and similarities in behaviour and ecology may be more important in determining levels of EPF in these species than sexual phenotypic differences.     

Social mating systems and extrapair fertilizations in passerine birds

Two alternative hypotheses have been proposed to explain howsocial and genetic mating systems are interrelated in birds.According to the first (male trade-off) hypothesis, socialpolygyny should increase extrapair fertilizations because whenmales concentrate on attracting additional social mates, theycannot effectively protect females with whom they have already paired from being sexually assaulted. According to the second(female choice) hypothesis, social polygyny should decreaseextrapair fertilizations because a substantial proportion offemales can pair with the male of their choice, and males caneffectively guard each mate during her fertile period. To discriminatethese alternatives, we comprehensively reviewed informationon social mating systems and extrapair fertilizations in temperatezone passerine birds. We found significant inverse relationshipsbetween proportions of socially polygynous males and frequenciesof extrapair young, whether each species was considered asan independent data point (using parametric statistics) orphylogenetically related species were treated as nonindependent (using contrasts analyses). When social mating systems weredichotomized, extrapair chicks were twice as frequent in monogamousas in polygynous species (0.23 vs. 0.11). We hypothesize thatin socially polygynous species, (1) there is less incentivefor females and males to pursue extrapair matings and (2) femalesincur higher costs for sexual infidelity (e.g., due to physical retaliation or reduction of paternal efforts) than in sociallymonogamous species.     

Extrapair paternity in hooded warblers

We examined the role of extrapair fertilizations (EPFs) in themating system of the hooded warbler (Wilsonia citrina), a monogamoussongbird. DNA fingerprinting revealed that 8 of 17 (47%) femaleshad extrapair young in their first or second brood, and 23 of78 (29%) nestlings were the result of EPFs. Extrapair youngwere signifkandy more likely to occur in first broods than insecond broods. The proportion of EPFs within a brood was stronglybirnodal among broods: nests had 50% or more extrapair youngor none. In seven of eight broods where EPFs occurred, an adjacentmale neighbor was identified as the actual father. Male-likecoloration in females did not reduce the likelihood of havingextrapair young. Females with extrapair young did not receiveless parental care from their mates. All males who obtainedEPFs were mated to fertile females or were feeding offspringat the time they most likely mated with the extrapair female.Our results are consistent with the female control hypothesis,which predicts that females benefit from extrapair copulations(EPCs) and have some control over which males, if any, obtainEPCs. However, we could not reject the alternative hypothesisthat some male neighbors are particularly dominant and aggressiveduring EPC attempts, so females accept these EPCs to minimizecosts.     

Female mate preferences and subsequent resistance to copulation in the mallard

In the majority of socially monogamous bird species, femalessolicit or accept copulations from males other than their partner.Females may gain direct benefits from extrapair males, suchas greater access to resources, or indirect genetic benefitsthat will influence the future success of their offspring. However,one group of birds appears to be the exception to this generalrule; in the wildfowl (Anseriformes), all extrapair copulationsappear to be resisted by females. It has been suggested thatresistance behavior may be a strategy to allow females a greaterchoice of mates, either at the precopulatory level (to promotechoice of copulation partner) and/or the postcopulatory level(to promote multiple mating to increase their choice of sperm).This paper examines the function of female resistance behaviorin one of the dabbling ducks, the mallard (Anas platyrhynchos).Observations on a marked population of wild mallard and experimentswith captive birds found that although females showed a strongpreference for particular males that are the first to molt intotheir breeding plumage, male attractiveness did not influencefemale responses to pair or extrapair copulation attempts. Femaleresistance decreased the likelihood that copulation attemptswould end in successful insemination. The findings did not supportthe hypothesis that females resist copulations to promote femalechoice and the reasons why waterfowl may benefit from avoidingall extrapair copulations are discussed.