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.     

Extrapair paternity in a flock-living passerine, the vinous-throated parrotbill Paradoxornis webbianus

Understanding the factors that affect the occurrence of extrapair paternity (EPP) is one of the central issues in sexual selection. We investigated genetic parentage and the ecological factors affecting patterns of EPP in the vinous-throated parrotbill, Paradoxornis webbianus , a flock-living species with double broods. Using microsatellite DNA fingerprinting, we determined parentage of 246 offspring in 50 broods over two years (2005 and 2006). Nineteen offspring (8%) from 13 broods (26%) were sired by extrapair males and one offspring (0.4%) was probably the result of intraspecific brood parasitism. The prevalence of EPP varied significantly through the breeding season: 95% of broods with EPP (12/13) occurred in the first of two laying peaks. Parentage assignment revealed that half of extrapair males (6/12) were adjacent neighbours. The distribution of EPP was not significantly related to the ecological factors including breeding density and breeding synchrony. Instead, we suggest that social characteristics such as flocking and weak territoriality may determine the observed pattern of EPP in this study.     

Reproductive success of polygynous male corn buntings (Miliaria calandra) as confirmed by DNA fingerprinting

Despite a sex ratio approximating to unity, female corn buntingswere not equally distributed among males. In 1989 and 1990,41.2% of 50 males were monogamously paired, 29.4% were polygynous,and 23.5% were unpaired. Polygynous males usually paired withtwo females, although in 1990 three males were trigamous. Polygynousmales fledged more offspring from their territories than didmonogamous males, mainly because they had more mates. The fledgingsuccess per nesting female was slightly higher in territoriesof polygynous males, but not significantly so. DNA fingerprintingwas used to confirm the true paternity of 44 offspring from15 broods and the true maternity of 50 offspring from 16 broods.A further 12 offspring from three broods for which neither putativeparent was available were also fingerprinted. Actual reproductivesuccess of parents was close to that inferred from observationsof number of young raised. There was only one brood, containingtwo chicks (4.5% of offspring, or in 6.7% of broods), wherethe chicks were not fathered by the male defending the territory.However, this nest was close to the territory boundary, andthe defending male may have been assigned incorrectly. Therewere no cases of intraspecific brood parasitism (n = 16 broods).The copulation rate was low, and extrapair copulation attemptswere rare, probably because of the poor chances of sneakingonto a neighbor's territory undetected and the costs of leavinga territory unguarded.     

Extrapair paternity in insular African Blue Tits Cyanistes teneriffae is no less frequent than in continental Eurasian Blue Tits Cyanistes caeruleus

Birds breeding on islands often exhibit lower rates of extrapair paternity than their mainland counterparts, perhaps explained by low genetic variation, ‘slower’ life histories and reduced sexual selection in island populations. Extrapair paternity was apparent in 39% (12/19) of broods, and encompassed 15% (21/137) of nestlings, in a population of African Blue Tits Cyanistes teneriffae, in Tenerife, Canary Islands. There were no cases of intraspecific brood parasitism. The incidence of extrapair young lies in the upper range of that reported from mainland populations of the closely related Eurasian Blue Tit Cyanistes caeruleus. We conclude that there is no strong island effect on the genetic mating system in the Cyanistes species group but that extrapair paternity rates in Cyanistes are greater at southern latitudes.     

Extrapair paternity in the Hoopoe Upupa epops: an exploration of the influence of interactions between breeding pairs, non-pair males and strophe length

Previous studies of the Hoopoe Upupa epops have shown that the strophe length of male songs influences female mate choice, and is correlated with female reproductive rates and male production of fledglings in the male’s own brood. However, frequent interactions between breeding pairs and non‐pair males suggests that extrapair copulations could occur and could affect the real number of fledglings sired by males, and therefore the relationship between strophe length and breeding success. Here we analyse the incidence of interactions between breeding pairs and non‐pair males, and of extrapair paternity, the interrelation of these parameters, the influence of male strophe length on them, and whether extrapair fertilizations affect the correlation between strophe length and breeding success of males, in a colour‐ringed population of Hoopoes in south‐eastern Spain. Multilocus DNA‐fingerprinting revealed that 10% of the broods contained offspring sired by extrapair males, representing 7.7% of the chicks. However, the interactions between pairs and non‐pair males were more frequent, with more than 25% of broods being visited by non‐pair males, and about 10% being helped (fed or defended) by males other than the nest owner. Most of these relationships were apparently attempts by visitor males to obtain copulations with paired females, or to obtain access to such females or nests in future breeding attempts. However, there was no significant link between the detection of interactions with alien males in a nest and the occurrence of extrapair paternity in it, indeed extrapair paternity was found in only 30% of the nests with interactions, and therefore the detection of visits or helping by non‐pair males cannot be considered evidence of extrapair paternity in visited or helped broods. Males that sang with long strophes never suffered losses of paternity within their broods, while 25% of males that sang with short strophes did. However, these differences were not significant. Nevertheless, strophe length of males was significantly positively correlated with per brood and seasonal production of fledglings after accounting for losses of paternity within their own broods.     

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.     

Willow tit Parus montanus extrapair offspring are more heterozygous than their maternal half‐siblings

Through extrapair matings, males can sire additional offspring with low cost and females may look for direct benefits in form of food or additional paternal care or gain genetic benefits that increase offspring fitness. We studied the patterns of female mate choice and frequency of extrapair paternity in the socially monogamous willow tit Parus montanus using microsatellites. We also examined the effect of heterozygosity on the growth rate and survival of the chicks. We found 25 mixed‐paternity broods out of 117 broods of which both parents were sampled. Altogether, 6.7% of sampled chicks were classified as extrapair young. The pairwise relatedness of social pairs did not correlate with the percentage of extrapair young in the brood and there was no difference in heterozygosity between promiscuous and monogamous parents. However, the extrapair young were more heterozygous than the within‐pair young in the mixed‐paternity broods. The maternal half‐siblings in mixed paternity broods were similar in body size. Thus, there was no indication for different growth rate between the siblings, but there were indications that heterozygosity affects survival.     

Males achieve greater reproductive success through multiple broods than through extrapair mating in house wrens

In polygynous species, it is unclear whether extrapair matings provide a better reproductive payoff to males than additional social mates. Male house wrens, Troglodytes aedon, show three types of social mating behaviour: single-brooded monogamy, sequential monogamy (two broods) and polygyny. Thus, male reproductive success can vary depending on the number of mates, the number of broods and the number of extrapair fertilizations. We used microsatellite markers to determine the realized reproductive success (total number of young sired from both within-pair and extrapair fertilizations) of males in these three categories. We found that polygynous males were more likely to be cuckolded than monogamous males; however, half of the polygynous males had a third brood, which resulted in similar reproductive success for sequentially monogamous and polygynous males. Despite the paternity gained from extrapair fertilizations by single-brooded males, males were more successful when they produced multiple broods during a season, either sequentially (monogamy) or simultaneously (polygyny). In our population, multibrooded males were more likely to have prior breeding experience and arrived earlier in the season, which provided a better opportunity to obtain more than one brood and, thus, produce more young.     

Extrapair paternity in the common sandpiper, Actitis hypoleucos, revealed by DNA fingerprinting

The prevalence of extrapair paternity in many socially monogamous passerines has not been mirrored in most monogamous nonpasserines studied to date. Here, we investigated the reproductive behaviour of a socially monogamous shorebird, the common sandpiper, using multilocus DNA fingerprinting. Given the high level of paternal care in the species, and the likely high costs in allocating care between kin and nonkin in species with precocial young, we predicted low levels of extrapair paternity similar to other monogamous shorebirds. We found the social mating system to be predominantly monogamous although one polyandrous pairing was identified. Of 83 offspring from 27 broods, 13 (15.7%) young from five (18.5%) broods were identified as being extrapair. There was no evidence of intraspecific nest parasitism or quasiparasitism. In this population, territorial intrusions were carried out largely by males but did not appear to be related to seeking extrapair copulations (EPCs). Seventy copulation attempts were observed and most were within-pair (84%). Six of eight EPC attempts occurred outside the territory of the female's social mate. Copulation rates were significantly higher just before and during egg laying than at other times during the study. At least two females that reared extrapair young had associated with males other than their eventual mates on arrival, suggesting that some females use rapid mate switching as a mating tactic, facilitated perhaps by the asynchronous arrival among both sexes in this population. Why some female sandpipers mate promiscuously remains unresolved.     

Injury and paternity loss in cooperatively breeding American Crows

ABSTRACT Although survivable injuries have been documented in several species of birds, little is known about the social and reproductive consequences of such injuries. We examined relationships between injuries and group composition, reproductive output, and paternity of male breeders in 27 family groups of American Crows (Corvus brachyrhynchos) using 96 broods sampled from 2004 to 2009. Injuries and permanent disfigurement of wings or feet were sustained by 25.9% (7/27) of dominant male breeders. Injured male breeders had smaller broods (2.13 vs. 3.38 nestlings per brood for injured vs. uninjured breeders), lost more paternity (48% vs. 13% extrapair young per brood), and had more adult male auxiliaries in their groups (1.63 vs. 0.65 auxiliaries per group) than uninjured birds. Some of the variation in reproductive partitioning, extrapair paternity rates, and group composition among American Crow family groups can therefore be explained by injuries to male breeders. These results suggest that injuries could account for some of the unexplained variation in the rates and distribution of extrapair paternity across populations and taxa, as well as some of the variation in reproductive skew among cooperatively breeding birds.     

Territory quality drives intraspecific patterns of extrapair paternity

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

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.     

Direct fitness benefits of group living in a complex cooperative society of carrion crows, Corvus corone corone

The social behaviour of carrion crows varies between populations. In northern Spain cooperatively breeding groups form through delayed natal dispersal and/or immigration of individuals (usually males) into the territory. In this population, carrion crows therefore breed as either unassisted pairs, pairs with nondispersing 1-2-year-old helpers (nondispersers), pairs with immigrant helpers or mixed groups (pairs with both immigrants and nondispersers). We used a microsatellite-based genotyping system to determine the parentage of 57 nestlings (19 broods). Polygamous mating was involved in 26% of the broods and reproduction was shared among group members of both sexes in at least three groups. Immigrants of both sexes can therefore gain access to mates by living in a group, while reproduction is unlikely to involve nondispersers. This implies that nondispersers and immigrants gain different sorts of benefits from group living and helping at the nest. Our genetic data confirmed that nondispersers associated with their parents on the natal territory and therefore that delayed natal dispersal leads to family formation in the carrion crow. Polygamous mating was not found in groups without immigrants, suggesting that, in this population, breeders lose parentage in their brood when sociality is extended beyond the limit of the nuclear family.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Genetic evaluation of the mating system in the blue-and-yellow macaw (Ara ararauna, Aves, Psittacidae) by DNA fingerprinting

More than 90% of birds are socially monogamous, although genetic studies indicate that many are often not sexually monogamous. In the present study, DNA fingerprinting was used to estimate the genetic relationships between nestlings belonging to the same broods to evaluate the mating system in the socially monogamous macaw, Ara ararauna. We found that in 10 of 11 broods investigated, the nestlings showed genetic similarity levels congruent with values expected among full-sibs, suggesting that they shared the same parents. However, in one brood, the low genetic similarity observed between nestlings could be a result of intraspecific brood parasitism, intraspecific nest competition or extra-pair paternity. These results, along with available behavioral and life-history data, imply that the blue-and-yellow macaw is not only socially, but also genetically monogamous. However, the occurrence of eventual cases of extra-pair paternity cannot be excluded.     

Cichlids do not adjust reproductive skew to the availability of independent breeding options

Helpers in cooperatively breeding species forego all or partof their reproduction when remaining at home and assisting breedersto raise offspring. Different models of reproductive skew generatealternative predictions about the share of reproduction unrelatedsubordinates will get depending on the degree of ecologicalconstraints. Concession models predict a larger share when independentbreeding options are good, whereas restraint and tug-of-warmodels predict no effects on reproductive skew. We tested thesepredictions by determining the share of reproduction by unrelatedmale and female helpers in the Lake Tanganyika cichlid Neolamprologuspulcher depending on experimentally manipulated possibilitiesfor helper dispersal and independent breeding and dependingon helper size and sex. We created 32 breeding groups in thelaboratory, consisting of two breeders and two helpers each,where only the helpers had access to a nearby dispersal compartmentwith (treatment) or without (control) breeding substrate, usinga repeated measures design. We determined the paternity andmaternity of 1185 offspring from 47 broods using five to nineDNA microsatellite loci and found that: (1) helpers participatedin reproduction equally across the treatments, (2) large malehelpers were significantly more likely to reproduce than smallhelpers, and (3) male helpers engaged in significantly morereproduction than female helpers. Interestingly, in four broods,extragroup helper males had fertilized part of the brood. Nohelper evictions from the group after helper reproduction wereobserved. Our results suggest that tug-of-war models based oncompetition over reproduction within groups describe best thereproductive skew observed in our study system. Female breedersproduced larger clutches in the treatment compared to the controlsituation when the large helpers were males. This suggests thatmale breeder-male helper reproductive conflicts may be alleviatedby females producing larger clutches with helpers around.     

Extra-pair paternity in the Skylark Alauda arvensis

We present the first quantitative data on the genetic breeding system of a lark (Alaudidae), the Skylark Alauda arvensis . Using a set of eight microsatellite loci isolated in a variety of passerine species, we genotyped 171 offspring from 52 broods of Skylark and detected 35 extra-pair offspring (20%), in 14 different broods (27%). All offspring matched their putative mother, so there was no evidence of intraspecific brood parasitism. Previous non-genetic studies had suggested that the species was predominantly socially monogamous, with only rare occurrences of social polygyny and polyandry, although some behaviours, such as mate guarding, did suggest the possibility of extra-pair copulations. The relatively high level of extra-pair paternity in this species is likely to affect the variation in male reproductive success because extra-pair paternity was non-randomly distributed amongst males, with those with shorter wings more likely to be cuckolded.     

Bi‐parental vs. cooperative breeding in a passerine: fitness‐maximizing strategies of males in response to risk of extra‐pair paternity?

In socially monogamous species, males that risk cuckoldry more than others might gain inclusive fitness by yielding paternity to relatives. We tested this prediction in the Tibetan ground tit Pseudopodoces humilis , an unusual facultative cooperative breeder wherein most helpers (87% males) join a mated pair shortly before clutch completion. Extra-pair paternity among bi-parental broods occurred less often (26% of broods, 9% of young) compared with cooperative broods (68%, 25%). In the former, most extra-pair sires (88%) were pair breeders unrelated to the cuckolded males, whereas in the latter, sires (87%) were mainly helpers related to the dominant males. Brood productivity did not differ between the bi-parental and cooperative breeders, but helpers' partitioning over group paternity reduced the realized reproductive success of helped males. After taking inclusive fitness into account, however, there was no difference in success of dominant males between the two social systems. One possible explanation for the differences in the rates of cuckoldry in the two systems was body size, because pair-bond males in bi-parental situations were significantly larger than those in cooperative ones. We propose two alternative strategies for males to maximize fitness: breed as a pair if large to avoid cuckoldry from helpers, or breed cooperatively if small but compromise some paternity to relatives. Our results provide an unusual route to the incidence of cooperative groups, based on constraints imposed by low competitive ability of breeding males rather than some external ecological or demographic factors.     

Speckled warblers break cooperative rules: absence of helping in a group-living member of the Pardalotidae

In the majority of cooperatively breeding bird species, subordinates help the dominant pair to provision the young, regardless of the origin of groups and relatedness between members. Within the family that includes speckled warblers, Chthonicola sagittata, there is considerable variation in social organization and parental behaviour, but the societies of other group-living species in this family are of kin, and subordinates provision the young of breeders. Speckled warblers differ in that offspring are never philopatric, and breeding groups comprise unrelated individuals. We used behavioural observations and DNA fingerprinting to examine genetic parentage and the mating system of the group-living speckled warbler in Canberra, Australia. Speckled warblers breed as pairs or in trios consisting of a female with two males. Alpha males are socially dominant to beta males and maintain dominance through aggression. Beta males never helped to feed nestlings or fledglings, even though they competed for copulations and in one case gained paternity of two of three young in a brood. The social system is therefore polyandrous but not cooperative. As well as competing for copulations with females on their own territories, beta males and single males (those that had lost their breeding partner) regularly undertook extraterritorial forays, most often when the neighbouring female was fertile. Failure by beta males to help even with broods containing their own offspring may be adaptive in this species and may result from increased opportunity for extrapair fertilizations or enhancement of prospects for future reproduction through the formation of alliances with females.     

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.     

Extra-pair paternity does not result in differential sexual selection in the mutually ornamented black swan (Cygnus atratus)

We studied patterns of parentage in 85 broods (332 cygnets) of black swans during three breeding seasons, using a set of eight polymorphic microsatellite markers. We detected both intraspecific brood parasitism (IBP; < 5% of cygnets per year) and extra-pair paternity (EPP). In these years, 10-17% (mean = 15.1%) of cygnets resulted from EPP, and 27-40% (mean 37.6%) of broods contained at least one extra-pair cygnet. Compared with levels of EPP in closely related species with similar life histories, these values are unexpectedly high. EPP in black swans appears unrelated to ecological factors (breeding density and synchrony) or genetic factors (genetic similarity between pair members or genetic quality of the offspring). We found no evidence that a mutual sexual feather ornament known to play a role in social mate choice in black swans (curled wing feathers) is involved in extra-pair mate choice. EPP does not lead to greater variance in reproductive success in males, relative to females in this species. We therefore suggest that EPP does not result in differential sexual selection on males and females, explaining why they are ornamented to the same degree.