High frequency of extra‐pair paternity in an urban population of Cooper's Hawks

Raptors exhibit some of the highest rates of intra‐pair copulations among birds, perhaps in an attempt by males to reduce the risk of being cuckolded. Indeed, the frequency of extra‐pair fertilizations reported in studies of raptors to date is relatively low (0–11.2%). Socially monogamous Cooper's Hawks (Accipiter cooperii) exhibit one of the highest copulation rates among birds, yet there are no published accounts of extra‐pair copulations (or paternity). We studied a population of Cooper's Hawks in Milwaukee, Wisconsin, during three breeding seasons (2003, 2004, and 2007), examining the possible effects of age (1 yr old vs. ≥ 2 yr old), adult mass, and brood size on the frequency of extra‐pair paternity (EPP). We found that 19.3% of nestlings (N = 27/140) were extra‐pair young (EPY), and 34% of all broods (N = 15/44) had at least one EPY. The sires of the EPY in our study were identified for only two broods, suggesting that floater males may have engaged in extra‐pair copulations with territorial females. We found that brood size was a good predictor of the occurrence of EPP (EPP) in nests, but adult mass and female age were not. To our knowledge, these possible correlates of the occurrence of EPP in raptors had not previously been investigated. Male Cooper's Hawks provide food for females during the pre‐nesting period, and delivery of food is, in contrast to other raptor species, typically followed by copulation. Thus, one possible explanation of the relatively high rates of EPP in our study is that females might accept or even solicit extra‐pair copulations from males other than their mates as a means of maximizing energy intake for egg production. Such behavior might be particularly likely in our study area, i.e., a food‐rich urban setting with a high breeding density of Cooper's Hawks.     

Does nest predation risk affect the frequency of extra‐pair paternity in a socially monogamous passerine?

While considerable variations in both the frequency of extra‐pair paternity (EPP) and the behavioral events that produce it are recognized among species, populations, individuals, and breeding attempts, the determinants of these variations are surprisingly difficult to establish. Nest predation may be one such determinant, since it is the most important source of reproductive failure, and past studies have suggested a variety of reproductive flexibilities under nest predation risk. However, despite its potentially significant effect on mating behaviors, nest predation risk has rarely been discussed in association with variations in intraspecific EPP patterns. Here, we examined the effect of naturally occurring nest predation, which varied between sites, years, and breeding attempts, on patterns of EPP in 92 broods (132 adults and 710 nestlings) of the Japanese great tit Parus major minor. We found that the frequency of extra‐pair offspring was positively correlated with the nest predation rate, along with a correlation to breeding attempts in a season, but not with other factors such as individual quality or breeding density. Under high nest‐predation risk, it may be adaptive for males to search for additional extra‐pair copulation to spread the risk of losing all offspring and to invest less in mate‐guarding, which also enables females to seek additional extra‐mating. The results of this study suggest that nest predation risk, among other factors, may significantly influence paternity allocation in birds.     

Extra‐pair paternity in a population of Chilean Swallows breeding at 54 degrees south

Geographic patterns of variation in life‐history traits have puzzled researchers for decades. However, the widely accepted idea that mating systems exhibit a tropical–temperate latitudinal trend, with extra‐pair mating systems being the norm among temperate species and genetic monogamy the norm among tropical species, is supported by sparse data, particularly for birds breeding in the tropics and even more so for birds that breed in the southern hemisphere temperate zone. Our objective was to examine the genetic mating system of Chilean Swallows (Tachycineta meyeni) breeding at 54°S in Tierra del Fuego, Argentina. From 2006 to 2009, we examined the paternity of young in 52 broods. Contrary to predictions based on their congeners that breed at equivalent latitudes in the northern hemisphere, Chilean Swallows in our study had low rates of extra‐pair paternity (EPP), with 13.5% of nests (N = 52) having at least one extra‐pair young and 6.8% of all nestlings (N = 161) fathered by extra‐pair males. These rates are also lower than those reported for species of Tachycineta swallows that breed at tropical latitudes. We found no support for a tropical–south temperate latitudinal cline in EPP rates. The highly unpredictable weather of the island of Tierra del Fuego might be influencing parental investment at this site; small clutch sizes and low EPP rates are expected if biparental attention is crucial for chick survival and reproductive success for these aerial insectivores. We argue that the sparse sampling of mating systems in birds worldwide may have contributed to a misapprehension of a global pattern. More studies of tropical and south‐temperate systems are needed to build on theories based on a wider set of taxa.     

Extra‐pair paternity as a strategy to reduce the costs of heterospecific reproduction? Insights from the crow hybrid zone

Within hybrid zones of socially monogamous species, the number of mating opportunities with a conspecific can be limited. As a consequence, individuals may mate with a heterospecific (social) partner despite possible fitness costs to their hybrid offspring. Extra‐pair copulations with a conspecific may thus arise as a possible post hoc strategy to reduce the costs of hybridization. We here assessed the rate of extra‐pair paternity in the hybrid zone between all‐black carrion crows (Corvus (corone) corone) and grey hooded crows (C. (c.) cornix) and tested whether extra‐pair paternity (EPP) was more likely in broods where parents differed in plumage colour. The proportion of broods with at least one extra‐pair offspring and the proportion of extra‐pair offspring were low overall (6.98% and 2.90%, respectively) with no evidence of hybrid broods having higher EPP rates than purebred nests.     

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.     

Spatial distribution of nests constrains the strength of sexual selection in a warbler

In socially monogamous species, extra‐pair paternity may increase the strength of intersexual selection by allowing males with preferred phenotypes to monopolize matings. Several studies have found relationships between male signals and extra‐pair mating, but many others fail to explain variation in extra‐pair mating success. A greater appreciation for the role that ecological contingencies play in structuring behavioural processes may help to reconcile contradictory results. We studied extra‐pair mating in a spatial context in the common yellowthroat (Geothlypis trichas), a territorial wood warbler. Over the course of 6 years, we observed 158 breeding attempts by 99 males, resulting in a total of 369 nests and 520 sampled nestlings. The spatial distribution of territories varied greatly, with males having between 0 and 10 close neighbours and between three and 39 neighbouring nestlings close enough to represent extra‐pair siring opportunities. Both within‐pair and extra‐pair reproductive success increased with breeding density, but the opportunity for sexual selection and strength of selection varied with density. Total variance in reproductive success was highest at low density and was mostly explained by variation in within‐pair success. In contrast, at high density, both within‐pair and extra‐pair successes contributed substantially to variance in reproductive success. The relationships between plumage and extra‐pair mating also varied by density; plumage was under strong sexual selection via extra‐pair mating success at high density, but no selection was detected at low density. Thus, ecological factors that structure social interactions can drive patterns of sexual selection by facilitating or constraining the expression of mating preferences.     

High rates of extra‐pair paternity in two equatorial populations of rufous‐collared sparrow,Zonotrichia capensis

The latitudinal increase in extra‐pair paternity (EPP) rates in birds suggests broad selective benefits to low EPP rates in the tropics. However, we have few EPP data from tropical birds, particularly from species with close relatives at high latitudes. Here, we report EPP rates in two resident equatorial populations of rufous‐collared sparrow Zonotrichia capensis, a genus well‐represented at high latitudes. We found 64% and 60% of broods contained extra‐pair offspring, and 42% and 52% of all young were extra‐pair. EPP rates were similar in these populations, despite clear differences in elevation, temperature, rainfall, and breeding season length. These findings provide evidence that EPP rates in tropical birds can be as high as those observed in temperate birds, and suggest that the selective pressures acting on EPP rates vary markedly across tropical birds.     

Territory configuration moderates the frequency of extra‐group mating in superb fairy‐wrens

The frequency of extra‐pair paternity (EPP) in socially monogamous birds varies substantially between and within species, but ecological drivers of this variation remain poorly understood. Habitat configuration could influence EPP by moderating access to extra‐pair mates, because species occupying territories in a clustered ‘honeycomb’ configuration have a larger pool of potential extra‐group mates in their immediate neighbourhood than those living in linearly arranged territories (e.g. along narrow strips of riparian or fragmented habitat). We exploited variation in the spatial arrangement of territories due to anthropogenic modification of habitat of the cooperatively breeding superb fairy‐wren Malurus cyaneus to test whether habitat configuration influenced the frequency of EPP. In this species, most paternity is obtained by males outside the social group [extra‐group paternity (EGP)]. We found that the frequency of EGP among groups living in linear strips of roadside vegetation (41% of 44 offspring) was lower than it was for groups living in clustered territories within continuous habitat (59% of 70 offspring). Differences in group size and pair relatedness did not explain differences in EGP associated with territory configuration, although the frequency of EGP was negatively correlated with pair relatedness. Our finding suggests that territory configuration can influence rates of EGP and that anthropogenic habitat fragmentation has the potential to limit access to extra‐pair mates, affecting mating systems and ultimately fitness.     

Breeding synchrony and extrapair paternity in a species with alternative reproductive strategies

Breeding synchrony may affect the tradeoff between pursuing multiple mates and avoiding paternity loss, translating into differences in the rate of extrapair paternity (EPP). However, diverse empirical relationships between breeding synchrony and EPP remain challenging to explain. We examined whether the relationship between breeding synchrony and EPP varied with male morph, age, body size, or breeding density in the white‐throated sparrow Zonotrichia albicollis. In this species, males of two genetically determined morphs pursue alternative mating strategies. Breeding synchrony positively correlated with EPP within polygamous white morph males, which have high rates of EPP and cuckoldry, but was unrelated to EPP within tan morph males, which prioritize mate guarding and paternal care. As previously reported, males that gained EPP were primarily white males. Males gained EPP more often than expected by chance during their mate's fertile period and on neighboring territories. Since extrapair copulation appears primarily male‐driven in this species, these results indicate that white males focus extra‐pair mating effort during periods of high synchrony and during their mates’ fertile periods, even at the expense of paternity loss within their own nests. Breeding density, male age, and male size did not modify the relationship between breeding synchrony and EPP. However, older white males had higher cuckoldry rates, perhaps reflecting declines in performance associated with senescence. Results suggest that, even within species, mating strategy may modify how breeding synchrony affects rates of EPP, with positive relationships manifest only within subsets of individuals that pursue a strategy of polygyny at the expense of paternity loss.     

Manipulation of male quality in wild tits: effects on paternity loss

Extrapair paternity (EPP) has proved to be widespread and highlyvariable among birds and other taxa, including socially monogamousspecies. A multitude of hypotheses have been put forward toexplain this variation, but its occurrence is not fully understood.Male age, social dominance rank, song and breeding density orsynchrony have been among the suggested correlates of EPP, butresults so far are inconclusive. We interspecifically cross-fosteredblue tits (Parus caeruleus) and great tits (Parus major) inthe wild, thus manipulating males to exhibit reduced socialdominance rank, sing aberrant songs, and consequently be perceivedas low-quality males as compared to controls. This allowed usto test if male quality had an influence on loss of paternity.We found no statistically significant differences between cross-fosteredand control males of either species, neither with respect tolevels of cuckoldry nor proportions of extrapair young (EPY)in the broods. Paternity levels were comparable to other studieson the same species. No effect of density could be detectedon levels of EPP either, while an age effect seemed to be presentat least in the blue tit, EPY being almost absent in broodsof older blue tit males. We conclude that the effects of malequality on paternity loss are minor, if any, in these populations.     

Ecological opportunities and individual condition as predictors of extra‐pair paternity in a south‐temperate swallow (Tachycineta leucorrhoa)

Ecological and physiological factors such as breeding density, breeding synchrony, and adult body condition can all affect extra‐pair mating behavior, but the relative importance of these factors may vary among species. White‐rumped Swallows (Tachycineta leucorrhoa) nesting in Buenos Aires Province, Argentina, exhibit high rates of extra‐pair paternity, with 77% of nests having extra‐pair young. Our objective was to determine the extent to which extra‐pair paternity in this species is explained by breeding synchrony, breeding density, and adult body condition. Our study of a population of White‐rumped Swallows breeding in nest boxes was conducted during two consecutive breeding seasons (September – early January 2006–2008). We found that neither breeding synchrony nor density of neighbors predicted levels of extra‐pair paternity in our study population. Leaner females were more likely to engage in extra‐pair behavior and fledged more nestlings, but did not differ in structural size from females that did not engage in extra‐pair behavior, suggesting that female mass is an important predictor of mating decisions and fitness for these aerial insectivores. Male body condition was not related to male extra‐pair behavior. The mass of female White‐rumped Swallows may affect their flying ability such that, during their fertile period, they are exposed to more potential extra‐pair mates during longer foraging flights. Being lighter may also improve the ability of females to provision nestlings later in the breeding cycle.     

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.     

Experimental evidence that brighter males sire more extra‐pair young in tree swallows

Across taxa, extra‐pair mating is widespread among socially monogamous species, but few studies have identified male ornamental traits associated with extra‐pair mating success, and even fewer studies have experimentally manipulated male traits to determine whether they are related directly to paternity. As a consequence, there is little experimental evidence to support the widespread hypothesis that females choose more ornamented males as extra‐pair mates. Here, we conducted an experimental study of the relationship between male plumage colour and fertilization success in tree swallows (Tachycineta bicolor), which have one of the highest levels of extra‐pair mating in birds. In this study, we experimentally dulled the bright blue plumage on the back of males (with nontoxic ink markers) early in the breeding season prior to most mating. Compared with control males, dulled males sired fewer extra‐pair young, and, as a result, fewer young overall. Among untreated males, brighter blue males also sired more extra‐pair young, and in paired comparisons, extra‐pair sires had brighter blue plumage than the within‐pair male they cuckolded. These results, together with previous work on tree swallows, suggest that extra‐pair mating behaviour is driven by benefits to both males and females.     

Extra‐Pair Paternity Declines with Female Age and Wing Length in the Pied Flycatcher

Despite many studies of how male characteristics affect paternity in predominantly monogamous birds, relatively little attention has been given to the traits of females that may influence extra‐pair paternity (EPP). However, the occurrence of EPP may be the result of behavioural interactions in which both male and female traits are important for determining the outcome. If EPP is driven mainly by female choice of extra‐pair sires, older, more experienced or larger females would be better able to evade mate guarding tactics and more capable of selecting extra‐pair mates and resisting unwanted suitors. This would be especially noticeable in females paired with unattractive mates. On the other hand, if EPP is driven mainly by male pursuit, we should expect that young, inexperienced or small females would be more exposed to coercive male approaches independently of social mate traits. In a study of an Iberian population of the pied flycatcher Ficedula hypoleuca, we found that EPP affected 38% of the broods and 17% of the nestlings. These values are relatively high, allowing a relatively large number of affected within‐pair mates to be included. We found that EPP is related to both female and male traits although not to any interaction between male and female traits. EPP was higher at nests tended by both younger and short‐winged females and by browner males. Older females may be more experienced and dominant while long‐winged females may be faster fliers, these traits enabling them to avoid extra‐pair copulations, while brown males are less aggressive towards male intruders. In our study population, EPP appears to be caused by male pursuit, which in some cases may overwhelm female attempts to avoid extra‐pair copulations and their social partner's ability to prevent them.     

A Contrast in Extra-Pair Paternity Levels on Mainland and Island Populations of Mediterranean Blue Tits

Extra‐pair copulation (EPC) is a widespread behaviour amongst birds, yet the rate of occurrence of extra‐pair offspring is highly variable both within and across species. Two populations of Mediterranean blue tits, Parus caeruleus, one on the mainland and the other on the island of Corsica, are characterized by high levels of extra‐pair paternity (EPP), with 14 and 25% of extra‐pair offspring (in 46 and 68% of the nests), respectively. The rate of EPP is significantly higher in the island population. Such high rates on Corsica contradict the predictions of higher mate fidelity and lower levels of EPP on islands. Despite expressing several traits that characterize an insular syndrome, blue tits of Corsica do not exhibit lower genetic variation which could be associated with low levels of EPP on islands. Furthermore, our results do not support any of the hypotheses that have been proposed so far to explain variation in EPP rates at the local level. We tentatively suggest that proximate Mediterranean constraints, especially consistent food shortage, prompt females to seek better breeding opportunities through a two‐step process including high rates of EPC and divorce.     

Correlates of complete brood failure in blue tits: could extra‐pair mating provide unexplored benefits to females?

Behavioural ecologists have for decades investigated the adaptive value of extra‐pair copulation (EPC) for females of socially monogamous species. Despite extensive effort testing for genetic benefits, there now seems to be a consensus that the so‐called ‘good genes’ effects are at most weak. In parallel the search for direct benefits has mostly focused on the period surrounding egg laying, thus neglecting potential correlates of EPC that might be expressed at later stages in the breeding cycle. Here we used Bayesian methods to analyse data collected over four years in a population of blue tits Cyanistes caeruleus, where no support was previously found for ‘good genes’ effects. We found that broods with mixed paternity experienced less brood failure at the nestling stage than broods with single paternity, and that females having experienced complete brood failure in their previous breeding attempt had higher rates of mixed paternity than either yearling or previously successful females. To better understand these observations we also explored relationships between extra‐pair mating, male and female phenotype, and local breeding density. We found that in almost all cases the sires of extra‐pair offspring were close neighbours, and that within those close neighbourhoods extra‐pair sires were older than other males not siring extra‐pair offspring. Also, females did not display consistent EPC status across years. Taken together our results suggest that multiple mating might be a flexible female behaviour influenced by previous breeding experience, and motivate further experimental tests of causal links between extra‐pair copulation and predation.     

Reed bunting females increase fitness through extra-pair mating with genetically dissimilar males

Females of many socially monogamous species accept or even actively seek copulations outside the social pair bond. As females cannot increase the number of offspring with promiscuous behaviour, the question arises why they engage in extra-pair mating. We used microsatellite data to determine paternity, heterozygosity and genetic relatedness in the reed bunting (Emberiza schoeniclus), a species with high levels of extra-pair paternity (EPP). We found that extra-pair young (EPY) were more heterozygous than within-pair young (WPY). The high heterozygosity of the EPY resulted from a low genetic similarity between females and their extra-pair mates. EPY were heavier and larger when compared with their maternal half-siblings shortly before they left the nest. Recapture data indicated a higher fledgling survival of EPY compared with WPY. Our data suggest that reed bunting females increase the viability of their offspring and thus fitness through extra-pair mating with genetically dissimilar males.     

Steller Sex: Infidelity and Sexual Selection in a Social Corvid (Cyanocitta stelleri)

Genetic analysis of avian mating systems has revealed that more than 70% of monogamous species show incidence of offspring parentage that does not match the social partner. Extra-pair parentage (EPP) has been linked to a variety of factors, including size and symmetry of ornamental traits, coloration, resource availability, and local conspecific density. We examined how ornamental plumage traits of individual Steller''s jays (Cyanocitta stelleri) and territory characteristics influence genetic fidelity of socially monogamous pairs. We used seven highly polymorphic microsatellite markers to assign paternity to 79 offspring, and identified 12 (15.2%) as extra-pair young (EPY). Steller''s jays with extra-pair young had significantly lower values of feather brightness and hue, indicating more ultraviolet-blue shifted coloration, and nested in closer proximity to the forest edge than Steller''s jays with no detected EPY. Body size, crest height, asymmetry of ornamental crest stripes, as well as vegetative composition of territories and their proximity to supplemental feeders appeared to have little relationship to EPP. These results indicate that extra-pair parentage plays a role in the evolution of secondary sexual characteristics in both sexes, and suggest local density and availability of resources may influence Steller''s jay mating dynamics.     

Extra‐pair paternity in Swainson's Hawks

ABSTRACT Although passerines have been relatively well studied and many species found to exhibit relatively high rates of extra‐pair paternity (EPP), less is known about the frequency of EPP in other avian taxa, including raptors. From 2008 to 2010, we examined the frequency of EPP in a population of Swainson's Hawks (Buteo swainsoni) in Butte Valley, California. We examined paternity of 56 nestlings from 19 pairs and 27 broods and found that only three nestlings (5%) in two (7%) broods were the result of extrapair fertilizations. This relatively low frequency of EPP may be the result of mechanisms that reduce the likelihood of extra‐pair fertilization (e.g., mate guarding and frequent copulation), or could result from females limiting EPP to assure paternity of the social male and ensure paternal investment in offspring.