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.     

Evidence of genetic monogamy in the lemur Indri (Indri indri)

Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair‐living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra‐pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair‐living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra‐pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair‐living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair‐living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species.     

Analysis of extra‐pair paternity and conspecific brood parasitism in mallards Anas platyrhynchos using non‐invasive techniques

A method that was based on non‐invasive sampling of genetic material was used to determine the rates of extra‐pair paternity (EPP) and conspecific brood parasitism (CBP) in mallards. Maternal and offspring DNA were extracted from feathers in nest material and hatched eggshell membranes. Using 8 microsatelite loci, extra‐pair offspring were detected in 48% of nests and accounted for 9.3% of all offspring. In addition, 10.1% of the offspring were confirmed to result from CBP, and 24% of all nests contained at least 1 offspring from CBP. Rates of conspecific nest parasitism were higher than those of related species, which might have been due to higher breeding densities at our study site. The incidence of EPP was distributed randomly (i.e. did not deviate from bionomial distribution) throughout the population, indicating that variations in pre‐copulatory (e.g. female choice, mate guarding) or post‐copulatory processes (e.g. sperm competition, cryptic female choice) do not affect the distribution of EPP among breeding pairs markedly. Yet, our data provide evidence of variation in the risk of being parasitized among breeding females. The occurrence of CBP and EPP was unaffected by the timing of the breeding attempt or breeding synchrony.     

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.     

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.     

Small changes in timing of breeding among subarctic passerines over a 32‐year period

Many bird populations in temperate regions have advanced their timing of breeding in response to a warming climate in recent decades. However, long‐term trends in temperature differ geographically and between seasons, and so do responses of local breeding populations. Data on breeding bird phenology from subarctic and arctic passerine populations are scarce, and relatively little data has been recorded in open‐nesting species. We investigated the timing of breeding and its relationship to spring temperature of 14 mainly open‐nesting passerine species in subarctic Swedish Lapland over a period of 32 years (1984–2015). We estimated timing of breeding from the progress of post‐juvenile moult in mist‐netted birds, a new method exploring the fact that the progress of post‐juvenile moult correlates with age. Although there was a numerical tendency for earlier breeding in most species (on average ?0.09 days/year), changes were statistically significant in only three species (by ?0.16 to ?0.23 days/year). These figures are relatively low compared with what has been found in other long‐term studies but are similar to a few other studies in subarctic areas. Generally, annual hatching dates were negatively correlated with mean temperature in May. This correlation was stronger in long‐distance than in short‐distance migrants. Although annual temperatures at high northern latitudes have increased over recent decades, there was no long‐term increase in mean temperature in May over the study period at this subarctic site. This is probably the main reason why there were only small long‐term changes in hatching dates.     

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.     

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.     

Habitat selection in reintroduced bird populations: a case study of Stewart Island robins and South Island saddlebacks on Ulva Island

An understanding of the mechanisms influencing habitat selection in reintroduced bird populations is fundamental for successful translocation programmes. Plant species composition, abundance, structure and food availability are likely to influence animal movement and habitat choice, but few studies have evaluated their combined effect on habitat selection of translocated birds. Stewart Island robins (Petroica australis rakiura) and South Island saddlebacks (Philesturnus carunculatus carunculatus) are two threatened New?Zealand bird species that have been reintroduced to Ulva Island (Stewart Island). We hypothesised that their initial settlement patterns were driven by habitat quality. We tested this hypothesis by comparing habitat components between occupied and unoccupied habitats as the population grew after initial tanslocation. We also modelled probabilities of site selection as a function of the composition and structure of vegetation, availability of food (invertebrate composition) and nesting resources (cavity type). Founding pairs of both species first established territories in coastal habitat in the western part of the island, which is characterised by structurally complex broadleaved vegetation. Birds also selected sites with a greater abundance and diversity of food resources. Thus in the early stages of population establishment robins and saddlebacks appear to select high quality habitat that offers enhanced cover and foraging opportunities.     

Comprehensive paternity assignment: genotype,spatial location and social status in song sparrows,Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra‐pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6‐day‐old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra‐pair sires primarily occupied territories neighbouring their extra‐pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra‐pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.     

Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Rates of extra‐pair paternity (EPP) have frequently been associated with genetic relatedness between social mates in socially monogamous birds. However, evidence is limited in mammals. Here, we investigate whether dominant females use divorce or extra‐pair paternity as a strategy to avoid the negative effects of inbreeding when paired with a related male in meerkats Suricata suricatta, a species where inbreeding depression is evident for several traits. We show that dominant breeding pairs seldom divorce, but that rates of EPP are associated with genetic similarity between mates. Although extra‐pair males are no more distantly related to the female than social males, they are more heterozygous. Nevertheless, extra‐pair pups are not more heterozygous than within‐pair pups. Whether females benefit from EPP in terms of increased fitness of the offspring, such as enhanced survival or growth, requires further investigations.     

Weather conditions affect levels of extra-pair paternity in the reed bunting Emberiza schoeniclus

Extra-pair paternity (EPP) is common in many socially monogamous birds, but large variations in frequency of EPP are found both between and within species. Local ecological factors can affect the costs and benefits of extra-pair mating behaviour, and may therefore influence the chance that individuals engage in extra-pair copulations (EPCs). We investigated the effect of weather conditions during the peak fertile period of the female on the levels of EPP in reed buntings Emberiza schoeniclus . The reed bunting is a socially monogamous passerine, with extremely high levels of EPP (50% of offspring in 80% of broods). We found that higher daily minimum temperatures and more rainfall during the peak fertile period were associated with lower proportions of EPP. As during adverse weather conditions individuals have to invest more in self maintenance, we suggest that during long periods of rain the extra-pair mating behaviour of all individuals will be restricted, leading to lower proportions of EPP. During cold mornings, time-consuming activities such as mate guarding are likely to be more strongly affected than less time-consuming activities such as EPCs, leading to higher proportions of EPP.     

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.     

Extrapair paternities in black-browed Thalassarche melanophris, grey-headed T. chrysostoma and wandering albatrosses Diomedea exulans at South Georgia

Extrapair paternities (EPP) are relatively common in passerines, but rare in seabirds. Like most seabirds, albatrosses are long lived, form long-term pair bonds and require biparental care for chick-rearing. Microsatellite analyses of 327 chicks from black-browed Thalassarche melanophris , grey-headed T. chrysostoma and wandering albatrosses Diomedea exulans over two breeding seasons revealed the presence of EPP in all three species. Though EPP rates varied between species and years, up to 21% of offspring were the result of extrapair matings. Rates were highest in wandering albatrosses (6–21%) followed by grey-headed (3–10%) and black-browed (0–9%) albatrosses. EPP rates were lower in 1998 compared to 1999 in both black-browed and grey-headed albatrosses, whereas the reverse was true for wandering albatrosses. Interspecific differences in EPP rates may reflect differences in breeding phenology and sexual size dimorphism. Differences in timing and frequency of breeding may promote different opportunities for interactions with birds other than their normal partner. The different breeding habitat, dispersion and mate-attraction rituals in wandering albatross, together with the disparity in size between the sexes may also offer more scope for higher rates of EPP. Despite extensive sampling within each colony, we were unable to identify sires for many of the extrapair young; however males from other colonies were involved, raising interesting questions regarding the timing and nature of such events.     

Indirect fitness benefits through extra‐pair mating are large for an inbred minority,but cannot explain widespread infidelity among red‐winged fairy‐wrens

Extra‐pair paternity (EPP) has been suggested to improve the genetic quality of offspring, but evidence has been equivocal. Benefits of EPP may be only available to specific individuals or under certain conditions. Red‐winged fairy‐wrens have extremely high levels of EPP, suggesting fitness benefits might be large and available to most individuals. Furthermore, extreme philopatry commonly leads to incestuous social pairings, so inbreeding avoidance may be an important selection pressure. Here, we quantified the fitness benefits of EPP under varying conditions and across life‐stages. Extra‐pair offspring (EPO) did not appear to have higher fitness than within‐pair offspring (WPO), neither in poor years nor in the absence of helpers‐at‐the‐nest. However, EPP was beneficial for closely related social pairs, because inbred WPO suffered an overall 75% reduction in fitness. Inbreeding depression was nonlinear and reduced nestling body condition, first year survival and reproductive success. Our comprehensive study indicates that EPP should be favored for the 17% of females paired incestuously, but cannot explain the widespread infidelity in this species. Furthermore, our finding that fitness benefits of EPP only become apparent for a small part of the population could potentially explain the apparent absence of fitness differences in population wide comparisons of EPO and WPO.     

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.     

Habitat selection by South Island saddlebacks and Stewart Island robins reintroduced to Ulva Island

Determining whether animals select some habitats over others provides basic information about how animals meet their requirements for survival and reproduction. Habitat selection is therefore an important component of conservation research. Studies involving the release and establishment of threatened species on island refuges can be particularly insightful because breeding pairs should be able to select habitat of the highest quality within the range available. This study uses GIS technology to investigate the spatial distribution of breeding territories in relation to overall habitat availability of two threatened passerines, South Island saddlebacks (Philesturnus carunculatus carunculatus) and Stewart Island robins (Petroica australis rakiura) two years after their release onto predator-free Ulva Island. Both species established breeding territories around the periphery of the island in coastal forest fringe habitat and away from mature forest in the interior of the island. Compositional analysis suggested that both species prefer dense, fringe-type habitat with open ground cover and deep litter layers and avoid more mature forests, especially with moss cover. Thus habitat structure is likely to be more important for both species than plant-species composition. However, the possibility exists that the preference of coastal fringe habitat could represent an ‘ecological trap’, where habitat preference does not correspond to better quality habitat in terms of reproductive fitness. It will be useful to continue monitoring saddlebacks and robins to obtain data on survival and fecundity as the density of birds increases, and breeding pairs are forced to establish territories in what is presently perceived to be less preferred habitat in the interior part of the island.     

Social organization,demography and genetic mating system of a Tibetan cooperative breeder

Knowledge of cooperative breeding in birds from longitudinal studies is available only for a small proportion of species. This paper reports data from a 12‐year study on the Tibetan Ground Tit Pseudopodoces humilis. On average, 27.2% (range: 13.0–36.1%) of monogamous pairs in each year contained one (85.4%) or more (14.6%) male helpers, 83.7% of which were yearlings staying on natal territories. Most helpers (89.6%) helped once and then bred independently. Adults had male‐biased sex ratios, low annual survival rates (averaging 0.50) and shorter longevities (averaging 1.8 years) compared with low‐altitude avian cooperative breeders, suggesting that mate shortage promotes helping behaviour in this species. Incest occurred rarely (2.1% of pairs), probably because kin recognition occurs through year‐around living in family groups. There was a low level (3.1% of broods) of extra‐pair parentage, which could facilitate the maintenance of cooperative breeding.     

Cross‐amplification of polymorphic microsatellites reveals extra‐pair paternity and brood parasitism in Sturnus vulgaris

We tested the cross‐amplification of 37 microsatellites in a population of starlings (Sturnus vulgaris). Twenty‐three of them amplified and five exhibited a large number of alleles per locus and high heterozygosity (on average: 14.6 alleles/locus and H_E = 0.704). We assessed the occurrence of extra‐pair paternity (EPP) and intraspecific brood parasitism (IBP) in this population. The EPP rate was 16% to 18% offspring from 43% to 45% of nests. IBP was very variable between two successive years (14% to 27% chicks from 25% to 64% of clutches). These five polymorphic markers will be of potential use in studies of genetic diversity, population structure and reproductive strategy of this species.     

Climate change and annual survival in a temperate passerine: partitioning seasonal effects and predicting future patterns

Predicting climate change impacts on population size requires detailed understanding of how climate influences key demographic rates, such as survival. This knowledge is frequently unavailable, even in well‐studied taxa such as birds. In temperate regions, most research into climatic effects on annual survival in resident passerines has focussed on winter temperature. Few studies have investigated potential precipitation effects and most assume little impact of breeding season weather. We use a 19‐year capture–mark–recapture study to provide a rare empirical analysis of how variation in temperature and precipitation throughout the entire year influences adult annual survival in a temperate passerine, the long‐tailed tit Aegithalos caudatus. We use model averaging to predict longer‐term historical survival rates, and future survival until the year 2100. Our model explains 73% of the interannual variation in survival rates. In contrast to current theory, we find a strong precipitation effect and no effect of variation in winter weather on adult annual survival, which is correlated most strongly to breeding season (spring) weather. Warm springs and autumns increase annual survival, but wet springs reduce survival and alter the form of the relationship between spring temperature and annual survival. There is little evidence for density dependence across the observed variation in population size. Using our model to estimate historical survival rates indicates that recent spring warming has led to an upward trend in survival rates, which has probably contributed to the observed long‐term increase in the UK long‐tailed tit population. Future climate change is predicted to further increase survival, under a broad range of carbon emissions scenarios and probabilistic climate change outcomes, even if precipitation increases substantially. We demonstrate the importance of considering weather over the entire annual cycle, and of considering precipitation and temperature in combination, in order to develop robust predictive models of demographic responses to climate change. Synthesis Prediction of climate change impacts demands understanding of how climate influences key demographic rates. In our 19‐year mark‐recapture study of long‐tailed tits Aegithalos caudatus, weather explained 73% of the inter‐annual variation in adult survival; warm springs and autumns increased survival, wet springs reduced survival, but winter weather had little effect. Robust predictions thus require consideration of the entire annual cycle and should not focus solely on temperature. Unexpectedly, survival appeared not to be strongly density‐dependent, so we use historical climate data to infer that recent climate change has enhanced survival over the four decades in which the UK long‐tailed tit population has more than doubled. Furthermore, survival rates in this species are predicted to further increase under a wide range of future climate scenarios.