Tests of spatial and temporal factors influencing extra-pair paternity in red-winged blackbirds.

Extra-pair paternity (EPP) is a widespread and highly variable reproductive phenomenon in birds. We tested the effects of habitat, spatial factors, and timing of breeding on the occurrence of EPP in red-winged blackbirds (Agelaius phoeniceus). We used PCR-amplified microsatellites to assess the paternity of 1479 nestlings from 537 broods on 235 territories over four breeding seasons. Over 4 years, 40% of nestlings were extra-pair. At least 27% of actual sires were non-neighbours, suggesting that males or females interacted over longer distances than in other populations of red-winged blackbirds. The level of EPP was significantly clumped within broods and males but not within females across broods. EPP was negatively related to the area of a male's territory. The spatial proximity of a female's nest to the territory boundary had no effect on total EPP, but tended to increase the probability of an EPP by a nearby male. We found no influence on EPP of the type of habitat on the territory or the level of nesting activity nearby. The time in the season when a nest was started and the synchrony of breeding also had no significant effect on the level of EPP. The age of the male, the age of his neighbours, and the interaction between the two had no effect on total EPP. However, older males were less likely to have an offspring sired by a neighbour on their territory. Males with older neighbours were also less likely to have offspring sired by a neighbour, particularly if they were new territory owners. The high variability in who gained and lost paternity, and the limited impact of spatial and temporal factors influencing it, have some interesting implications for theories seeking to explain mating patterns.

Westneat DF ，Mays HL Jr 《MOLECULAR ECOLOGY》

Spatial patterns of extra-pair paternity: beyond paternity gains and losses.

Most studies on extra-pair paternity (EPP) focus either on a specific male's extra-pair gains or his extra-pair losses. For an individual bird however, mate choice or mate availability may underlie strong spatial restrictions. Disregarding this spatial aspect may underestimate or mask effects of parameters influencing observed EPP patterns. Here, we propose a spatially explicit model for investigating the probability of having extra-pair offspring (EPO) within local networks of breeding pairs. The data set includes all realized and unrealized potential extra-pair matings. This method is biologically meaningful because it allows (a) considering both members of an extra-pair mating and their social mates, and (b) direct modelling of the spatial context in which extra-pair behaviour occurs. The method has the advantage that it can provide inference about the relative contribution of spatial and non-spatial parameters, and about the relative importance of male and female neighbourhoods. We apply this method to parentage data from 1025 broods collected over 12 breeding seasons in two independent study populations of blue tits (Cyanistes caeruleus). We investigate a set of predictions based on the EPP literature, namely that EPP depends on male age and body size, breeding density and breeding synchrony. In all analyses, we control for breeding distance, a parameter that is expected to influence EPP even under random mating. The results show that older and larger males were more likely to sire EPO, but both effects decreased with increasing breeding distance. Local breeding density but not synchrony predicted whether a particular male-female combination had EPO, at least in one of the study areas. Apart from breeding distance, male age had the strongest effect on EPP, followed by a measure of breeding density. The method thus allows a comprehensive assessment of the relative importance of different types of spatial and non-spatial parameters to explain variation in the occurrence of EPP, while controlling for the fact that individuals that breed further apart are less likely to have EPO. The proposed approach is not limited to investigate EPP, but can be applied to other behavioural interactions between two individuals, such as dominance, competition and (social) mating.

Schlicht L ，Valcu M ，Kempenaers B 《-》

How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods.

Extra-pair paternity is an important aspect of reproductive strategies in many species of birds. Given that in most species females control whether fertilization occurs, they are expected to benefit in some way from the extra-pair matings. In this study we use patterns of extra-pair paternity (EPP) in broods of individual reed buntings (Emberiza schoeniclus), both within and between seasons, to test four hypothesized female benefits: (1) assessing potential future partners and seeking (2) genetic diversity (3) good genes, or (4) compatible genes. Reed buntings are socially monogamous, multibrooded passerines with extremely high levels of extra-pair paternity. We studied a population of reed buntings in the Netherlands in 2002 and 2003; 51% of offspring in 74% of nests were extra-pair. We showed that patterns of EPP did not support the first and second hypotheses, since females did not form a pair with previous extra-pair partners, EPP was not evenly distributed among broods and more broods than expected were sired by a single male. Furthermore, there was no relation between a male's within- and extra-pair fertilization success, no consistency in EPP between breeding attempts, no effect of parental relatedness on EPP and several cases of reciprocal paternity. These patterns do not support the good genes hypothesis and are most consistent with the genetic compatibility hypothesis. However, our previous finding that older males are more successful in gaining EPP, suggests some effect of good genes. These hypotheses need not be mutually exclusive, as females may select compatible males above a certain quality threshold (e.g. old males).

Bouwman KM ，Burke T ，Komdeur J 《MOLECULAR ECOLOGY》

Little effect of extrapair paternity on the opportunity for sexual selection in Savannah sparrows (Passerculus sandwichensis).

Extrapair paternity (EPP) can dramatically increase the opportunity for sexual selection if relatively few males are able to monopolize the majority of fertilizations in a population. Although recent work with birds suggests that EPP can increase the standardized variance in male reproductive success (Is) as much as 13-fold, only a male's within-pair success is typically quantified with any accuracy. In most cases, nearly half of all extrapair young are of unknown parentage. A strong, negative correlation across studies between the proportion of extrapair young for which parentage is known and the apparent effect of EPP on Is (r(s) = -0.71, P = 0.013, N = 13 studies) suggests that the incomplete sampling of extrapair sires has greatly exaggerated the influence of EPP. To achieve a more thorough accounting of EPP and its importance to variation in male fitness, we used a suite of four to six microsatellite loci to identify extrapair young and their sires in a polygynous population of Savannah sparrows (Passerculus sandwichensis). Pooling over the 2002 and 2003 breeding seasons, 79 of 116 females (68.1%) produced young outside of the pairbond and 194 of 411 offspring (47.2%) were extrapair. We identified sires for 96.4% of all young (N = 396), including sires for 92.3% of the extrapair young (N = 179), allowing us to partition Is into within-pair and extrapair components. In both years, EPP-related fitness components generated more variation in male reproductive success than the number or quality of within-pair mates. Differences among males in the number of extrapair mates alone accounted for 56.6% of Is in 2002 and for 23.6% of Is in 2003. Nonetheless, in absolute terms, the occurrence of EPP on Kent Island increased the opportunity for sexual selection less than two-fold. Averaging over the two years, Is was only 78% higher than Is,app, the variance in male reproductive success that would have occurred had EPP been nonexistent and males sired all young on their territories. Likewise, across nine socially monogamous species, we found no correlation between the extent of EPP and its effect on the opportunity for sexual selection (Is/Is,app) and only a marginally significant positive correlation between EPP and Is itself. Taken together, our results suggest that the relationship between EPP and sexual selection in birds may be much less strong and much less straightforward than commonly thought.

Freeman-Gallant CR ，Wheelwright NT ，Meiklejohn KE ，States SL ，Sollecito SV ... -  《EVOLUTION》

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.

Kraaijeveld K ，Carew PJ ，Billing T ，Adcock GJ ，Mulder RA ... -  《MOLECULAR ECOLOGY》