Incidence Of Extra-pair Paternity Research Articles

Temporal patterns of extra-pair paternity in a population of Grasshopper Sparrows (Ammodramus savannarum) in Maryland

The incidence of extra-pair paternity (EPP) is highly variable across bird taxa. While EPP is known to affect reproductive variance, the causes of temporal variation in rates of EPP are poorly studied. Breeding density has often been proposed as an important factor influencing EPP variation, but it has received mixed support. Over a 5-year period we examined the rate of EPP in a socially monogamous Grasshopper Sparrow (Ammodramus savannarum) population on a restored grassland in Maryland. Of 124 broods, 62.1% had extra-pair young (EPY), and of 448 nestlings, 36.8% were the result of extra-pair fertilizations. Over the 5-year study, percent EPY ranged from 26% to 60%. EPP rates were positively correlated with the local density of territorial males, supporting the density hypothesis, and 81% of the EPY were from neighboring males. Male within-pair mating success was related to extra-pair mating, suggesting an active behavioral tradeoff between within- and extra-pair matings, especially at high densities. By examining males at the individual level, we found males that were not cuckolded also had the most genetic offspring (within-pair and extra-pair), whereas males that were cuckolded also failed to sire many extra-pair offspring. Here we show that density plays an important role in the availability of mates, EPP, and the opportunity for sexual selection. Received 9 April 2016. Accepted 3 August 2017.

Spatial patterns of extra-pair paternity in a waterbird colony: separating the effects of nesting density and nest site location.

Centres of avian colonies are usually associated with reduced predation risk and, thus, attract individuals of high quality, while poor-quality individuals are relegated to peripheral zones. Assuming that the incidence of extra-pair paternity (EPP) is dependent on individual quality, we could expect lower incidence of extra-pair offspring in the central parts of colonies. On the other hand, central pairs often nest in higher densities, which might increase EPP rate. To test these hypotheses, we sampled 124 great cormorant Phalacarocorax carbo sinensis chicks from 30 broods from different zones of a colony and genotyped them at seven highly polymorphic microsatellite loci. Sibship reconstruction confirmed the presence of at least one extra-pair chick in 30.0 % of broods. We found that EPP varied significantly between the zones of the colony, with higher incidence of extra-pair broods in the peripheral zone (53.3 vs. 6.7 % of broods). Centre-edge difference in EPP was consistent with the expected distribution of pair quality and suggested that poor-quality peripheral females were more likely to solicit extra-pair interactions, possibly to gain ‘good genes’ for their offspring. By contrast, we found no evidence for density dependence in EPP rate, indicating that likelihood of raising extra-pair offspring was not constrained by limited availability of local males. The results indicate that spatial randomization of sampling within avian colonies is critical to obtain robust estimations of EPP for non-solitary species. To our knowledge, this study provides the first evidence for the centre-edge difference in EPP within a breeding colony of birds.

Female Red-Breasted Flycatchers(Ficedula Parva) mated with older males produce male-biased broods

Recent avian studies suggest that offspring sex ratios can vary with environmental or parental characteristics. One example is that females may adjust brood sex ratio of fledglings in response to the sexual attractiveness of their mate and are expected to produce more sons when mated with older or more ornamented males. We determined offspring sex ratios at fledging (158 nestlings from 33 broods) in a population of migratory bird species, Red-breasted Flycatchers (Ficedula parva) that were breeding on the western edge of their geographic range, in the strictly protected part of the Białowieża Forest (north-eastern Poland). The ratio of individual broods ranged from all male to all female, but the average offspring sex ratio at the population level did not deviate significantly from the expected 50:50 sex ratio. Moreover, we found no evidence that sex ratio varied significantly with year, with the incidence of extra-pair paternity, with partial brood losses, or with brood size. However, females mated to older males (older males are also more ornamented) were significantly more likely to produce male-biased broods. Our data suggest that female Red-breasted Flycatchers manipulate sex ratio in response to their mate’s age.

Assortative Mating in Relation to Plumage Traits Shared by Male and Female American Robins

Abstract. Whereas the ecological and evolutionary causes and consequences of sexual dimorphism in birds have been widely explored, the functional significance of female ornamentation in mutually ornamented species is less well understood. One hypothesis for mutual ornamentation is mutual sexual selection, where similar selective pressures shape the ornamental traits in both sexes. We examined multiple melanin-based plumage traits (chestnut-colored breast plumage, tail-spot size and damage) in male and female American Robins (Turdus migratorius) in relation to patterns of mating, individual quality, breeding performance, and incidence of extra-pair paternity. We found positive assortative social mating based on breast color and tail-spot damage. Tail-spot size was unrelated to patterns of social mating, and none of the plumage traits examined was associated with the incidence of extra-pair paternity. Brighter breast plumage and less damage to tail spots were positively associated with several measures of b...

Females may not obtain indirect genetic benefits from extra-pair paternity in vinous-throated parrotbills, Paradoxornis webbianus

In birds, determining what females seek through extra-pair paternity (EPP) is fundamental in the understanding of variation in the incidence of EPP within and between species. I conducted genetic parentage analyses in vinous-throated parrotbills, Paradoxornis webbianus, a typical double-brooded passerine with a strong flock habit. In this species, it is known that the prevalence of EPP varies significantly between two egg-laying peaks; 95% of EPP occurred in the first peak. In the present study, I focused on whether or not females obtain genetic benefits through EPP and its relevance to the biased distribution of EPP between the two laying peaks. I found that females did not obtain ‘good genes’ so that extra-pair young were not better than within-pair young in terms of their body condition at the nestling stage or their survival rate to their first winter. I also found no significant effect of parental genetic similarity and local genetic diversity on the occurrence of EPP, and these genetic correlates were not related to the patchy distribution of EPP. Overall, this study concluded that female parrotbills may not pursue indirect benefits through EPP, and further study testing the possibility of direct benefits will be worthwhile.

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.

Agricultural management affects evolutionary processes in a migratory songbird

Hay harvests have detrimental ecological effects on breeding songbirds, as harvesting results in nest failure. Importantly, whether harvesting also affects evolutionary processes is not known. We explored how hay harvest affected social and genetic mating patterns, and thus, the overall opportunity for sexual selection and evolutionary processes for a ground-nesting songbird, the Savannah sparrow (Passerculus sandwichensis). On an unharvested field, 55% of females were in polygynous associations, and social polygyny was associated with greater rates of extra-pair paternity (EPP). In this treatment, synchrony explained variation in EPP rates, as broods by more synchronous females had more EPP than broods by asynchronous females. In contrast, on a harvested field, simultaneous nest failure caused by haying dramatically decreased the overall incidence of EPP by increasing the occurrence of social monogamy and, apparently, the ability of polygynous males to maintain paternity in their own nests. Despite increased social and genetic monogamy, these haying-mediated changes in mating systems resulted in greater than twofold increase in the opportunity for sexual selection. This effect arose, in part, from a 30% increase in the variance associated with within-pair fertilization success, relative to the unharvested field. This effect was caused by a notable increase (+110%) in variance associated with the quality of social mates following simultaneous nest failure. Because up to 40% of regional habitat is harvested by early June, these data may demonstrate a strong population-level effect on mating systems, sexual selection, and consequently, evolutionary processes.

Experimental evidence for adjustment of parental investment in relation to brood sex ratio in the blue tit

Parents should allocate parental investment in relation to the expected reproductive value of their offspring. We used a cross-fostering experiment to see whether factors influencing offspring reproductive value (brood size, nestling sex, age or paternity) were related to parental investment in nest defence in the blue tit, Cyanistes caeruleus . Although brood size and the incidence of extrapair paternity did not influence the nest defence behaviour of parents, we found a significant difference in the way male and female parents responded to the experimental change in sex ratio of the brood; the nest defence response of males was faster at nests with an increased proportion of sons, but the response of females was unrelated to changes in brood sex ratio. Furthermore, there was no relation between the original sex ratio of the brood, before manipulation, and the nest defence response of the male, indicating that paternal investment in this behaviour was a direct response to the manipulated brood sex ratio.

Extra‐pair paternity in the strongly monogamous Wandering AlbatrossDiomedea exulanshas no apparent benefits for females

Although 92% of avian species are socially monogamous, extra‐pair copulation (EPC), resulting in extra‐pair paternity (EPP), is a common reproductive strategy in birds. Among seabirds, in which the rate of social monogamy reaches 100%, Procellariiformes (albatrosses and petrels) show low EPP rates, with the noticeable exception of the only albatross investigated in this regard, the Waved AlbatrossPhoebastria irrorata. This species, in which forced copulations are known to occur, showed a surprisingly high rate of EPP (25% of chicks). We investigate here EPP rates in another albatross species, the Wandering AlbatrossDiomedea exulans, subject to a demographic survey conducted for 38 years. We combined data on pair bonds with analysis of ten microsatellite loci and found that 10.7% of 75 chicks had an extra‐pair sire. Although there was some evidence for inbreeding avoidance, within‐pair and extra‐pair chicks showed similar levels of heterozygosity, and the incidence of EPP was independent of age, experience or past reproductive success. Hence, we found no evidence that females benefit from EPCs. Owing to the male‐biased sex ratio in adults, widowed and divorced males required more time to find a new mate (+28 and +72%, respectively) than did females. Combined with high sexual size dimorphism, this phenomenon might promote the forced copulations observed in this species. Our data therefore suggest that EPC is beneficial to unpaired males but occurs at random in females, consistent with the hypothesis that EPP results solely from forced EPCs. However, the importance of the latter for EPP and the part played by solitary males require further investigation.

Cuckoldry and recapture probability of adult males are not related in the socially monogamous coal tit (Parus ater)

Despite substantial research effort, the benefits of female extra-pair matings in socially monogamous bird species remain elusive. The “good genes” hypothesis assumes that females engage in extra-pair copulations with males of superior genetic quality compared to their respective social mate. Therefore, a negative association between the degree of cuckoldry and male survival is predicted, if genetic quality is phenotypically reflected by high viability. Furthermore, genetic sires of extra-pair offspring (EPO) should survive better than the social fathers they cuckolded. We tested these predictions in a nestbox population of the coal tit (Parus ater), a socially monogamous passerine with low breeding dispersal and high rates of extra-pair paternity (EPP). Based on 257 genotyped first broods of two consecutive years, we found no relationship between the incidence of EPP or the proportion of EPO within a given brood and male or female recapture probabilities. Furthermore, recapture rates did not differ between social and genetic fathers of EPO or males that did or did not appear as extra-pair sires in other broods. Our results were not affected by differential (short-range) breeding dispersal with respect to EPP or by other potentially confounding variables. Hence, they are not in accordance with the “good genes as viability genes” hypothesis.

Reply from N.E. Langmore

Although female song for mate attraction could well be more widespread than is currently thought, the examples presented by Eens and Pinxten highlight the difficulties of inferring function in the absence of detailed, experimental studies. For example, in the experimental study they refer to, two out of nine female blue tits sang after their mates had been removed, suggesting that they were singing to attract a new mate. However, three of these nine females were also reported to engage in fights with neighbouring females[1xKempenaers, B. et al. Behav. Ecol. Sociobiol. 1995; 36: 33–42Crossref | Scopus (105)See all References[1]. As blue tits are facultatively polygynous[1xKempenaers, B. et al. Behav. Ecol. Sociobiol. 1995; 36: 33–42Crossref | Scopus (105)See all References[1], it is equally plausible that female song in this species could function in female–female aggression, as has been observed in many other facultatively polygynous species[2xLangmore, N.E. Trends Ecol. Evol. 1998; 13: 136–140Abstract | Full Text | Full Text PDF | PubMed | Scopus (155)See all References[2], rather than for mate attraction. It would be interesting to know if the female songs described in the other studies were also associated with female–female aggression. Although the possibility that females sing to attract extra-pair males is intuitively appealing, an experimental study of female song in the species with the highest incidence of extra-pair paternity failed to find any support for this hypothesis[3xCooney, R. and Cockburn, A. Anim. Behav. 1995; 49: 1635–1647Crossref | Scopus (58)See all References[3]. I agree with Eens and Pinxten that more experimental studies are needed to differentiate between the possible functions of female song. In particular, before we can conclude that female song functions for mate attraction we need to know that males can distinguish between male and female songs, and that they are preferentially attracted to female songs.