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      Mating system and extra-pair paternity in the Fan-tailed Gerygone Gerygone flavolateralis in relation to parasitism by the Shining Bronze-cuckoo Chalcites lucidus

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          Abstract

          Extra-pair copulation can increase genetic diversity and offspring fitness. However, it may also increase intra-nest variability in avian hosts of brood parasites, which can decrease the discrimination ability of host parents towards the parasite. In New Caledonia, the Fan-tailed Gerygone ( Gerygone flavolateralis), which is parasitized by the Shining Bronze-cuckoo ( Chalcites lucidus), has two nestling morphs, dark and bright, that can occur in monomorphic and polymorphic broods. Gerygone parents recognize and eject parasite nestlings from their nest, but the presence of polymorphic broods may increase the chances of recognition errors. Using 17 microsatellite markers, we investigated the mating system of the Fan-tailed Gerygone to understand the mechanisms underlying nestling polymorphism. We hypothesised that extra-pair copulations would lead to a higher proportion of polymorphic broods caused by higher genetic variability, thus creating a trade-off between genetic benefits and host defence reliability. Extra-pair paternity occurred in 6 of 36 broods, which resulted in 6 of 69 offspring sired by extra-pair males. Broods with and without mixed paternity were comparably often parasitized. Extra-pair paternity did not influence the proportions of bright, dark and polymorphic broods. Compared to bright siblings in polymorphic broods, dark nestlings tended to have lower heterozygosity, particularly in loci associated with skin coloration. The results also suggested that there is no obstacle for genetic exchange between individuals from forest and savannah, possibly due to dispersal of offspring. We conclude that the Fan-tailed Gerygone is a socially monogamous species with a low rate of extra-pair paternity compared to closely related species. Extra-pair paternity increased offspring genetic variability without measurable associated costs by brood parasitism. The results highlight the importance of studying host mating systems to assess the trade-offs between host defence and offspring fitness in co-evolutionary arms races.

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          Most cited references 37

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          Prevalence of different modes of parental care in birds.

          Estimates of the incidence of major classes of parental care by birds are drawn from classical studies that preceded both the publication of a massive secondary literature and the revolution driven by molecular approaches to avian phylogeny. Here, I review this literature in the light of new phylogenetic hypotheses and estimate the prevalence of six distinct modes of care: use of geothermal heat to incubate eggs, brood parasitism, male only care, female only care, biparental care and cooperative breeding. Female only care and cooperative breeding are more common than has previously been recognized, occurring in 8 and 9% of species, respectively. Biparental care by a pair-bonded male and female is the most common pattern of care but at 81% of species, the pattern is less common than once believed. I identify several problems with existing hypotheses for the evolution of parental care and highlight a number of poorly understood contrasts which, once resolved, should help elucidate avian social evolution.
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            Females increase offspring heterozygosity and fitness through extra-pair matings.

            Females in a variety of species commonly mate with multiple males, and there is evidence that they benefit by producing offspring of higher genetic quality; however, the nature of these genetic benefits is debated. Enhanced offspring survival or quality can result from intrinsic effects of paternal genes---'good genes'--or from interactions between the maternal and paternal genomes--'compatible genes'. Evidence for the latter process is accumulating: matings between relatives lead to decreased reproductive success, and the individual level of inbreeding--measured as average heterozygosity--is a strong fitness predictor. Females should thus benefit from mating with genetically dissimilar males. In many birds, social monogamy restricts mate choice, but females may circumvent this by pursuing extra-pair copulations. Here we show that female blue tits, Parus caeruleus, increase the heterozygosity of their progeny through extra-pair matings. Females thereby produce offspring of higher reproductive value, because less inbred individuals have increased survival chances, a more elaborate male secondary sexual trait (crown colour) and higher reproductive success. The cost of inbreeding may therefore be an important factor driving the evolution of female extra-pair mating.
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              Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler

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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                8 March 2018
                2018
                : 13
                : 3
                Affiliations
                [1 ] Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw, Poland
                [2 ] Unit of Molecular Zoology, Chair of Zoology, Department of Animal Science, Technische Universität München, Freising, Germany
                [3 ] Department of Fish, Wildlife & Conservation Ecology and Molecular Biology Program, New Mexico State University, Las Cruces, New Mexico, United States of America
                [4 ] Department of Life Sciences, Rikkyo University, Tokyo, Japan
                Hungarian Academy of Sciences, HUNGARY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Article
                PONE-D-17-34241
                10.1371/journal.pone.0194059
                5843341
                29518150
                © 2018 Bojarska et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 4, Tables: 3, Pages: 14
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: 2012/05/E/NZ8/02694
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 24-4578
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 24770028
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 23255004
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100007118, Rikkyo University;
                Award ID: SFR 11-54
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: 2016/23/B/NZ8/03082
                This study was financed by the Polish National Science Centre (grants NCN 2012/05/E/NZ8/02694 and NCN 2016/23/B/NZ8/03082), the Japan Society for the Promotion of Science (grant 24-4578 to N.J.S., grant 24770028 to K.D.T., grant 23255004 to K.U.), and Rikkyo University (grant SFR 11-54 to N.J.S.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Genetics
                Heredity
                Heterozygosity
                Biology and Life Sciences
                Behavior
                Habits
                Nesting Habits
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Genetic Polymorphism
                Biology and Life Sciences
                Genetics
                Population Genetics
                Genetic Polymorphism
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Genetic Polymorphism
                Biology and Life Sciences
                Behavior
                Animal Behavior
                Animal Sexual Behavior
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Animal Sexual Behavior
                Biology and Life Sciences
                Species Interactions
                Parasitism
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Biology and Life Sciences
                Genetics
                Gene Types
                Microsatellite Loci
                Biology and Life Sciences
                Genetics
                Genetic Loci
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Copulation
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Copulation
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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