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      Coevolution in Action: Disruptive Selection on Egg Colour in an Avian Brood Parasite and Its Host

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          Abstract

          Background

          Trait polymorphism can evolve as a consequence of frequency-dependent selection. Coevolutionary interactions between hosts and parasites may lead to selection on both to evolve extreme phenotypes deviating from the norm, through disruptive selection.

          Methodology/Principal finding

          Here, we show through detailed field studies and experimental procedures that the ashy-throated parrotbill ( Paradoxornis alphonsianus) and its avian brood parasite, the common cuckoo ( Cuculus canorus), have both evolved egg polymorphism manifested in discrete immaculate white, pale blue, and blue egg phenotypes within a single population. In this host-parasite system the most common egg colours were white and blue, with no significant difference in parasitism rates between hosts laying eggs of either colour. Furthermore, selection on parasites for countering the evolution of host egg types appears to be strong, since ashy-throated parrotbills have evolved rejection abilities for even partially mimetic eggs.

          Conclusions/Significance

          The parrotbill-cuckoo system constitutes a clear outcome of disruptive selection on both host and parasite egg phenotypes driven by coevolution, due to the cost of parasitism in the host and by host defences in the parasite. The present study is to our knowledge the first to report the influence of disruptive selection on evolution of discrete phenotypes in both parasite and host traits in an avian brood parasitism system.

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          Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings.

          Mary Stoddard, Richard Prum (2008)
          We use a tetrahedral color space to describe and analyze male plumage color variation and evolution in a clade of New World buntings--Cyanocompsa and Passerina (Aves: Cardinalidae). The Goldsmith color space models the relative stimulation of the four retinal cones, using the integrals of the product of plumage reflectance spectra and cone sensitivity functions. A color is represented as a vector defined by the relative stimulation of the four cone types--ultraviolet, blue, green, and red. Color vectors are plotted in a tetrahedral, or quaternary, plot with the achromatic point at the origin and the ultraviolet/violet channel along the Z-axis. Each color vector is specified by the spherical coordinates theta, phi, and r. Hue is given by the angles theta and phi. Chroma is given by the magnitude of r, the distance from the achromatic origin. Color vectors of all distinct patches in a plumage characterize the plumage color phenotype. We describe the variation in color space occupancy of male bunting plumages, using various measures of color contrast, hue contrast and diversity, and chroma. Comparative phylogenetic analyses using linear parsimony (in MacClade) and generalized least squares (GLS) models (in CONTINUOUS) with a molecular phylogeny of the group document that plumage color evolution in the clade has been very dynamic. The single best-fit GLS evolutionary model of plumage color variation over the entire clade is a directional change model with no phylogenetic correlation among species. However, phylogenetic innovations in feather color production mechanisms--derived pheomelanin and carotenoid expression in two lineages--created new opportunities to colonize novel areas of color space and fostered the explosive differentiation in plumage color. Comparison of the tetrahedral color space of Goldsmith with that of Endler and Mielke demonstrates that both provide essentially identical results. Evolution of avian ultraviolet/violet opsin sensitivity in relation to chromatic experience is discussed.
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            The evolution of egg colour and patterning in birds.

            R Kilner (2006)
            Avian eggs differ so much in their colour and patterning from species to species that any attempt to account for this diversity might initially seem doomed to failure. Here I present a critical review of the literature which, when combined with the results of some comparative analyses, suggests that just a few selective agents can explain much of the variation in egg appearance. Ancestrally, bird eggs were probably white and immaculate. Ancient diversification in nest location, and hence in the clutch's vulnerability to attack by predators, can explain basic differences between bird families in egg appearance. The ancestral white egg has been retained by species whose nests are safe from attack by predators, while those that have moved to a more vulnerable nest site are now more likely to lay brown eggs, covered in speckles, just as Wallace hypothesized more than a century ago. Even blue eggs might be cryptic in a subset of nests built in vegetation. It is possible that some species have subsequently turned these ancient adaptations to new functions, for example to signal female quality, to protect eggs from damaging solar radiation, or to add structural strength to shells when calcium is in short supply. The threat of predation, together with the use of varying nest sites, appears to have increased the diversity of egg colouring seen among species within families, and among clutches within species. Brood parasites and their hosts have probably secondarily influenced the diversity of egg appearance. Each drives the evolution of the other's egg colour and patterning, as hosts attempt to avoid exploitation by rejecting odd-looking eggs from their nests, and parasites attempt to outwit their hosts by laying eggs that will escape detection. This co-evolutionary arms race has increased variation in egg appearance both within and between species, in parasites and in hosts, sometimes resulting in the evolution of egg colour polymorphisms. It has also reduced variation in egg appearance within host clutches, although the benefit thus gained by hosts is not clear.
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              Parasite adaptation to locally common host genotypes.

              C. M. Lively, M Dybdahl (2000)
              According to the Red Queen hypothesis--which states that interactions among species (such as hosts and parasites) lead to constant natural selection for adaptation and counter-adaptation--the disproportionate evolutionary success of parasites on common host genotypes leads to correlated selection for sexual reproduction and local adaptation by the parasite population. Here we determined whether local adaptation is due to disproportionate infection of common host genotypes, and, if so, whether infection of common host genotypes is due to commonness per se, or some other aspect of these genotypes. In a reciprocal cross-inoculation experiment parasites occupying the same geographical area (sympatric) infected locally common host genotypes significantly more often than rare host genotypes, whereas parasites occupying separate geographical areas (allopatric) showed no such significant difference. A mixed source of parasites (containing F1 hybrids) also showed no difference in infection between rare and common host genotypes. These results show that local adaptation results from parasite tracking of locally common host genotypes, and, as such, a necessary condition of the Red Queen hypothesis is met.
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                Author and article information

                Contributors
                : Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2010
                Publication date (Electronic): 26 May 2010
                Volume: 5
                Issue: 5
                Electronic Location Identifier: e10816
                Affiliations
                [1 ]School of Life Sciences, Sun Yat-sen University, Guangzhou, People's Republic of China
                [2 ]College of Life Sciences, Hainan Normal University, Haikou, People's Republic of China
                [3 ]Department of Information and Computer Sciences, Nara Women's University, Kita-Uoya Nishimachi, Nara, Japan
                [4 ]Laboratoire d'Ecologie, Systématique et Evolution, Université Paris-Sud, Orsay, France
                [5 ]Department of Biology, Norwegian University of Science and Technology (NTNU), Trondheim, Norway
                [6 ]Centre for Advanced Study (CAS), Oslo, Norway
                Smithsonian Institution National Zoological Park, United States of America
                Author notes

                Conceived and designed the experiments: CY WL YC SS FT AM ER BGS. Performed the experiments: CY WL YC SS. Analyzed the data: CY APM AA FF BGS. Wrote the paper: CY WL FT APM AA FF AM ER BGS.

                Article
                Publisher ID: 10-PONE-RA-16154R1
                DOI: 10.1371/journal.pone.0010816
                PMC ID: 2877083
                PubMed ID: 20520815
                SO-VID: 6ec9fc2c-70ec-40db-8a01-351356d02100
                Copyright © Yang 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.
                History
                Date received : 9 February 2010
                Date accepted : 3 May 2010
                Page count
                Pages: 8
                Categories
                Subject: Research Article
                Subject: Evolutionary Biology
                Subject: Evolutionary Biology/Animal Behavior
                Subject: Evolutionary Biology/Evolutionary Ecology

                ScienceOpen disciplines: Uncategorized
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                ScienceOpen disciplines: Uncategorized

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