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      Nature’s Palette: Characterization of Shared Pigments in Colorful Avian and Mollusk Shells

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          Abstract

          Pigment-based coloration is a common trait found in a variety of organisms across the tree of life. For example, calcareous avian eggs are natural structures that vary greatly in color, yet just a handful of tetrapyrrole pigment compounds are responsible for generating this myriad of colors. To fully understand the diversity and constraints shaping nature’s palette, it is imperative to characterize the similarities and differences in the types of compounds involved in color production across diverse lineages. Pigment composition was investigated in eggshells of eleven paleognath bird taxa, covering several extinct and extant lineages, and shells of four extant species of mollusks. Birds and mollusks are two distantly related, calcareous shell-building groups, thus characterization of pigments in their calcareous structures would provide insights to whether similar compounds are found in different phyla (Chordata and Mollusca). An ethylenediaminetetraacetic acid (EDTA) extraction protocol was used to analyze the presence and concentration of biliverdin and protoporphyrin, two known and ubiquitous tetrapyrrole avian eggshell pigments, in all avian and molluscan samples. Biliverdin was solely detected in birds, including the colorful eggshells of four tinamou species. In contrast, protoporphyrin was detected in both the eggshells of several avian species and in the shells of all mollusks. These findings support previous hypotheses about the ubiquitous deposition of tetrapyrroles in the eggshells of various bird lineages and provide evidence for its presence also across distantly related animal taxa.

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          Most cited references20

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          Genetics, development and evolution of adaptive pigmentation in vertebrates.

          The study of pigmentation has played an important role in the intersection of evolution, genetics, and developmental biology. Pigmentation's utility as a visible phenotypic marker has resulted in over 100 years of intense study of coat color mutations in laboratory mice, thereby creating an impressive list of candidate genes and an understanding of the developmental mechanisms responsible for the phenotypic effects. Variation in color and pigment patterning has also served as the focus of many classic studies of naturally occurring phenotypic variation in a wide variety of vertebrates, providing some of the most compelling cases for parallel and convergent evolution. Thus, the pigmentation model system holds much promise for understanding the nature of adaptation by linking genetic changes to variation in fitness-related traits. Here, I first discuss the historical role of pigmentation in genetics, development and evolutionary biology. I then discuss recent empirically based studies in vertebrates, which rely on these historical foundations to make connections between genotype and phenotype for ecologically important pigmentation traits. These studies provide insight into the evolutionary process by uncovering the genetic basis of adaptive traits and addressing such long-standing questions in evolutionary biology as (1) are adaptive changes predominantly caused by mutations in regulatory regions or coding regions? (2) is adaptation driven by the fixation of dominant mutations? and (3) to what extent are parallel phenotypic changes caused by similar genetic changes? It is clear that coloration has much to teach us about the molecular basis of organismal diversity, adaptation and the evolutionary process.
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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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              Convergence in pigmentation at multiple levels: mutations, genes and function.

              Convergence--the independent evolution of the same trait by two or more taxa--has long been of interest to evolutionary biologists, but only recently has the molecular basis of phenotypic convergence been identified. Here, we highlight studies of rapid evolution of cryptic coloration in vertebrates to demonstrate that phenotypic convergence can occur at multiple levels: mutations, genes and gene function. We first show that different genes can be responsible for convergent phenotypes even among closely related populations, for example, in the pale beach mice inhabiting Florida's Gulf and Atlantic coasts. By contrast, the exact same mutation can create similar phenotypes in distantly related species such as mice and mammoths. Next, we show that different mutations in the same gene need not be functionally equivalent to produce similar phenotypes. For example, separate mutations produce divergent protein function but convergent pale coloration in two lizard species. Similarly, mutations that alter the expression of a gene in different ways can, nevertheless, result in similar phenotypes, as demonstrated by sister species of deer mice. Together these studies underscore the importance of identifying not only the genes, but also the precise mutations and their effects on protein function, that contribute to adaptation and highlight how convergence can occur at different genetic levels.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                9 December 2015
                2015
                : 10
                : 12
                : e0143545
                Affiliations
                [1 ]The Graduate Center, City University of New York, New York, New York, United States of America
                [2 ]Division of Invertebrate Zoology, American Museum of Natural History, New York, New York, United States of America
                [3 ]Department of Chemistry, Hunter College Belfer Research Building, City University of New York, New York, New York, United States of America
                [4 ]Department of Psychology, University of Massachusetts, Amherst, Massachusetts, United States of America
                [5 ]Department of Zoology and Laboratory of Ornithology, Palacký University, Olomouc, Czech Republic
                [6 ]Department of Psychology, Hunter College, City University of New York, New York, New York, United States of America
                University of California, UNITED STATES
                Author notes

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

                Conceived and designed the experiments: AV M. Holford MEH. Performed the experiments: AV WC M. Hossain DH MEH. Analyzed the data: AV WC M. Holford DH MEH. Contributed reagents/materials/analysis tools: PLRB DH TG M. Holford. Wrote the paper: AV PLRB DH TG MEH M. Holford.

                Article
                PONE-D-15-35862
                10.1371/journal.pone.0143545
                4674117
                26650398
                81c0f69d-aaed-4bdb-8e5b-0df1cc38b4da
                © 2015 Verdes 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
                : 18 August 2015
                : 5 November 2015
                Page count
                Figures: 2, Tables: 2, Pages: 13
                Funding
                AV acknowledges funding from The Weissman School of Arts and Sciences of Baruch College, Hunter College and The Graduate Center of the City University of New York. Funding was also provided by CUNY Summer Undergraduate Research Program to WC. This project was supported by National Science Foundation CAREER program NSF-CHE 1247550, NSF-MRI 1228921, and Camille Dreyfus Teacher-Scholar Award to MH. The European Social Fund and the state budget of the Czech Republic (project no. CZ.1.07/2.3.00/30.0041) co-financed DH. Additional support came from a Human Frontier Science Program Young Investigator Award to MEH and TG.
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