Why are birds' eggs colourful? Eggshell pigments co‐vary with life‐history and nesting ecology among British breeding non‐passerine birds

657..672 The colourful appearance of bird eggshells has long fascinated biologists and considerable research effort has focused on the structure and biochemistry of the avian eggshell matrix. The presence of tetrapyrrole pigments was identified nearly a century ago. Surprisingly, how the concentrations of avian eggshell pigments vary among related species, and whether this variability is associated with either eggshell appearance and/or species life-history traits, remains poorly understood. We quantified the concentrations of the two key eggshell pigments, protoporphyrin IX and biliverdin, from a diverse sample of eggshells stored at the Natural History Museum, Tring, UK. We explicitly tested how these two pigments are associated with physical measures of eggshell coloration and whether the pigment concentrations and colour diversity co-vary with phylogenetic affiliations among species. We also tested a series of comparative hypotheses regarding the association between the concentrations of the two pigments and specific life-history and breeding ecology traits. Across species, the average concentrations of protoporphyrin and biliverdin were positively correlated, and both strongly co-varied with phylogenetic relatedness. Controlling for phylogeny, protoporphyrin concentration was associated with a higher likelihood of cavity nesting and ground nesting, whereas biliverdin concentration was associated with a higher likelihood of non-cavity nesting habit and bi-parental provisioning. Although unlikely to be explained by a single function, the breeding ecology and life history-dependence of eggshell pigment concentrations in these comparative analyses implies that related species share pigment strategies, and that those strategies relate to broad adaptive roles in the evolution of variation in avian eggshell coloration and its underlying mechanisms. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 657-672.

[1]  David H. Brainard,et al.  Colorimetry , 2020, Definitions.

[2]  J. Ewen,et al.  Sources of variation in reflectance spectrophotometric data: a quantitative analysis using avian eggshell colours , 2012 .

[3]  N. Sparks.  Eggshell Pigments–from Formation to Deposition , 2011 .

[4]  P. Cassey,et al.  Review: an embryo's eye view of avian eggshell pigmentation , 2011 .

[5]  P. Cassey,et al.  Speckles of cryptic black‐headed gull eggs show no mechanical or conductance structural function , 2011 .

[6]  A. Møller,et al.  Genetic differentiation among sympatric cuckoo host races: males matter , 2011, Proceedings of the Royal Society B: Biological Sciences.

[7]  N. Hart,et al.  Sexual selection based on egg colour: physiological models and egg discrimination experiments in a cavity-nesting bird , 2011, Behavioral Ecology and Sociobiology.

[8]  J. Li,et al.  Expression and activity analysis reveal that heme oxygenase (decycling) 1 is associated with blue egg formation. , 2011, Poultry science.

[9]  Thomas W. Pike,et al.  Using digital cameras to investigate animal colouration: estimating sensor sensitivity functions , 2011, Behavioral Ecology and Sociobiology.

[10]  J. Moreno,et al.  Eggshell blue-green colouration fades immediately after oviposition: a cautionary note about measuring natural egg colours , 2011, Ornis Fennica.

[11]  C. Riehl.  Paternal Investment and the “Sexually Selected Hypothesis” for the Evolution of Eggshell Coloration: Revisiting the Assumptions , 2011 .

[12]  A. Velando,et al.  Biliverdin-based egg coloration is enhanced by carotenoid supplementation , 2011, Behavioral Ecology and Sociobiology.

[13]  J. D. Hoyo,et al.  Handbook of the Birds of the World , 2010 .

[14]  J. Ewen,et al.  Impact of time since collection on avian eggshell color: a comparison of museum and fresh egg specimens , 2010, Behavioral Ecology and Sociobiology.

[15]  J. Ewen,et al.  Variability in Avian Eggshell Colour: A Comparative Study of Museum Eggshells , 2010, PloS one.

[16]  A. Gosler,et al.  Avian eggshell coloration: new perspectives on adaptive explanations , 2010 .

[17]  S. Merino,et al.  On the heritability of blue‐green eggshell coloration , 2010, Journal of evolutionary biology.

[18]  Y. Nys,et al.  The Role of Matrix Proteins in Eggshell Formation , 2010 .

[19]  T. Getty,et al.  Are brighter eggs better? Egg color and parental investment by House Wrens , 2010 .

[20]  H. Hoekstra,et al.  Vertebrate pigmentation: from underlying genes to adaptive function. , 2010, Trends in genetics : TIG.

[21]  D. Hanley,et al.  A Blackmail Hypothesis for the Evolution of Conspicuous Egg Coloration in Birds , 2010 .

[22]  J Zoons,et al.  The transmission color value: a novel egg quality measure for recording shell color used for monitoring the stress and health status of a brown layer flock. , 2010, Poultry science.

[23]  M. Hauber,et al.  Detecting pigments from colourful eggshells of extinct birds , 2010, Chemoecology.

[24]  E. Fukuda,et al.  Photodynamic antimicrobial activity of avian eggshell pigments , 2010, FEBS letters.

[25]  L. Lian,et al.  Comparison of the total amount of eggshell pigments in Dongxiang brown-shelled eggs and Dongxiang blue-shelled eggs. , 2009, Poultry science.

[26]  P. Cassey,et al.  Is sexual selection blurring the functional significance of eggshell coloration hypotheses? , 2009, Animal Behaviour.

[27]  P. Cassey,et al.  Extraction and analysis of colourful eggshell pigments using HPLC and HPLC/electrospray ionization tandem mass spectrometry. , 2009, Biomedical chromatography : BMC.

[28]  D. Hanley,et al.  Egg coloration in ring-billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis , 2009, Behavioral Ecology and Sociobiology.

[29]  D. Lahti.  Population Differentiation and Rapid Evolution of Egg Color in Accordance with Solar Radiation , 2008 .

[30]  G. Thomas.  Phylogenetic distributions of British birds of conservation concern , 2008, Proceedings of the Royal Society B: Biological Sciences.

[31]  A. Velando,et al.  Pigment allocation to eggs decreases plasma antioxidants in a songbird , 2008, Behavioral Ecology and Sociobiology.

[32]  N. Marshall,et al.  Eggshell colour does not predict measures of maternal investment in eggs of Turdus thrushes , 2008, Naturwissenschaften.

[33]  R. Ricklefs,et al.  PATTERNS OF GROWTH IN BIRDS , 2008 .

[34]  B. Bertram,et al.  ARE OSTRICH STRUTHIO CAMELUS EGGS THE WRONG COLOUR , 2008 .

[35]  D. Lack.  THE SIGNIFICANCE OF CLUTCH‐SIZE. Part III.—Some Interspecific Comparisons , 2008 .

[36]  D. Lack.  The Significance of Clutch‐size , 2008 .

[37]  L. Lian,et al.  Study of the deposition process of eggshell pigments using an improved dissolution method. , 2007, Poultry science.

[38]  L. Walker,et al.  Eggshell pigmentation indicates pesticide contamination , 2007 .

[39]  I. Cuthill,et al.  Using digital photography to study animal coloration , 2007 .

[40]  T. Grim,et al.  Are blue eggs a sexually selected signal of female collared flycatchers? A cross-fostering experiment , 2007, Behavioral Ecology and Sociobiology.

[41]  A. Møller,et al.  Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus , 2006, Behavioral Ecology and Sociobiology.

[42]  J. Moreno,et al.  Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird , 2006, Biology Letters.

[43]  A. Cockburn,et al.  Cryptic gentes revealed in pallid cuckoos Cuculus pallidus using reflectance spectrophotometry , 2006, Proceedings of the Royal Society B: Biological Sciences.

[44]  R. Kilner.  The evolution of egg colour and patterning in birds , 2006, Biological reviews of the Cambridge Philosophical Society.

[45]  A. Gosler,et al.  Speckled eggs: water-loss and incubation behaviour in the great tit Parus major , 2006, Oecologia.

[46]  S. Merino,et al.  Experimental evidence that egg color indicates female condition at laying in a songbird , 2006 .

[47]  Wickramasinghe M Bandaranayake,et al.  The nature and role of pigments of marine invertebrates. , 2006, Natural product reports.

[48]  T Troscianko,et al.  Stability of the color-opponent signals under changes of illuminant in natural scenes. , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[49]  A. Gosler,et al.  Why are birds' eggs speckled? , 2005 .

[50]  S. Beissinger,et al.  THE SHELF LIFE OF BIRD EGGS: TESTING EGG VIABILITY USING A TROPICAL CLIMATE GRADIENT , 2005 .

[51]  William R. Mathew,et al.  Color as a Science , 2005 .

[52]  S. Merino,et al.  Egg colouration and male parental effort in the pied flycatcher Ficedula hypoleuca , 2004 .

[53]  K. Wakamatsu,et al.  YOU CAN'T JUDGE A PIGMENT BY ITS COLOR: CAROTENOID AND MELANIN CONTENT OF YELLOW AND BROWN FEATHERS IN SWALLOWS, BLUEBIRDS, PENGUINS, AND DOMESTIC CHICKENS , 2004 .

[54]  J. Moreno,et al.  Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? , 2003 .

[55]  Bruce E. Lyon,et al.  Egg recognition and counting reduce costs of avian conspecific brood parasitism , 2003, Nature.

[56]  M. Pagel,et al.  Phylogenetic Analysis and Comparative Data: A Test and Review of Evidence , 2002, The American Naturalist.

[57]  K. Weidinger.  Does egg colour affect predation rate on open passerine nests? , 2001, Behavioral Ecology and Sociobiology.

[58]  G. Sorci.  Cuckoos, Cowbirds and Other Cheats , 2000, Animal Behaviour.

[59]  N. Davies,et al.  Cuckoos, Cowbirds and Other Cheats , 2000 .

[60]  M. Pagel.  Inferring the historical patterns of biological evolution , 1999, Nature.

[61]  Lionel R. Milgrom,et al.  The Colours of Life: An Introduction to the Chemistry of Porphyrins and Related Compounds , 1997 .

[62]  V. Holan,et al.  AVIAN EGGSHELL PIGMENTS AND THEIR VARIABILITY , 1996 .

[63]  B. Monroe,et al.  A World Checklist of Birds , 1993 .

[64]  F. Götmark.  Blue eggs do not reduce nest predation in the song thrush, Turdus philomelos , 1992, Behavioral Ecology and Sociobiology.

[65]  N. Davies,et al.  AN EXPERIMENTAL STUDY OF CO-EVOLUTION BETWEEN THE CUCKOO, CUCULUS CANORUS, AND ITS HOSTS. I. HOST EGG DISCRIMINATION , 1989 .

[66]  H. Southern,et al.  The Birds of the Western Palaearctic. Vol. IV. Terns to Woodpeckers , 1986 .

[67]  J. Felsenstein.  Phylogenies and the Comparative Method , 1985, The American Naturalist.

[68]  C. Harrison.  An Atlas of the Birds of the Western Palaearctic , 1982 .

[69]  T. Birkhead.  Behavioural adaptations to high density nesting in the common guillemot Uria aalge , 1978, Animal Behaviour.

[70]  A. E. Needham.  The Significance of Zoochromes , 1974, Zoophysiology and Ecology.

[71]  H. K. Poole.  Spectrophotometric Identification of Eggshell Pigments and Timing of Superficial Pigment Deposition in the Japanese Quail , 1965 .

[72]  Charles H. Gray.  The bile pigments. , 1957 .

[73]  A. Comfort.  THE PIGMENTATION OF MOLLUSCAN SHELLS , 1951 .

[74]  B. Gardiner,et al.  The Linnean Society of London , 1937, Nature.

[75]  J. M. Hipfner,et al.  EGG SIZE, EGGSHELL POROSITY, AND INCUBATION PERIOD IN THE MARINE BIRD FAMILY ALCIDAE , 2007 .

[76]  S. Beissinger,et al.  Microbial infection affects egg viability and incubation behavior in a tropical passerine , 2005 .

[77]  J. García‐Ruiz,et al.  General Palaeontology (Palaeobiochemistry) Avian eggshell mineralization: biochemical and functional characterization of matrix proteins , 2004 .

[78]  D. Deeming.  Avian Incubation: Behaviour, Environment, and Evolution , 2002 .

[79]  N. Otsu.  A Threshold Selection Method from Gray-Level Histograms , 1979, IEEE Trans. Syst. Man Cybern..

[80]  H. G. Vevers,et al.  A survey of avian eggshell pigments. , 1976, Comparative biochemistry and physiology. B, Comparative biochemistry.

[81]  N. Tinbergen,et al.  Egg Shell Removal By the Black-Headed Gull, Larus Ridibundus L.; a Behaviour Component of Camouflage , 1962 .

[82]  B. Gardiner,et al.  The Linnean Society of London , 1960, Nature.

[83]  R. Lemberg.  Bile pigments. VI. Biliverdin, uteroverdin and oocyan. , 1934, The Biochemical journal.

[84]  F. Kögl.,et al.  Zur Kenntnis der natürlichen Porphyrine (IV). Über das Coporphyrin. , 1923 .

[85]  A. Wallace.  Darwinism : an exposition of the theory of natural selection, with some of its applications / by Alfred Russel Wallace. , 1889 .