Abstract
The known chemical basis of diverse avian eggshell coloration is generated by the same two classes of tetrapyrrole pigments in most living birds. We aimed to extend the evolutionary scope of these patterns by detecting pigments from extinct birds’ eggs. In our samples biliverdin was successfully extracted from subfossil shell fragments of the blue-green egg-laying upland moa Megalapteryx didinus, while protoporphyrin was extracted from the beige eggs of two other extinct moa species. Our data on pigment detection from eggshells of other extant paleognath birds, together with published information on other modern lineages, confirm tetrapyrroles as ubiquitous and conserved pigments contributing to diverse eggshell colours throughout avian evolution.
References
Aviles JM, Stokke BG, Moksnes A, Roskaft E, Moller AP (2007) Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus. Behav Ecol Sociobiol 61:475–485
Brennan PLR (2009) Incubation behavior of great tinamous (Tinamus major). Wilson J Ornithol 121:506–511
Bunce M, Worthy TH, Ford T, Hoppitt W, Willerslev E, Drummond A, Cooper A (2003) Extreme reversed sexual size dimorphism in the extinct New Zealand moa Dinornis. Nature 425:172–175
Bunce M, Worthy TH, Phillips MJ, Holdaway RN, Willerslev E, Haile J, Shapiro B, Scofield RP, Drummond A, Kamp PJJ, Cooper A (2009) The evolutionary history of the extinct ratite moa and New Zealand Neogene paleogeography. Proc Natl Acad Sci USA 106:20646–20651
Cassey P, Honza M, Grim T, Hauber ME (2008) The modeling of avian visual perception predicts behavioural rejection responses to foreign egg colours. Biol Lett 4:515–517
Cassey P, Ewen JG, Marshall NJ, Vorobyev M, Blackburn TM, Hauber ME (2009) Are avian eggshell colours effective intraspecific communication signals? A perceptual modeling approach. Ibis 151:689–698
Corfield JR, Wild JM, Hauber ME, Parsons S, Kubke MF (2008) Evolution of brain size in the Palaeognath lineage, with an emphasis on New Zealand ratites. Brain Behav Evol 71:87–99
Fadzly N, Jack C, Schaefer HM, Burns KC (2009) Ontogenetic colour changes in an insular tree species: signalling to extinct browsing birds? New Phytol 184:495–501
Gill BJ (2007) Eggshell characteristics of moa eggs (Aves: Dinornithiformes). J R Soc N Z 37:139–150
Gorchein A, Lim CK, Cassey P (2009) Extraction and analysis of colourful eggshell pigments using HPLC and HPLC/electrospray ionization tandem mass spectrometry. Biomed Chromatogr 23:602–606
Huynen L, Millar CD, Scofield RP, Lambert DM (2003) Nuclear DNA sequences detect species limits in ancient moa. Nature 425:175–178
Kennedy GY, Vevers HG (1976) A survey of eggshell pigments. Comp Biochem Physiol B Biochem Mol Biol 55:117–123
Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406
Miksik I, Holan V, Deyl Z (1996) Avian eggshell pigments and their variability. Comp Biochem Physiol B 113:607–612
Miksik I, Eckhardt A, Sedlakova P, Mikulikova K (2007) Proteins of insoluble matrix of avian (Gallus gallus) eggshell. Connect Tissue Res 48:1–8
Moreno J, Lobato E, Morales J, Merino S, Tomas G, Martinez-de la Puente J, Sanz JJ, Mateo R, Soler JJ (2006) Experimental evidence that egg color indicates female condition at laying in a songbird. Behav Ecol 17:651–655
Patek SN, Oakley TH (2003) Comparative tests of evolutionary tradeoffs in a palinurid lobster acoustic system. Evolution 57:2082–2100
Rawlence NJ, Wood JR, Armstrong KN, Cooper A (2009) DNA content and distribution in ancient feathers and potential to reconstruct the plumage of extinct avian taxa. Proc R Soc Lond B 276:3395–3402
Reynolds SJ, Martin GR, Cassey P (2009) Is sexual selection blurring the functional significance of eggshell coloration hypotheses? Anim Behav 78:209–215
Sharp RM, Silyn-Roberts H (1984) Development of preferred orientation in the eggshell of the domestic fowl. Biophys J 46:175–179
Starling M, Heinsohn R, Cockburn A, Langmore NE (2006) Cryptic gentes revealed in pallid cuckoos Cuculus pallidus using reflectance spectrophotometry. Proc R Soc Lond B 273:1929–1934
Tennyson A, Martinson P (2006) Extinct birds of New Zealand. Te Papa Press, Wellington
Turvey ST, Green OR, Holdaway RN (2005) Cortical growth marks reveal extended juvenile development in New Zealand moa. Nature 435:940–943
Varricchio DJ, Moore JR, Erickson GM, Norell MA, Jackson FD, Borkowski JJ (2008) Avian paternal care had dinosaur origin. Science 322:1826
Walters M (1994) Birds’ eggs. Dorling Kindersley, London
Wang XT, Zhao CJ, Li JY, Xu GY, Lian LS, Wu CX, Deng XM (2009) Comparison of the total amount of eggshell pigments in Dongxiang brown-shelled and Dongxiang blue-shelled eggs. Poult Sci 88:1735–1739
Zelenitsky DK, Therrien F, Kobayashi Y (2009) Olfactory acuity in theropods: palaeobiological and evolutionary implications. Proc R Soc Lond B 276:667–673
Acknowledgments
We are grateful to the School of Biological Sciences at the University of Auckland for major support. We thank D. Dearborn, M. Hyland, C. Moskat, H. Silyn-Roberts, The University of Auckland Vice-Chancellor’s Development Fund and the Human Frontier Science Program (to P.C., T.G. and M.E.H.) for assistance, discussions, and funding.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Igic, B., Greenwood, D.R., Palmer, D.J. et al. Detecting pigments from colourful eggshells of extinct birds. Chemoecology 20, 43–48 (2010). https://doi.org/10.1007/s00049-009-0038-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-009-0038-2