First Documented Report of Complete Shell Pigment Loss in the Blue-Green Eggs of the Pied Flycatcher

  1. Fuertes-Recuero, Manuel 1
  2. Cantarero, Alejandro 1
  1. 1 Universidad Complutense de Madrid
    info

    Universidad Complutense de Madrid

    Madrid, España

    ROR 02p0gd045

Revista:
Ardea

ISSN: 0373-2266,  2213-1175

Any de publicació: 2024

Volum: 112

Número: 1

Pàgines: 152-157

Tipus: Article

DOI: 10.5253/ARDE.2023.A22 GOOGLE SCHOLAR lock_openAccés obert editor

Altres publicacions en: Ardea

Resum

The marked variation in egg coloration within many bird species has attracted the interest of evolutionary biologists for decades. Many species, such as the Pied Flycatcher Ficedula hypoleuca, use biliverdin pigment to lay vibrant blue-green eggs that function as a signal of female condition to increase parental care from their partner. Here we report on the first case of complete shell pigment loss in this species. So far, we have monitored thousands of Pied Flycatcher clutches over 33 breeding seasons, and we have never observed such a phenomenon before. We observed and studied a complete clutch of five eggs with shell pigment loss. We evaluated the condition of the female and performed blood smears to discuss the potential causes of this phenomenon. The most plausible hypothesis that explains the finding is a genetic mutation affecting the biliverdin production pathway.

Referències bibliogràfiques

  • D.C. Lahti and D.R. Ardia "Am. Nat." 187, "Shedding light on bird egg color: pigment as parasol and the dark car effect." 547 (2016)
  • J. Moreno and J.L. Osorno "Ecol. Lett." 6, "Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality?" 803 (2003)
  • D.P. Bai, X.Y. Lin, Y. Wu, et al. "BMC Genomics." 20, "Isolation of blue-green eggshell pigmentation-related genes from Putian duck through RNA-seq." 66 (2019)
  • T. Baird, S.E. Solomon, D.R. Tedstone, "Br. Poult. Sci." 16, "Localisation and characterisation of egg shell porphyrins in several avian species." 201 (1975)
  • G.D. Butcher and R.D. Miles "Cooperative Extension Service Fact Sheet VM94." "Factors causing poor pigmentation of brown-shelled eggs." (2011)
  • K.K. Chousalkar, B.F. Cheetham, J.R. Roberts, "J. Virol. Methods." 155, "LNA probe-based real-time RT-PCR for the detection of infectious bronchitis virus from the oviduct of unvaccinated and vaccinated laying hens." 67 (2009)
  • N.B. Davies and M.D.L. Brooke "J. Anim. Ecol." 58, "An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. Host egg discrimination." 207 (1989)
  • T.A. Ebeid, T. Suzuki, T. Sugiyama, "Poult. Sci." 91, "High ambient temperature influences eggshell quality and calbindin-D28k localization of eggshell gland and all intestinal segments of laying hens." 2282 (2012)
  • K.H. Falchuk, J.M. Contin, T.S. Dziedzic, et al. "Proc. Natl. Acad. Sci. USA." 99, "A role for biliverdin IXalpha in dorsal axis development of Xenopus laevis embryos." 251 (2002)
  • R.B. Fronstin, S.M. Doucet, J.K. Christians, "BMC Ecol." 16, "Haematocrit, eggshell colouration and sexual signaling in the European starling (Sturnus vulgaris)." 31 (2016)
  • R. Hamchand, D. Hanley, R.O. Prum, et al. "Sci. Rep." 10, "Expanding the eggshell colour gamut: uroerythrin and bilirubin from tinamou (Tinamidae) eggshells." 11264 (2020)
  • D. Hanley, S.M. Doucet, D.C. Dearborn, "Auk." 127, "A blackmail hypothesis for the evolution of conspicuous egg coloration in birds." 453 (2010)
  • D. Hanley, T. Grim, P. Cassey, et al. "Biol. Lett." 11, "Not so colourful after all: eggshell pigments constrain avian eggshell colour space." 15 (2015)
  • R. Hargitai, N. Boross, S. Hámori, et al. "Physiol. Biochem. Zool." 90, "Eggshell biliverdin and protoporphyrin pigments in a songbird: are they derived from erythrocytes, blood plasma, or the shell gland?" 613 (2017)
  • K.P.M. Heirwegh, J. Fevery, N. Blanckaert, "J. Chromatogr. B." 496, "Chromatographic analysis and structure determination of biliverdins and bilirubins." 1 (1989)
  • J.A. Himes and C.E. Cornelius "Cornell Vet." 65, "Biliverdin and bilirubin excretion in the turkey." 374 (1975)
  • B.O. Hughes, A.B. Gilbert, M.F. Brown, "Br. Poult. Sci." 27, "Categorisation and causes of abnormal egg shells: relationship with stress." 325 (1986)
  • A. Jagannath, R.F. Shore, L.A. Walker, et al. "J. Appl. Ecol." 45, "Eggshell pigmentation indicates pesticide contamination." 133 (2008)
  • H. Kaur, M.N. Hughes, C.J. Green, et al. "FEBS Lett." 543, "Interaction of bilirubin and biliverdin with reactive nitrogen species." 113 (2003)
  • G.Y. Kennedy and H.G. Vevers "Comp. Biochem. Physiol. B." 55, "A survey of avian eggshell pigments." 117 (1976)
  • S. Khan, J. Roberts, S.B. Wu, "BMC Mol. Cell Biol." 20, "Genes involved in mitochondrial biogenesis and function may not show synchronised responses to mitochondria in shell gland of laying chickens under infectious bronchitis virus challenge." 3 (2019)
  • M. Krist and T. Grim "Behav. Ecol. Sociobiol." 61, "Are blue eggs a sexually selected signal of female collared flycatchers? A cross-fostering experiment." 863 (2007)
  • G. Lin, J. Himes, C. Cornelius, "Am. J. Physiol." 226, "Bilirubin and biliverdin excretion by the chicken." 881 (1974)
  • R. Mateo, W.N. Beyer, J. Spann, et al. "J. Toxicol. Environ." 66, "Relationship between oxidative stress, pathology, and behavioral signs of lead poisoning in mallards." 1371 (2003)
  • A.F. McDonagh, "Nat. Struct. Biol." 8, "Turning green to gold." 198 (2001)
  • K. Mertens, I. Vaesen, J. Loffel, et al. "Poult. Sci." 89, "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." 609 (2010)
  • I. Miksik, V. Holáň, Z. Deyl, "Comp. Biochem. Physiol." 109, "Quantification and variability of eggshell pigment content." 769 (1994)
  • J. Morales, "BioEssays." 42, "Eggshell biliverdin as an antioxidant maternal effect: biliverdin as an antioxidant resource in oviparous animals." 2000010 (2020)
  • J. Moreno, E. Lobato, J. Morales, et al. "Behav. Ecol." 17, "Experimental evidence that egg color indicates female condition at laying in a songbird." 651 (2006)
  • J. Moreno, J. Morales, E. Lobato, et al. "Behav. Ecol." 16, "Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca." 931 (2005)
  • M. Noguchi, T. Yoshida, G. Kikuchi, "FEBS Lett." 98, "Specific requirement of NADPH-cytochrome c reductase for the microsomal heme oxygenase reaction yielding biliverdin IX alpha." 281 (1979)
  • L.E. Otterbein, M.P. Soares, K. Yamashita, et al. "Trends Immunol." 24, "Heme oxygenase-1: unleashing the protective properties of heme." 449 (2003)
  • D. Phelan, G.M. Winter, W.J. Rogers, et al. "Arch. Biochem. Biophys." 357, "Activation of the Ah receptor signal transduction pathway by bilirubin and biliverdin." 155 (1998)
  • W.M. Schluchter and A.N. Glazer "J Biol. Chem." 272, "Characterization of cyanobacterial biliverdin reductase. Conversion of biliverdin to bilirubin is important for normal phycobiliprotein biosynthesis." 13562 (1997)
  • Y. Shi, J. Kovacs-Nolan, B. Jiang, et al. "J. Funct. Foods." 10, "Antioxidant activity of enzymatic hydrolysates from eggshell membrane proteins and its protective capacity in human intestinal epithelial Caco-2 cells." 35 (2014)
  • L. Siefferman, K.J. Navara, G.E. Hill, "Behav. Ecol. Sociobiol." 59, "Egg coloration is correlated with female condition in eastern bluebirds (Sialia sialis)." 651 (2006)
  • R. Stocker, Y. Yamamoto, A.F. McDonagh, et al. "Science." 235, "Bilirubin is an antioxidant of possible physiological importance." 1043 (1987)
  • M.C. Stoddard, K.L.A. Marshall, R.M. Kilner, "Avian Biol. Res." 4, "Imperfectly Camouflaged Avian Eggs: Artefact or Adaptation?" 196 (2011)
  • A.W. Walker and B.O. Hughes "Br. Poult. Sci." 39, "Egg shell colour is affected by laying cage design." 696 (1998)
  • Z. Zhu, A.T. Wilson, B.A. Luxon, et al. "Hepatology." 52, "Biliverdin inhibits hepatitis C virus nonstructural 3/4A protease activity: Mechanism for the antiviral effects of heme oxygenase?" 1897 (2010)