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Innate humoural immunity is related to eggshell bacterial load of European birds: a comparative analysis

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Abstract

Fitness benefits associated with the development of a costly immune system would include not only self-protection against pathogenic microorganisms but also protection of host offspring if it reduces the probability and the rate of vertical transmission of microorganisms. This possibility predicts a negative relationship between probabilities of vertical transmission of symbionts and level of immune response that we here explore inter-specifically. We estimated eggshell bacterial loads by culturing heterotrophic bacteria, Enterococcus, Staphylococcus and Enterobacteriaceae on the eggshells of 29 species of birds as a proxy of vertical transmission of bacteria from mother to offspring. For this pool of species, we also estimated innate immune response (natural antibody and complement (lysis)) of adults, which constitute the main defence against bacterial infection. Multivariate general linear models revealed the predicted negative association between natural antibodies and density of bacteria on the eggshell of 19 species of birds for which we sampled the eggs in more than one nest. Univariate analyses revealed significant associations for heterotrophic bacteria and for Enterobacteriaceae, a group of bacteria that includes important pathogens of avian embryos. Therefore, these results suggest a possible trans-generational benefit of developing a strong immune system by reducing vertical transmission of pathogens.

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References

  • Barrow PA (1994) The microflora of the alimentary tract and avian pathogens: translocation and vertical transmission. In: Board RG, Fuller R (eds) Microbiology of avian eggs. Chapman & Hall, London, pp 117–138

    Chapter  Google Scholar 

  • Board RG, Fuller R (1994) Microbiology of the avian egg. Chapman & Hall, London

    Google Scholar 

  • Bruce J, Drysdale EM (1994) Trans-shell transmission. In: Board RG, Fuller R (eds) Microbiology of avian eggs. Chapman & Hall, London, pp 63–91

    Chapter  Google Scholar 

  • Clark L, Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia 67:169–176

    Article  Google Scholar 

  • Clark L, Mason JR (1988) Effect of biologically active plants used as nest material and the derived benefit to starling nestlings. Oecologia 77:174–180

    Article  Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2003) Trans-shell infection by pathogenic micro-organisms reduces the shelf life of non-incubated bird’s eggs: a constraint on the onset of incubation? Proc R Soc Lond B 270:2233–2240

    Article  Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005a) Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Letters 8:532–537

    Article  Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2005b) Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behav Ecol 16:30–36

    Article  Google Scholar 

  • Cotter SC, Kilner RM (2010) Personal immunity versus social immunity. Behav Ecol 21:663–668

    Article  Google Scholar 

  • Franz CMAP, Holzapfel WH, Stiles ME (1999) Enterococci at the crossroads of food safety? Int J Food Microbiol 47:1–24

    Article  PubMed  CAS  Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    Article  PubMed  CAS  Google Scholar 

  • Gallizzi K, Guenon B, Richner H (2008) Maternally transmitted parasite defence can be beneficial in the absence of parasites. Oikos 117:223–230

    Article  Google Scholar 

  • Garamszegi LZ, Møller AP (2010) Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta-analytic review. Biol Rev 4:797–805

    Google Scholar 

  • Gerhardt P (1981) Manual of methods for general bacteriology. American Society for Microbiology, Washington, DC

    Google Scholar 

  • Giraffa G (2004) Studying the dynamics of microbial populations during food fermentation. FEMS Microbiol Rev 28:251–260

    Article  PubMed  CAS  Google Scholar 

  • Giraffa G, Neviani E (2001) DNA-based, culture-independent strategies for evaluating microbial communities in food-associated ecosystems. Int J Food Microbiol 67:19–34

    Article  PubMed  CAS  Google Scholar 

  • Gunderson AR (2008) Feather degrading bacteria: a new frontier in avian and host–parasite research? Auk 125:972–979

    Article  Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Houston CS, Saunders JR, Crawford RD (1997) Aerobic bacterial flora of addled raptor eggs in Saskatchewan. J Wildl Dis 33:328–331

    PubMed  CAS  Google Scholar 

  • Jønsson KA, Fjeldså J (2006) A phylogenetic supertree of oscine passerine birds (Aves: Passeri). Zool Scripta 35:149–186

    Article  Google Scholar 

  • Krieg NR, Holt JG (1984) Bergey’s manual of systematic bacteriology. Williams & Wilkins, Baltimore

    Google Scholar 

  • Matson KD, Ricklefs RE, Klasing KC (2005) A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Imm 29:275–286

    Article  CAS  Google Scholar 

  • Matson KD, Tieleman BI, Klasing KC (2006) Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds. Physiol Biochem Zool 79:556–564

    Article  PubMed  Google Scholar 

  • Mennerat A, Mirleau P, Blondel J, Perret P, Lambrechts M, Heeb P (2009) Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria. Oecologia 161:849–855

    Article  PubMed  Google Scholar 

  • Møller AP (1987) Egg predation as a selective factor for nest design: an experiment. Oikos 50:91–94

    Article  Google Scholar 

  • Møller AP (1997) Parasitism and the evolution of host life history. In: Clayton DH, Moore J (eds) Host–parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 105–127

    Google Scholar 

  • Møller AP, Erritzøe J (1996) Parasite virulence and host immune defense: host immune response is related to nest reuse in birds. Evolution 50:2066–2072

    Article  Google Scholar 

  • Møller AP, Haussy C (2007) Fitness consequences of variation in natural antibodies and complement in the Barn Swallow Hirundo rustica. Funct Ecol 21:363–371

    Article  Google Scholar 

  • Møller AP, Merino S, Brown CR, Robertson RJ (2001) Immune defense and host sociality: a comparative study of swallows and martins. Am Nat 158:136–145

    Article  PubMed  Google Scholar 

  • Møller AP, Martin-Vivaldi M, Soler JJ (2004) Parasitism, host immune defence and dispersal. J Evol Biol 17:603–612

    Article  PubMed  Google Scholar 

  • Møller AP, Nielsen JT, Garamszegi LZ (2008) Risk taking by singing males. Behav Ecol 19:41–53

    Article  Google Scholar 

  • Moreno J, Briones V, Merino S, Ballesteros C, Sanz JJ, Tomás G (2003) Beneficial effects of cloacal bacteria on growth and fledging size in nestling pied flycatchers (Ficedula hypoleuca) in Spain. Auk 120:784–790

    Article  Google Scholar 

  • Narushin VG (2005) Production, modeling, and education: egg geometry calculation using the measurements of length and breadth. Poultry Sci 84:482–484

    CAS  Google Scholar 

  • Nde CW, Mcevoy JM, Sherwood JS, Logue CM (2007) Cross contamination of turkey carcasses by Salmonella species during defeathering. Poultry Sci 86:162–167

    CAS  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    Article  PubMed  CAS  Google Scholar 

  • Peralta-Sánchez JM, Møller AP, Martín-Platero AM, Soler JJ (2010) Number and colour composition of nest lining feathers predict eggshell bacterial community in barn swallow nests: an experimental study. Funct Ecol 24:426–433

    Article  Google Scholar 

  • Playfair J, Bancroft G (2004) Infection and immunity. Oxford University Press, Oxford

    Google Scholar 

  • Roth O, Joop G, Eggert H, Hilbert J, Daniel J, Schmid-Hempel P, Kurtz J (2010) Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J Anim Ecol 79:403–413

    Article  PubMed  Google Scholar 

  • Ruiz-de-Castañeda R, Vela AI, Lobato E, Briones V, Moreno J (2011a) Bacterial loads on eggshells of the pied flycatcher: environmental and maternal factors. Condor 113:200–208

    Article  Google Scholar 

  • Ruiz-de-Castañeda R, Vela AI, Lobato E, Briones V, Moreno J (2011b) Prevalence of potentially pathogenic culturable bacteria on eggshells and in cloacae of female Pied Flycatchers in a temperate habitat in central Spain. J Field Ornithol 82:215–224

    Article  Google Scholar 

  • Sæther SA, Grøtan V, Engen S, Noble DG, Freckleton RP (2011) Rarity, life history and scaling of the dynamics in time and space of British birds. J Anim Ecol 80:215–224

    Article  PubMed  Google Scholar 

  • Saino N, Dall’ara P, Martinelli R, Møller AP (2002a) Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the barn swallow. J Evol Biol 15:735–743

    Article  CAS  Google Scholar 

  • Saino N, Ferrari RP, Martinelli R, Romano M, Rubolini D, Møller AP (2002b) Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc R Soc Lond B 269:1005–1009

    Article  Google Scholar 

  • Salyers AA, Whitt DD (2002) Bacterial pathogenesis. A molecular approach. ASM, Washington, DC

    Google Scholar 

  • Shawkey MD, Firestone MK, Brodie EL, Beissinger SR (2009) Avian incubation inhibits growth and diversification of bacterial assemblages on eggs. PLoS One 4:e4522

    Article  PubMed  Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven

    Google Scholar 

  • Singleton DR, Harper RG (1998) Bacteria in old house wren nests. J Field Ornithol 69:71–74

    Google Scholar 

  • Soler JJ, Martín-Vivaldi M, Haussy C, Møller AP (2007) Intra- and interspecific relationships between nest size and immunity. Behav Ecol 18:781–791

    Article  Google Scholar 

  • Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, Peralta-Sánchez JM, Méndez M (2008) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22:864–871

    Article  Google Scholar 

  • Soler JJ, Martín-Vivaldi M, Peralta-Sánchez JM, Ruiz-Rodríguez M (2010) Antibiotic-producing bacteria as a possible defence of birds against pathogenic microorganisms. Open Ornithology Journal 3:93–100

    Google Scholar 

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Acknowledgements

We thank E. Lopez-Hernández for technical assistance in the lab. This study was funded by a graduate research grant from Junta de Andalucia to JMP and by Ministerio de Ciencia e Innovación/FEDER (project CGL2010-19233-C03-01) and the Junta de Andalucía (P09-RNM-4557).

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Correspondence to Juan José Soler.

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Communicated by: Sven Thatje

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Soler, J.J., Peralta-Sánchez, J.M., Flensted-Jensen, E. et al. Innate humoural immunity is related to eggshell bacterial load of European birds: a comparative analysis. Naturwissenschaften 98, 807 (2011). https://doi.org/10.1007/s00114-011-0830-z

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  • DOI: https://doi.org/10.1007/s00114-011-0830-z

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