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Background

Females can differentially deposit the immune factor lysozyme into eggs based on conditions of local breeding density and laying order.

Materials

We collected 80 eggs from Great Cormorants (Phalacrocorax carbo) and then analyzed whether the level of lysozymes in the eggs is related to breeding density and laying order.

Results

Between clutches, the level of lysozyme in eggs is positively related to breeding density; while within a clutch, the level of lysozyme is positively related to the laying order.

Conclusion

When parents breed under conditions of high density, they allocate more lysozymes to their offspring, a trait adaptive to the local environment. That the increase in the level of lysozymes is a function of the laying order seems a necessary condition to mitigate the hierarchy among siblings for improving the survival of the entire clutch.


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Maternal lysozyme concentrations in the eggs of the Great Cormorant (Phalacrocorax carbo) in relation to breeding density and laying order

Show Author's information Jian Cao1,2Jirong Li1,2Wen Wang3Fang Yang1Zhuo Li1Laixing Li1( )
Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Science, 810001 Xining, China
University of Chinese Academy of Science, 100049 Beijing, China
Sichuan University, 610065 Chengdu, China

Abstract

Background

Females can differentially deposit the immune factor lysozyme into eggs based on conditions of local breeding density and laying order.

Materials

We collected 80 eggs from Great Cormorants (Phalacrocorax carbo) and then analyzed whether the level of lysozymes in the eggs is related to breeding density and laying order.

Results

Between clutches, the level of lysozyme in eggs is positively related to breeding density; while within a clutch, the level of lysozyme is positively related to the laying order.

Conclusion

When parents breed under conditions of high density, they allocate more lysozymes to their offspring, a trait adaptive to the local environment. That the increase in the level of lysozymes is a function of the laying order seems a necessary condition to mitigate the hierarchy among siblings for improving the survival of the entire clutch.

Keywords: Lysozyme, Survival, Great Cormorant, Innate immunity, Breeding density, Laying order, Phalacrocorax carbo

References(26)

Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy MW. Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Pro R Soc Lond B Bio Sci. 2002;269:29–36.

Brown CR, Brown MB. Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology. 1986;67:1206–18.

Clark AB, Wilson DS. Avian breeding adaptations: hatching asynchrony, brood reduction, and nest failure. Q Rev Biol. 1981;56:253–77.

Cook MI, Beissinger SR, Toranzos GA, Arendt WJ. Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett. 2005;8:532–7.

Danchin E, Wagner RH. The evolution of coloniality: the emergence of new perspectives. Trend Ecol Evol. 1997;12:342–7.

D'Alba L, Shawkey MD, Korsten P, Vedder O, Kingma SA, Komdeur J, Beissinger SR. Differential deposition of antimicrobial proteins in blue tit (Cyanistes caeruleus) clutches by laying order and male attractiveness. Behav Ecol Sociobiol. 2010;64:1037–45.PubMedCentral

Eising CM, Eikenaar C, Schwabl H, Groothuis TG. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B Biol Sci. 2001;268:839–46.

Gil D, Graves J, Hazon N, Wells A. Male attractiveness and differential testosterone investment in zebra finch eggs. Science. 1999;286:126–8.

Götmark F, Andersson M. Colonial breeding reduces nest predation in the Common Gull (Larus canus). Anim Behav. 1984;32:485–92.

Javurkova V, Krkavcova E, Kreisinger J, Hyrsl P, Hyankova L. Effects of experimentally increased in ovo lysozyme on egg hatchability, chicks complement activity, and phenotype in a precocial bird. J Exp Zool A Ecol Genet Physiol. 2015; 323:497–505.PubMed

Kaplan RH. Maternal influences on offspring development in the California newt, Taricha torosa. Copeia. 1985;4:1028–35.

Klasing K, Leshchinsky T. Functions, costs, and benefits of the immune system during development and growth. Ostrich. 1999;69:2817–32.

Kowalczyk K, Daiss J, Halpern J, Roth T. Quantitation of maternal-fetal IgG transport in the chicken. Immunology. 1985;54:755–62.

Lipar JL, Ketterson ED, Nolan V. Intraclutch variation in testosterone content of red-winged blackbird eggs. Auk. 1999;116:231–5.

Lipar JL, Ketterson ED. Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc Lond B Biol Sci. 2000;267:2005–10.

Mousseau TA, Fox CW. The adaptive significance of maternal effects. Trend Ecol Evol. 1998;13:403–7.

Pastoret PP, Griebel P, Bazin H, Govaerts A. Handbook of vertebrate Immunology. California: Academic Press; 1998.

Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R. Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B Biol Sci. 2002a;269:1729–33.

Saino N, Dall'Ara P, Martinelli R, Møller A. Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the barn swallow. J Evol Biol. 2002b;15:735–43.

Schwabl H. Yolk is a source of maternal testosterone for developing birds. Proc Nat Acad Sci USA. 1993;90:11446–50.PubMedCentral

Schwabl H. A hormonal mechanism for parental favouritism. Nature. 1997;386:231.

Shawkey MD, Kosciuch KL, Liu M, Rohwer FC, Loos ER, Wang JM, Beissinger SR. Do birds differentially distribute antimicrobial proteins within clutches of eggs? Behav Ecol. 2008;19:920–7.

Stoleson SH, Beissinger SR. Hatching asynchrony and the onset of incubation in birds, revisited. New York: Plenum Press; 1995.

DOI

Tella JL. The evolutionary transition to coloniality promotes higher blood parasitism in birds. J Evol Biol. 2002;15:32–41.

Trziszka T. Lysozyme and its functions in the egg. Arch Geflugelk. 1994;58:49–54.

Vinuela J. Adaptation vs. constraint: intraclutch egg-mass variation in birds. J Anim Ecol. 1997;66:781–92.

Publication history
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Publication history

Received: 07 April 2015
Accepted: 09 October 2015
Published: 20 November 2015
Issue date: January 2015

Copyright

© 2015 Cao et al.

Acknowledgements

Acknowledgements

We thank the entire staff of the Qinghai Lake National Nature Reserve for its assistance when we worked in the field, as well as Krill, Shouyang Du, Chao Ma and Xuze Zhang for their help in the laboratory. We are grateful to Shuli Liu whose advice improved significantly the data analysis. This study was financially supported by the State Forestry Administration Program (Grant Nos. Y31I351B01), the National Natural Science Foundation of China (Grant Nos. Y011331501), the National Science & Technology Pillar Program (Grant Nos. 2008BADB0B0303) and National Basic Research Program of China (Grant Nos. 2010CB530301).

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