Transfer of maternal antibodies against avian influenza virus in mallards (Anas platyrhynchos)

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Van Dijk, Jacintha G B ^a   Mateman, A Christa ^a   Klaassen, Marcel ^a,b  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b DEAKIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MATERNAL ANTIBODY;

ANAS PLATYRHYNCHOS; ANTIBODY BLOOD LEVEL; ANTIBODY DETECTION; ANTIBODY TITER; ARTICLE; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS; BODY MASS; CONTROLLED STUDY; EGG LAYING; EGG SIZE; EGG YOLK; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; HOST PARASITE INTERACTION; HOST RESISTANCE; NONHUMAN; PARASITE TRANSMISSION; PASSIVE IMMUNIZATION; SEX DETERMINATION; WATERFOWL; ANIMAL; BODY SIZE; IMMUNOLOGY; MALE; SEX DIFFERENCE; VIROLOGY;

ANAS PLATYRHYNCHOS; ANSERIFORMES; AVIAN INFLUENZA VIRUS;

ANIMALS; ANSERIFORMES; BODY SIZE; EGG YOLK; FEMALE; IMMUNITY, MATERNALLY-ACQUIRED; INFLUENZA IN BIRDS; MALE; SEX FACTORS;

EID: 84918838501     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112595     Document Type: Article

References (65)

1. Boulinier T, Staszewski V (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23: 282-288. doi:10.1016/j.tree.2007.12.006.
2. King MO, Owen JP, Schwabl HG (2010) Are maternal antibodies really that important? Patterns in the immunologic development of altricial passerine house sparrows (Passer domesticus). PLoS One 5: e9639. doi:e963910.1371/journal.pone.0009639.
3. Garnier R, Ramos R, Staszewski V, Militão T, Lobato E, et al. (2012) Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology. Proc R Soc B-Biol Sci 279: 2033-2041. doi:10.1098/rspb.2011.2277.
4. Grindstaff JL, Hasselquist D, Nilsson JA, Sandell M, Smith HG, et al. (2006) Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proc R Soc B-Biol Sci 273: 2551-2557. doi:10.1098/rspb.2006.3608.
5. Staszewski V, Gasparini J, McCoy KD, Tveraa T, Boulinier T (2007) Evidence of an interannual effect of maternal immunization on the immune response of juveniles in a long-lived colonial bird. J Anim Ecol 76: 1215-1223. doi:10.1111/j.1365-2656.2007.01293.x.
6. Hasselquist D, Nilsson JA (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos Trans R Soc B-Biol Sci 364: 51-60. doi:10.1098/rstb.2008.0137.
7. Pearce-Duvet JMC, Gauthier-Clerc M, Jourdain E, Boulinier T (2009) Maternal antibody transfer in yellow-legged gulls. Emerg Infect Dis 15: 1147-1149. doi:10.3201/eid1507.090036.
8. Hinshaw VS, Air GM, Gibbs AJ, Graves L, Prescott B, et al. (1982) Antigenic and genetic characterization of a novel hemagglutinin subtype of influenza A viruses from gulls. J Virol 42: 865-872.
9. Fouchier RAM, Munster VJ, Wallensten A, Bestebroer TM, Herfst S, et al. (2005) Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79: 2814-2822. doi:10.1128/jvi.79.5.2814-2822.2005.
10. Velarde R, Calvin SE, Ojkic D, Barker IK, Nagy E (2010) Avian influenza virus H13 circulating in ring-billed gulls (Larus delawarensis) in southern Ontario, Canada. Avian Dis 54: 411-419. doi:10.1637/8808-040109-Reg.1.
11. Hammouda A, Pearce-Duvet J, Chokri MA, Arnal A, Gauthier-Clerc M, et al. (2011) Prevalence of influenza A antibodies in yellow-legged gull (Larus michahellis) eggs and adults in southern Tunisia. Vector-Borne Zoonotic Dis 11: 1583-1590. doi:10.1089/vbz.2011.0639.
12. Hammouda A, Selmi S, Pearce-Duvet J, Chokri MA, Arnal A, et al. (2012) Maternal antibody transmission in relation to mother fluctuating asymmetry in a long-lived colonial seabird: the yellow-legged gull Larus michahellis. PLoS One 7: e34966. doi:10.1371/journal.pone.0034966.
13. Grindstaff JL, Demas GE, Ketterson ED (2005) Diet quality affects egg size and number but does not reduce maternal antibody transmission in Japanese quail Coturnix japonica. J Anim Ecol 74: 1051-1058. doi:10.1111/j.1365-2656.2005.01002.x.
14. Grindstaff JL (2010) Initial levels of maternally derived antibodies predict persistence time in offspring circulation. J Ornithol 151: 423-428. doi:10.1007/s10336-009-0472-5.
15. Hargitai R, Prechl J, Torok J (2006) Maternal immunoglobulin concentration in collared flycatcher (Ficedula albicollis) eggs in relation to parental quality and laying order. Funct Ecol 20: 829-838. doi:10.1111/j.1365-2435.2006.01171.x.
16. Martyka R, Rutkowska J, Cichon M (2011) Sex-specific effects of maternal immunization on yolk antibody transfer and offspring performance in zebra finches. Biol Lett 7: 50-53. doi:10.1098/rsbl.2010.0549.
17. Gasparini J, McCoy KD, Tveraa T, Boulinier T (2002) Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecol Lett 5: 519-524. doi:10.1046/j.1461-0248.2002.00345.x.
18. Karell P, Kontiainen P, Pietiäinen H, Siitari H, Brommer JE (2008) Maternal effects on offspring Igs and egg size in relation to natural and experimentally improved food supply. Funct Ecol 22: 682-690. doi:10.1111/j.1365-2435.2008.01425.x.
19. Grindstaff JL, Brodie ED, Ketterson ED (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc R Soc B-Biol Sci 270: 2309-2319. doi:10.1098/rspb.2003.2485.
20. Jacquin L, Haussy C, Bertin C, Laroucau K, Gasparini J (2013) Darker female pigeons transmit more specific antibodies to their eggs than do paler ones. Biol J Linnean Soc 108: 647-657. doi:10.1111/bij.12001.
21. Müller W, Groothuis TGG, Dijkstra C, Siitari H, Alatalo RV (2004) Maternal antibody transmission and breeding densities in the black-headed gull Larus ridibundus. Funct Ecol 18: 719-724. doi:10.1111/j.0269-8463.2004.00902.x.
22. Saino N, Ferrari RP, Martinelli R, Romano M, Rubolini D, et al. (2002) Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc R Soc B-Biol Sci 269: 1005-1009. doi:10.1098/rspb.2002.1992.
23. Morales J, Sanz JJ, Moreno J (2006) Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. Biol Lett 2: 334-336. doi:10.1098/rsbl.2006.0471.
24. Holveck MJ, Grégoire A, Staszewski V, Guerreiro R, Perret P, et al. (2012) Eggshell spottiness reflects maternally transferred antibodies in blue tits. PLoS One 7: e50389. doi:10.1371/journal.pone.0050389.
25. Groothuis TGG, Eising CM, Blount JD, Surai P, Apanius V, et al. (2006) Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. J Evol Biol 19: 1304-1313. doi:10.1111/j.1420-9101.2005.01072.x.
26. Pihlaja M, Siitari H, Alatalo RV (2006) Maternal antibodies in a wild altricial bird: effects on offspring immunity, growth and survival. J Anim Ecol 75: 1154-1164. doi:10.1111/j.1365-2656.2006.01136.x.
27. Saino N, Romano M, Ferrari RP, Martinelli R, Møller AP (2003) Maternal antibodies but not carotenoids in barn swallow eggs covary with embryo sex. J Evol Biol 16: 516-522. doi:10.1046/j.1420-9101.2003.00534.x.
28. Abad-Gomez JM, Masero JA, Villegas A, Albano N, Gutiérrez JS, et al. (2012) Sex-specific deposition and survival effects of maternal antibodies: a case study with the gull-billed tern Gelochelidon nilotica. J Avian Biol 43: 491-495. doi:10.1111/j.1600-048X.2012.05792.x.
29. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus ADME, et al. (2006) Global patterns of influenza A virus in wild birds. Science 312: 384-388. doi:10.1126/science.1122438.
30. Pehrsson O (1991) Egg and clutch size in the mallard as related to food quality. Can J Zool-Rev Can Zool 69: 156-162. doi:10.1139/z91-024.
31. Boyd H, Harrison J, Allison A (1975) Duck wings: a study of duck production. Chester: Marley Ltd., and the Harrison Zoological Museum. 112 p.
32. Byers SM, Cary JR (1991) Discrimination of mallard strains on the basis of morphology. J Wildl Manage 55: 580-586.
33. Baker K (1993) Identification Guide to European Non-Passerines. London: Butler & Tanner. 336 p.
34. Hoye BJ (2012) Variation in postsampling treatment of avian blood affects ecophysiological interpretations. Methods Ecol Evol 3: 162-167. doi:10.1111/j.2041-210X.2011.00135.x.
35. Kowalczyk K, Daiss J, Halpern J, Roth TF (1985) Quantitation of maternal-fetal IgG transport in the chicken. Immunology 54: 755-762.
36. Mohammed HO, Yamamoto R, Carpenter TE, Ortmayer HB (1986) Comparison of egg yolk and serum for the detection of mycoplasma gallisepticum and mycoplasma synoviae antibodies by enzyme-linked immunosorbent assay. Avian Dis 30: 398-408.
37. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
38. Jacobson RH (1998) Validation of serological assays for diagnosis of infectious diseases. Rev Sci Tech Off Int Epizoot 17: 469-486.
39. Geffen E, Yom-Tov Y (2001) Factors affecting the rates of intraspecific nest parasitism among Anseriformes and Galliformes. Anim Behav 62: 1027-1038. doi:10.1006/anbe.2001.1855.
40. Kreisinger J, Munclinger P, Javuorková V, Albrecht T (2010) Analysis of extrapair paternity and conspecific brood parasitism in mallards Anas platyrhynchos using non-invasive techniques. J Avian Biol 41: 551-557. doi:10.1111/j.1600-048X.2010.05002.x.
41. Denk AG, Gautschi B, Carter K, Kempenaers B (2004) Seven polymorphic microsatellite loci for paternity assessment in the mallard (Anas platyrhynchos). Mol Ecol Notes 4: 506-508. doi:10.1111/j.1471-8286.2004.00707.x.
42. Maak S, Wimmers K, Weigend S, Neumann K (2003) Isolation and characterization of 18 microsatellites in the peking duck (Anas platyrhynchos) and their application in other waterfowl species. Mol Ecol Notes 3: 224-227. doi:10.1046/j.1471-8286.2003.00405.x.
43. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16: 1099-1106. doi:10.1111/j.1365-294X.2007.03089.x.
44. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7: 1071-1075. doi:10.1046/j.1365-294x.1998.00389.x.
45. Boutette JB, Ramsay EC, Potgieter LND, Kania SA (2002) An improved polymerase chain reaction-restriction fragment length polymorphism assay for gender identification in birds. J Avian Med Surg 16: 198-202. doi:10.1647/1082-6742(2002)016[0198:aipcrr]2.0.co;2.
46. Hoyt DF (1979) Practical methods of estimating volume and fresh weight of bird eggs. Auk 96: 73-77.
47. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. 2nd edition. New York: Springer-Verlag. 488 p.
48. R Development Core Team (2012) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
49. Bates D, Maechler M, Bolker B (2012) lme4: linear mixed-effects models using S4 classes. R package version 0.999999-0. http://CRAN.R-project.org/package=lme4.
50. Liu SS, Higgins DA (1990) Yolk-sac transmission and post-hatching ontogeny of serum immunoglobulins in the duck (Anas platyrhynchos). Comp Biochem Physiol B-Biochem Mol Biol 97: 637-644.
51. Ismail A, Jacquin L, Haussy C, Legoupi J, Perret S, et al. (2013) Food availability and maternal immunization affect transfer and persistence of maternal antibodies in nestling pigeons. PLoS One 8: 8. doi:10.1371/journal.pone. 0079942.
52. Gasparini J, Boulinier T, Gill VA, Gil D, Hatch SA, et al. (2007) Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird. J Evol Biol 20: 874-880. doi:10.1111/j.1420-9101.2007.01315.x.
53. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22: 760-772. doi:10.1111/j.1365-2435.2008.01467.x.
54. Jeong OM, Kim MC, Kang HM, Ha GW, Oh JS, et al. (2010) Validation of egg yolk antibody based C-ELISA for avian influenza surveillance in breeder duck. Vet Microbiol 144: 287-292. doi:10.1016/j.vetmic.2010.01.022.
55. Al-Natour MQ, Ward LA, Saif YM, Stewart-Brown B, Keck LD (2004) Effect of different levels of maternally derived antibodies on protection against infectious bursal disease virus. Avian Dis 48: 177-182. doi:10.1637/5319.
56. Otaki Y, Saito K, Tajima M, Nomura Y (1992) Persistence of maternal antibody to chicken anemia agent and its effect on the susceptibility of young chickens. Avian Pathol 21: 147-151. doi:10.1080/03079459208418828.
57. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci U S A 90: 11446-11450. doi:10.1073/pnas.90.24.11446.
58. Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386: 231. doi:10.1038/386231a0.
59. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29: 329-352. doi:10.1016/j.neubiorev.2004.12.002.
60. Cramp S, Simmons KEL (1977) Handbook of the Birds of Europe, the Middle East, and North Africa: The Birds of the Western Palearctic, Vol. 1: Ostrich to Ducks. Oxford: Oxford University Press. 722 p.
61. MacCluskie MC, Flint PL, Sedinger JS (1997) Variation in incubation periods and egg metabolism in mallards: intrinsic mechanisms to promote hatch synchrony. Condor 99: 224-228.
62. Rhymer JM (1988) The effect of egg size variability on thermoregulation of mallard (Anas platyrhynchos) offspring and its implications for survival. Oecologia 75: 20-24. doi:10.1007/bf00378809.
63. Stearns SC (1992) The evolution of life histories. Oxford: Oxford University Press. 262 p.
64. Moreno J, Lobato E, Morales J, Merino S, Martínez-De La Puente J, et al. (2008) Pre-laying nutrition mediates maternal effects on offspring immune capacity and growth in the pied flycatcher. Oecologia 156: 727-735. doi:10.1007/s00442-008-1029-7.
65. Gunnarsson G, Elmberg J, Dessborn L, Jonzén N, Po..ysäH, et al. (2008) Survival estimates, mortality patterns, and population growth of Fennoscandian mallards Anas platyrhynchos. Ann Zool Fenn 45: 483-495. doi:10.5735/086.045.0603.