Abstract
The transfer of maternal antibodies is a critical mechanism for the early life survival of vertebrate newborns. In mammals, passive transfer of immune compounds can occur prenatally through the placenta and postnatally through the consumption of colostrum and milk. In social mammals, it has been hypothesized that allosuckling may be a way for pups to broaden and strengthen their passive access to antibodies after birth, but empirical evidence for this mechanism is still lacking. In order to investigate the potential for the occurrence of a cross-transfer of antibodies between pups exposed to several females, we bred in a common environment groups of two females Mongolian gerbils (Meriones unguiculatus), each previously injected with a different vaccine. Here we report the dynamics of passively acquired specific antibodies in the serum of newborns, showing that pups acquired antibodies from both females of a group. Our result provides the first experimental evidence of a cross-transfer between litters of passively acquired antibodies. We discuss how such evidence opens perspectives for exploring the potential importance of horizontal transfer of immunity in natural host-parasite systems and how this could be used as a tool to answer important behavioral ecology questions.
References
Baintner, K., 2007. Transmission of antibodies from mother to young: evolutionary strategies in a proteolytic environment, Vet. Immunol. Immunopathol. 117, 153–161.
Boulinier, T., Staszewski, V., 2008. Maternal transfer of antibodies: raising immuno-ecology issues, Trends Ecol. Evol. 23, 282–288.
Brambell, F.W.R., 1970. The Transmission of Passive Immunity from Mother to Young. American Elsevier Publishing Company, New York, USA.
Cant, M., 2000. Social control of reproduction in banded mongooses, Anim. Behav. 59, 147–158.
Cant, M.A., Hodge, S.J., Vell, M.B.V., Gilchrist, J.S., Nichols, H.J., 2010. Reproductive control via eviction (but not the threat of eviction) in banded mongooses, Proc. R. Soc. Lond. B: Biol. Sci. 277, 2219–2226.
Chucri, T.M., Monteiro, J.M., Lima, A.R., Salvadori, M.L.B., Kfoury Jr., J.R., Miglino, M.A., 2010. A review of immune transfer by the placenta, J. Reprod. Immunol. 87, 14–20.
Clutton-Brock, T.H., Brotherton, P.N.M., Russell, A.F., O’Riain, M.J., Gaynor, D., Kansky, R., Griffin, A., Manser, M., Sharpe, L., McIlrath, G.M., Small, T., Moss, A., Monfort, S., 2001. Cooperation, control, and concession in meerkat groups, Science 291, 478–481.
Cohas, A., Allainé, D., 2009. Social structure influences extra-pair paternity in socially monogamous mammals, Biol. Lett. 5, 313–316.
Elwood, R.W., 1991. Ethical implications of studies on infanticide and maternal aggression in rodents, Anim. Behav. 42, 841–849.
Frank, S.A., 2002. Immunology and Evolution of Infectious Disease. Princeton University Press, Princeton, NJ, 348 pp.
French, J.A., 1994. Alloparents in the Mongolian gerbil – impact on long-term reproductive performance of breeders and opportunities for independent reproduction, Behav. Ecol. 5, 273–279.
Gilchrist, J.S., 2006. Female eviction, abortion, and infanticide in banded mongooses (Mungos mungo): implications for social control of reproduction and synchronized parturition, Behav. Ecol. 17, 664–669.
Grenfell, B.T., Dobson, A.P., 1995. Ecology of Infectious Diseases in Natural Populations. Cambridge University Press, Cambridge, UK, 521 pp.
Grindstaff, J.L., Brodie III, E.D., Ketterson, E.D., 2003. Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission, Proc. R. Soc. Lond. B: Biol. Sci. 270, 2309–2319.
Gustafsson, E., Mattsson, A., Holmdahl, R., Mattsson, R., 1994. Pregnancy in B-Cell-deficient mice - postpartum transfer of immunoglobulins prevents neonatal runting and death, Biol. Reprod. 51, 1173–1180.
Halliday, R., 1955. Prenatal and postnatal transmission of passive immunity to young rats, Proc. R. Soc. Lond. B: Biol. Sci. 144, 427–430.
Halliday, R., 1978. Variation in immunoglobulin transfer from ewes to lambs, Ann. Rech. Vet. 9, 367–374.
Lindström, J., 1999. Early development and fitness in birds and mammals, Trends Ecol. Evol. 14, 343–348.
Morshed, M.G., Yokota, M., Nakazawa, T., Konishi, H., 1993. Transfer of antibody against Borrelia duttonii from motherto young in Ddy mice, Infect. Immun. 61, 4147–4152.
National Research Council, 2011. Guide for the Care and Use of Laboratory Animals, 8th edition. The National Academies Press, Washington, USA.
Norris, M.L., Adams, C.E., 1972. Mortality form birth to weaning in the Mongolian gerbil Meriones unguiculatus. Lab, Anim. 6, 49–53.
Packer, C, Lewis, S., Pusey, A., 1992. A comparative analysis of non-offspring nursing, Anim. Behav. 43, 265–281.
Pastoret, P.P., 1998. Handbook of Vertebrate Immunology. Academic Press Limited, London, UK.
Roopenian, D.C., Akilesh, S., 2007. FcRn: the neonatal Fc receptor comes of age, Nat. Rev. Immunol. 7, 715–725.
Roulin, A., 2002. Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence, Anim. Behav. 63, 201–208.
Roulin, A., Heeb, P., 1999. The immunological function of allosuckling, Ecol. Lett. 2, 319–324.
Sadeharju, K., Knip, M., Virtanen, S.M., Savilahti, E., Tauriainen, S., Koskela, P., Åkerblom, H.K., Hyöty, H., Finish TRIGR Study Group, 2007. Maternal antibodies in breast milk protect the child from enterovirus infections, Pediatrics 119, 941–946.
Staszewski, V., Boulinier, T., 2004. Vaccination: a way to address questions in behavioral and population ecology? Trends Parasitol. 20, 17–22.
Tompkins, D.M., Dobson, A.P., Arneberg, P., Begon, M.E., Cattadori, I.M., Green-man, J.V., Heesterbeek, J.A.P., Hudson, P.J., Newborn, D., Pugliese, A., Rizzoli, A.P., Rosà, R., Rosso, F., Wilson, K., 2002. Parasites and host population dynamics. In: Hudson, P.J., Rizzoli, A., Grenfell, B.T., Heesterbeek, H., Dobson, A.P. (Eds.), The Ecology of Wildlife Diseases. Oxford University Press, Oxford, UK, pp. 45–62.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Garnier, R., Gandon, S., Chaval, Y. et al. Evidence of cross-transfer of maternal antibodies through allosuckling in a mammal: Potential importance for behavioral ecology. Mamm Biol 78, 361–364 (2013). https://doi.org/10.1016/j.mambio.2012.11.004
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.mambio.2012.11.004