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Behavioral Ecology Advance Access originally published online on March 1, 2007
Behavioral Ecology 2007 18(3):513-520; doi:10.1093/beheco/arm004
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© The Author 2007. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Maternal immune factors and the evolution of secondary sexual characters

Nicola Sainoa, Roberta Martinellia, Clotilde Biardb, Diego Gilc, Claire N. Spottiswooded,e, Diego Rubolinif, Peter F. Suraig and Anders P. Møllerb

a Dipartimento di Biologia, Università degli Studi di Milano, via Celoria 26, I-20133 Milano, Italy b Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, Bâtiment A, 7ème étage, 7 quai Saint Bernard, Case 237, F-75252 Paris Cedex 05, France c Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, José Gutierrez Abascal 2, E-28006 Madrid, Spain d Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK e DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, University of Cape Town, Rondebosch 7701, South Africa f Dipartimento di Biologia Animale, Università di Pavia, piazza Botta 9, I-27100 Pavia, Italy g Avian Science Research Centre, Scottish Agricultural College, Ayrshire KA6 5HW, Scotland

Address correspondence to A. P. Møller. E-mail: anders.moller{at}snv.jussiev.fr.


   Abstract

Secondary sexual characters have been hypothesized to reveal the ability of males to resist debilitating parasites. Although such reliable signaling of parasite resistance may be maintained by parasite–host coevolution, maternal effects potentially provide a previously neglected factor that could affect the level of genetic variation in resistance to parasites. That could be the case because maternal effects have an entirely environmental basis, or because they can maintain considerable amounts of genetic variation through epistatic effects, even in the presence of strong directional selection. Maternal effects have been shown to occur as maternal allocation of immune factors to offspring, and such allocation may depend on the mating prospects of sons, causing mothers to differentially allocate maternal effects to eggs in species subject to intense sexual selection. Here we show that a maternal effect through innate antibacterial immune defense, lysozyme, which is transferred from the mother to the egg in birds, is positively associated with the evolution of secondary sexual characters. Previous studies have shown that females differentially allocate lysozyme to their eggs when mated to attractive males, and elevated levels of lysozyme are associated with reduced hatching failure and superior health among neonates and adults. In this study, comparative analyses of lysozyme from eggs of 85 species of birds showed a strong positive relationship between brightness of male plumage and egg lysozyme, even when controlling for potentially confounding variables. These findings suggest that maternal immune factors may play a role in the evolution of secondary sexual characters.

Key words: birds, comparative analyses, egg, immunity, lysozyme, maternal effects.

Received 21 February 2005; revised 16 January 2007; accepted 17 January 2007.


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