Abstract

Female birds transfer antibodies to their offspring via the egg yolk, thus possibly providing passive immunity against infectious diseases to which hatchlings may be exposed, thereby affecting their fitness. It is nonetheless unclear whether the amount of maternal antibodies transmitted into egg yolks varies with female quality and egg laying order. In this paper, we investigated the transfer of maternal antibodies against type A influenza viruses (anti-AIV antibodies) by a long-lived colonial seabird, the yellow-legged gull (Larus michahellis), in relation to fluctuating asymmetry in females, i.e. the random deviation from perfect symmetry in bilaterally symmetric morphological and anatomical traits. In particular, we tested whether females with greater asymmetry transmitted fewer antibodies to their eggs, and whether within-clutch variation in yolk antibodies varied according to the maternal level of fluctuating asymmetry. We found that asymmetric females were in worse physical condition, produced fewer antibodies, and transmitted lower amounts of antibodies to their eggs. We also found that, within a given clutch, yolk antibody level decreased with egg laying order, but this laying order effect was more pronounced in clutches laid by the more asymmetric females. Overall, our results support the hypothesis that maternal quality interacts with egg laying order in determining the amount of maternal antibodies transmitted to the yolks. They also highlight the usefulness of fluctuating asymmetry as a sensitive indicator of female quality and immunocompetence in birds.

Highlights

  • Most organisms face a dangerous world, in which parasitic species outnumber host species [1], and vertebrates have evolutionarily responded to this threat by developing a complex immune system in which antibodies provide tailored protection against the particular pathogens encountered

  • More data are needed for firmer conclusions about the association between patterns of maternal antibody transfer and mother fluctuating asymmetry (FA)

  • Both female body condition and plasma antibody level were found to be negatively correlated with the degree of fluctuating asymmetry

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Summary

Introduction

Most organisms face a dangerous world, in which parasitic species outnumber host species [1], and vertebrates have evolutionarily responded to this threat by developing a complex immune system in which antibodies provide tailored protection against the particular pathogens encountered. The capacity to synthesize and transmit antibodies to offspring via egg yolks, which could be related to female quality, may vary among females according to a multitude of factors [2,5,6,7]. Some of these may be proximate factors, such as current female condition and nutritional status, but others may be historical factors that acted during early life stages. Female quality could affect maternal antibody transfer in two ways: through the overall capacity to produce and deposit antibodies and their distribution within the clutch. The quantity of maternal antibodies deposited is known to vary among eggs according to egg laying order, but the directionality of this relationship depends on the reproductive strategy adopted [9,10,11]

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