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Maternal immunization increases nestling energy expenditure, immune function, and fledging success in a passerine bird

Burness, Gary; Moher, Deanna; Ben-Ezra, Noah; Kelly, Ryan J.; Hasselquist, Dennis LU and Chin, Eunice H. (2018) In Biology Open 7(4).
Abstract

Female birds transfer maternally derived antibodies (matAb) to their nestlings, via the egg yolk. These antibodies are thought to provide passive protection, and allow nestlings to avoid the costs associated with mounting an innate immune response. To test whether there is an energetic benefit to nestlings from receiving matAb, we challenged adult female tree swallows (Tachycineta bicolor) prior to clutch initiation with either lipopolysaccharide (LPS) or saline (Control). Following hatching, one half of each female's nestlings were immunized on day 8 post-hatch with LPS or saline, and the 4-h post-immunization nestling metabolic rate (MR) was measured. There was no difference in either LPS-reactive antibodies or total Ig levels between... (More)

Female birds transfer maternally derived antibodies (matAb) to their nestlings, via the egg yolk. These antibodies are thought to provide passive protection, and allow nestlings to avoid the costs associated with mounting an innate immune response. To test whether there is an energetic benefit to nestlings from receiving matAb, we challenged adult female tree swallows (Tachycineta bicolor) prior to clutch initiation with either lipopolysaccharide (LPS) or saline (Control). Following hatching, one half of each female's nestlings were immunized on day 8 post-hatch with LPS or saline, and the 4-h post-immunization nestling metabolic rate (MR) was measured. There was no difference in either LPS-reactive antibodies or total Ig levels between offspring of immunized and non-immunized mothers on day 6 or 14 post-hatch, possibly reflecting a relatively short half-life of matAbs in altricial birds. Additionally, we found no evidence that nestlings from LPS-immunized mothers could avoid the growth suppression that may result from activation of an inflammatory response. Unexpectedly, we found that control nestlings from LPS mothers had higher resting MR than control nestlings of control mothers.We attribute the increasedMR to the costs associated with a general non-specific enhancement of immune function in nestlings from LPS-immunized mothers. Consistent with enhanced immune function, nestlings of immunized mothers had a more robust inflammatory response to phytohaemagglutinin and higher fledging success. Our results suggest that maternal antigen exposure prelaying can result in increased fitness for both mothers and offspring, depending on food availability.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Energetics, Fitness, Growth, Lipopolysaccharide, Maternal antibody transmission, Maternal effects, Mismatch hypothesis
in
Biology Open
volume
7
issue
4
publisher
The Company of Biologists Ltd
external identifiers
  • scopus:85045408574
ISSN
2046-6390
DOI
10.1242/bio.028803
language
English
LU publication?
yes
id
2aa83947-6ca4-483f-b476-d82133dc4ba2
date added to LUP
2018-04-24 14:04:14
date last changed
2019-02-20 11:15:04
@article{2aa83947-6ca4-483f-b476-d82133dc4ba2,
  abstract     = {<p>Female birds transfer maternally derived antibodies (matAb) to their nestlings, via the egg yolk. These antibodies are thought to provide passive protection, and allow nestlings to avoid the costs associated with mounting an innate immune response. To test whether there is an energetic benefit to nestlings from receiving matAb, we challenged adult female tree swallows (Tachycineta bicolor) prior to clutch initiation with either lipopolysaccharide (LPS) or saline (Control). Following hatching, one half of each female's nestlings were immunized on day 8 post-hatch with LPS or saline, and the 4-h post-immunization nestling metabolic rate (MR) was measured. There was no difference in either LPS-reactive antibodies or total Ig levels between offspring of immunized and non-immunized mothers on day 6 or 14 post-hatch, possibly reflecting a relatively short half-life of matAbs in altricial birds. Additionally, we found no evidence that nestlings from LPS-immunized mothers could avoid the growth suppression that may result from activation of an inflammatory response. Unexpectedly, we found that control nestlings from LPS mothers had higher resting MR than control nestlings of control mothers.We attribute the increasedMR to the costs associated with a general non-specific enhancement of immune function in nestlings from LPS-immunized mothers. Consistent with enhanced immune function, nestlings of immunized mothers had a more robust inflammatory response to phytohaemagglutinin and higher fledging success. Our results suggest that maternal antigen exposure prelaying can result in increased fitness for both mothers and offspring, depending on food availability.</p>},
  articleno    = {bio028803},
  author       = {Burness, Gary and Moher, Deanna and Ben-Ezra, Noah and Kelly, Ryan J. and Hasselquist, Dennis and Chin, Eunice H.},
  issn         = {2046-6390},
  keyword      = {Energetics,Fitness,Growth,Lipopolysaccharide,Maternal antibody transmission,Maternal effects,Mismatch hypothesis},
  language     = {eng},
  month        = {01},
  number       = {4},
  publisher    = {The Company of Biologists Ltd},
  series       = {Biology Open},
  title        = {Maternal immunization increases nestling energy expenditure, immune function, and fledging success in a passerine bird},
  url          = {http://dx.doi.org/10.1242/bio.028803},
  volume       = {7},
  year         = {2018},
}