Differences in the oxidative balance of dispersing and non-dispersing individuals: an experimental approach in a passerine bird

Charlotte Récapet, Alexandre Zahariev, Stéphane Blanc, Mathilde Arrivé, François Criscuolo, Pierre Bize, Blandine Doligez

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Abstract

Background
Dispersal is often associated with a suite of phenotypic traits that might reduce dispersal costs, but can be energetically costly themselves outside dispersal. Hence, dispersing and philopatric individuals might differ throughout their life cycle in their management of energy production. Because higher energy expenditure can lead to the production of highly reactive oxidative molecules that are deleterious to the organism if left uncontrolled, dispersing and philopatric individuals might differ in their management of oxidative balance. Here, we experimentally increased flight costs during reproduction via a wing load manipulation in female collared flycatchers (Ficedula albicollis) breeding in a patchy population. We measured the effects of the manipulation on plasmatic markers of oxidative balance and reproductive success in dispersing and philopatric females.

Results
The impact of the wing load manipulation on the oxidative balance differed according to dispersal status. The concentration of reactive oxygen metabolites (ROMs), a marker of pro-oxidant status, was higher in philopatric than dispersing females in the manipulated group only. Differences between dispersing and philopatric individuals also depended on habitat quality, as measured by local breeding density. In low quality habitats, ROMs as well as nestling body mass were higher in philopatric females compared to dispersing ones. Independently of the manipulation or of habitat quality, plasma antioxidant capacity differed according to dispersal status: philopatric females showed higher antioxidant capacity than dispersing ones. Nestlings raised by philopatric females also had a higher fledging success.

Conclusions
Our results suggest that dispersing individuals maintain a stable oxidative balance when facing challenging environmental conditions, at the cost of lower reproductive success. Conversely, philopatric individuals increase their effort, and thus oxidative costs, in challenging conditions thereby maintaining their reproductive success. Our study sheds light on energetics and oxidative balance as possible processes underlying phenotypic differences between dispersing and philopatric individuals.
Original languageEnglish
Article number125
JournalBMC Evolutionary Biology
Volume16
DOIs
Publication statusPublished - 14 Jun 2016

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passerine
bird
birds
habitat quality
reproductive success
nestling
antioxidant
reactive oxygen species
metabolite
habitats
breeding
cost
antioxidants
oxygen
fledging
oxidants
oxidant
energy expenditure
body mass
expenditure

Keywords

  • dispersal
  • energetic constraint
  • breeding density
  • doubly-labeled water
  • reactive oxygen metabolites
  • antioxidant defences
  • oxidative stress
  • reprodutive outlet
  • Ficedula albicollis

Cite this

Differences in the oxidative balance of dispersing and non-dispersing individuals : an experimental approach in a passerine bird. / Récapet, Charlotte; Zahariev, Alexandre; Blanc, Stéphane; Arrivé, Mathilde; Criscuolo, François; Bize, Pierre; Doligez, Blandine.

In: BMC Evolutionary Biology, Vol. 16, 125, 14.06.2016.

Research output: Contribution to journalArticle

Récapet, Charlotte ; Zahariev, Alexandre ; Blanc, Stéphane ; Arrivé, Mathilde ; Criscuolo, François ; Bize, Pierre ; Doligez, Blandine. / Differences in the oxidative balance of dispersing and non-dispersing individuals : an experimental approach in a passerine bird. In: BMC Evolutionary Biology. 2016 ; Vol. 16.
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abstract = "BackgroundDispersal is often associated with a suite of phenotypic traits that might reduce dispersal costs, but can be energetically costly themselves outside dispersal. Hence, dispersing and philopatric individuals might differ throughout their life cycle in their management of energy production. Because higher energy expenditure can lead to the production of highly reactive oxidative molecules that are deleterious to the organism if left uncontrolled, dispersing and philopatric individuals might differ in their management of oxidative balance. Here, we experimentally increased flight costs during reproduction via a wing load manipulation in female collared flycatchers (Ficedula albicollis) breeding in a patchy population. We measured the effects of the manipulation on plasmatic markers of oxidative balance and reproductive success in dispersing and philopatric females.ResultsThe impact of the wing load manipulation on the oxidative balance differed according to dispersal status. The concentration of reactive oxygen metabolites (ROMs), a marker of pro-oxidant status, was higher in philopatric than dispersing females in the manipulated group only. Differences between dispersing and philopatric individuals also depended on habitat quality, as measured by local breeding density. In low quality habitats, ROMs as well as nestling body mass were higher in philopatric females compared to dispersing ones. Independently of the manipulation or of habitat quality, plasma antioxidant capacity differed according to dispersal status: philopatric females showed higher antioxidant capacity than dispersing ones. Nestlings raised by philopatric females also had a higher fledging success.ConclusionsOur results suggest that dispersing individuals maintain a stable oxidative balance when facing challenging environmental conditions, at the cost of lower reproductive success. Conversely, philopatric individuals increase their effort, and thus oxidative costs, in challenging conditions thereby maintaining their reproductive success. Our study sheds light on energetics and oxidative balance as possible processes underlying phenotypic differences between dispersing and philopatric individuals.",
keywords = "dispersal, energetic constraint, breeding density, doubly-labeled water, reactive oxygen metabolites, antioxidant defences, oxidative stress, reprodutive outlet, Ficedula albicollis",
author = "Charlotte R{\'e}capet and Alexandre Zahariev and St{\'e}phane Blanc and Mathilde Arriv{\'e} and Fran{\cc}ois Criscuolo and Pierre Bize and Blandine Doligez",
note = "Funding This work was supported by grants from the French Ministry of Research (PhD fellowship to CR), the University of Aberdeen (stipend to CR), the CNRS (PICS grant to BD), the L’Or{\'e}al Foundation-UNESCO “For Women in Science” program (fellowship to CR), the R{\'e}gion Rh{\^o}ne-Alpes (student mobility grant CMIRA Explora’doc to CR), the Rectors’ Conference of the Swiss Universities (mobility grant to CR), the F{\'e}d{\'e}ration de Recherche 41 BioEnvironnement et Sant{\'e} (training grant to CR), and the Journal of Experimental Biology (travel grant to CR).",
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T1 - Differences in the oxidative balance of dispersing and non-dispersing individuals

T2 - an experimental approach in a passerine bird

AU - Récapet, Charlotte

AU - Zahariev, Alexandre

AU - Blanc, Stéphane

AU - Arrivé, Mathilde

AU - Criscuolo, François

AU - Bize, Pierre

AU - Doligez, Blandine

N1 - Funding This work was supported by grants from the French Ministry of Research (PhD fellowship to CR), the University of Aberdeen (stipend to CR), the CNRS (PICS grant to BD), the L’Oréal Foundation-UNESCO “For Women in Science” program (fellowship to CR), the Région Rhône-Alpes (student mobility grant CMIRA Explora’doc to CR), the Rectors’ Conference of the Swiss Universities (mobility grant to CR), the Fédération de Recherche 41 BioEnvironnement et Santé (training grant to CR), and the Journal of Experimental Biology (travel grant to CR).

PY - 2016/6/14

Y1 - 2016/6/14

N2 - BackgroundDispersal is often associated with a suite of phenotypic traits that might reduce dispersal costs, but can be energetically costly themselves outside dispersal. Hence, dispersing and philopatric individuals might differ throughout their life cycle in their management of energy production. Because higher energy expenditure can lead to the production of highly reactive oxidative molecules that are deleterious to the organism if left uncontrolled, dispersing and philopatric individuals might differ in their management of oxidative balance. Here, we experimentally increased flight costs during reproduction via a wing load manipulation in female collared flycatchers (Ficedula albicollis) breeding in a patchy population. We measured the effects of the manipulation on plasmatic markers of oxidative balance and reproductive success in dispersing and philopatric females.ResultsThe impact of the wing load manipulation on the oxidative balance differed according to dispersal status. The concentration of reactive oxygen metabolites (ROMs), a marker of pro-oxidant status, was higher in philopatric than dispersing females in the manipulated group only. Differences between dispersing and philopatric individuals also depended on habitat quality, as measured by local breeding density. In low quality habitats, ROMs as well as nestling body mass were higher in philopatric females compared to dispersing ones. Independently of the manipulation or of habitat quality, plasma antioxidant capacity differed according to dispersal status: philopatric females showed higher antioxidant capacity than dispersing ones. Nestlings raised by philopatric females also had a higher fledging success.ConclusionsOur results suggest that dispersing individuals maintain a stable oxidative balance when facing challenging environmental conditions, at the cost of lower reproductive success. Conversely, philopatric individuals increase their effort, and thus oxidative costs, in challenging conditions thereby maintaining their reproductive success. Our study sheds light on energetics and oxidative balance as possible processes underlying phenotypic differences between dispersing and philopatric individuals.

AB - BackgroundDispersal is often associated with a suite of phenotypic traits that might reduce dispersal costs, but can be energetically costly themselves outside dispersal. Hence, dispersing and philopatric individuals might differ throughout their life cycle in their management of energy production. Because higher energy expenditure can lead to the production of highly reactive oxidative molecules that are deleterious to the organism if left uncontrolled, dispersing and philopatric individuals might differ in their management of oxidative balance. Here, we experimentally increased flight costs during reproduction via a wing load manipulation in female collared flycatchers (Ficedula albicollis) breeding in a patchy population. We measured the effects of the manipulation on plasmatic markers of oxidative balance and reproductive success in dispersing and philopatric females.ResultsThe impact of the wing load manipulation on the oxidative balance differed according to dispersal status. The concentration of reactive oxygen metabolites (ROMs), a marker of pro-oxidant status, was higher in philopatric than dispersing females in the manipulated group only. Differences between dispersing and philopatric individuals also depended on habitat quality, as measured by local breeding density. In low quality habitats, ROMs as well as nestling body mass were higher in philopatric females compared to dispersing ones. Independently of the manipulation or of habitat quality, plasma antioxidant capacity differed according to dispersal status: philopatric females showed higher antioxidant capacity than dispersing ones. Nestlings raised by philopatric females also had a higher fledging success.ConclusionsOur results suggest that dispersing individuals maintain a stable oxidative balance when facing challenging environmental conditions, at the cost of lower reproductive success. Conversely, philopatric individuals increase their effort, and thus oxidative costs, in challenging conditions thereby maintaining their reproductive success. Our study sheds light on energetics and oxidative balance as possible processes underlying phenotypic differences between dispersing and philopatric individuals.

KW - dispersal

KW - energetic constraint

KW - breeding density

KW - doubly-labeled water

KW - reactive oxygen metabolites

KW - antioxidant defences

KW - oxidative stress

KW - reprodutive outlet

KW - Ficedula albicollis

U2 - 10.1186/s12862-016-0697-x

DO - 10.1186/s12862-016-0697-x

M3 - Article

VL - 16

JO - BMC Evolutionary Biology

JF - BMC Evolutionary Biology

SN - 1471-2148

M1 - 125

ER -