Behavioural stress response and melanin-based plumage colouration in barn swallow nestlings

in Behaviour
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Consistent and correlated inter-individual differences in behaviours, the so-called ‘personalities’, have been identified in many vertebrates. The ability to respond to stressful events is part of personalities and can have important fitness consequences, as it determines how individuals cope with environmental challenges. As a consequence of pleiotropic effects of genes involved in several functions, inter-individual differences in behavioural responses can be associated with phenotypic traits, like melanin-based plumage colouration in birds. We examined the association between three proxies of the behavioural stress response and breast plumage colouration in barn swallow (Hirundo rustica) nestlings. We found that nestling behavioural responses were consistent within individuals and similar among siblings, thus suggesting that these behaviours may contribute to define individual ‘personalities’. However, nestling behavioural stress response was not significantly predicted by variation in breast plumage colouration, indicating that in juveniles of this species melanin-based colouration does not convey to conspecifics reliable information on individual ability to cope with stressful events.

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References

AlmasiB.RoulinA.Jenni-EiermannS.JenniL. (2008). Parental investment and its sensitivity to corticosterone is linked to melanin-based colouration in barn owls. — Horm. Behav. 54: 217-223.

AlmasiB.JenniL.Jenni-EiermannS.RoulinA. (2010). Regulation of stress response is heritable and functionally linked to melanin-based colouration. — J. Evol. Biol. 23: 987-996.

AlmasiB.RoulinA.Korner-NievergeltF.Jenni-EiermannS.JenniL. (2012). Colouration signals the ability to cope with elevated stress hormones: effects of corticosterone on growth of barn owls are associated with melanism. — J. Evol. Biol. 25: 1189-1199.

AmbrosiniR.BolzernA.M.CanovaL.ArieniS.MøllerA.P.SainoN. (2002). The distribution and colony size of barn swallows in relation to agricultural land use. — J. Appl. Ecol. 39: 524-534.

BellA.M. (2007). Evolutionary biology: animal personalities. — Nature 447: 539-540.

BellA.M.SihA. (2007). Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). — Ecol. Lett. 10: 828-834.

BellA.M.HankisonS.J.LaskowskiK.L. (2009). The repeatability of behaviour: a meta-analysis. — Anim. Behav. 77: 771-783.

BoissyA. (1995). Fear and fearfulness in animals. — Q. Rev. Biol. 70: 165-191.

BrommerJ.E.KluenE. (2012). Exploring the genetics of nestling personality traits in a wild passerine bird: testing the phenotypic gambit. — Ecol. Evol. 2: 3032-3044.

CarereC.van OersK. (2004). Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress. — Physiol. Behav. 82: 905-912.

CarereC.CaramaschiD.FawcettT.W. (2010). Covariation between personalities and individual differences in coping with stress: converging evidence and hypotheses. — Curr. Zool. 56: 728-740.

CharmandariE.TsigosC.ChrousosG. (2005). Endocrinology of the stress response 1. — Annu. Rev. Physiol. 67: 259-284.

CockremJ.F. (2007). Stress, corticosterone responses and avian personalities. — J. Ornithol. 148: 169-178.

CohenJ. (1988). Statistical power analysis for the behavioral sciences, 2nd edn.Erlbaum, Hillsdale, NJ.

CoppensC.M.de BoerS.F.KoolhaasJ.M. (2010). Coping styles and behavioural flexibility: towards underlying mechanisms. — Philos. Trans. Roy. Soc. Lond. B: Biol. Sci. 365: 4021-4028.

CostanzoA.ParoliniM.BazziG.KhoriauliL.SantagostinoM.PossentiC.D.RomanoA.SolomonG.N.RuboliniD.GiulottoE.SainoN. (2016). Brood size, telomere length, and parent-offspring color signaling in barn swallows. — Behav. Ecol. 28: 204-211.

DingemanseN.J.RéaleD. (2005). Natural selection and animal personality. — Behaviour 142: 1159-1184.

DingemanseN.J.BothC.DrentP.J.van OersK.van NoordwijkA.J. (2002). Repeatability and heritability of exploratory behaviour in great tits from the wild. — Anim. Behav. 64: 929-938.

DingemanseN.J.BothC.DrentP.J.TinbergenJ.M. (2004). Fitness consequences of avian personalities in a fluctuating environment. — Proc. Roy. Soc. Lond. B: Biol. Sci. 271: 847-852.

DucrestA.L.KellerL.RoulinA. (2008). Pleiotropy in the melanocortin system, colouration and behavioural syndromes. — Trends. Ecol. Evol. 23: 502-510.

FerrariR.P.MartinelliR.SainoN. (2006). Differential effect of egg albumen content on barn swallow nestlings in relation to hatch order. — J. Evol. Biol. 19: 981-993.

FucikovaE.DrentP.J.SmitsN.van OersK. (2009). Handling stress as a measurement of personality in great tit nestlings (Parus major). — Ethology 115: 366-374.

GoldsmithT.H. (1990). Optimization, constraint, and history in the evolution of eyes. — Q. Rev. Biol. 65: 281-322.

GriffithsR.DoubleM.C.OrrK.DawsonR.J. (1998). A DNA test to sex most birds. — Mol. Ecol. 7: 1071-1075.

HaaseE.ItoS.SellA.WakamatsuK. (1992). Melanin concentrations in feathers from wild and domestic pigeons. — J. Hered. 83: 64-67.

HearingV.J. (1998). The regulation of melanin production. — In: The pigmentary system: physiology and pathophysiology ( NordlundJ.J.BoissyR.HearingV.J.KingR.A.OrtonneJ.P., eds). Oxford University Press, New York, NY, p.  423-438.

HubbardJ.K.JenkinsB.R.SafranR.J. (2015). Quantitative genetics of plumage color: lifetime effects of early nest environment on a colorful sexual signal. — Ecol. Evol. 5: 3436-3449.

ItoS.WakamatsuK.OzekiH. (2000). Chemical analysis of melanins and its application to the study of the regulation of melanogenesis. — Pigment. Cell. Res. 13: 103-109.

JaworJ.M.BreitwischR. (2003). Melanin ornaments, honesty, and sexual selection. — Auk. 120: 249-265.

JenkinsB.R.VitousekM.N.SafranR.J. (2013). Signaling stress? An analysis of phaeomelanin-based plumage color and individual corticosterone levels at two temporal scales in North American barn swallows, Hirundo rustica erythrogaster. — Horm. Behav. 64: 665-672.

JenniL.WinklerR. (1989). The feather-length of small passerines: a measurement for wing-length in live birds and museum skins. — Bird Stud. 36: 1-15.

JonesR.B. (1986). The tonic immobility reaction of the domestic fowl: a review. — World. Poult. Sci. J. 41: 82-96.

JonesR.B.FaureJ.M. (1981). Sex and strain comparisons of tonic immobility (‘righting time’) in the domestic fowl and the effects of various methods of induction. — Behav. Process. 6: 47-55.

KluenE.SiitariH.BrommerJ.E. (2014). Testing for between individual correlations of personality and physiological traits in a wild bird. — Behav. Ecol. Sociobiol. 68: 205-213.

KoolhaasJ.M.KorteS.M.De BoerS.F.Van Der VegtB.J.Van ReenenC.G.HopsterH.De JongI.C.RuisM.A.W.BlokhuisH.J. (1999). Coping styles in animals: current status in behavior and stress-physiology. — Neurosci. Biobehav. Rev. 23: 925-935.

KoolhaasJ.M.De BoerS.F.CoppensC.M.BuwaldaB. (2010). Neuroendocrinology of coping styles: towards understanding the biology of individual variation. — Front. Neuroendocrinol. 31: 307-321.

LessellsC.M.BoagP.T. (1987). Unrepeatable repeatabilities: a common mistake. — Auk 104: 116-121.

MajerusM.E.N. (1998). Melanism, evolution in action. — Oxford University Press, Oxford.

MarkóG.AzcárateM.HegyiG.HercegG.LacziM.NagyG.SeñarJ.C.TörökJ.GaramszegiL.Z. (2013). Behavioural responses to handling stress in the Great Tit: within-individual consistency and the effect of age, sex and body condition. — Ornis Hungarica. 21: 12-25.

McGrawK.J. (2006). Mechanics of carotenoid-based colouration. — In: Bird colouration, volume I, mechanisms and measurements ( HillG.E.McGrawK.J., eds). Harvard University Press, Cambridge, MA, p.  177-242.

McGrawK.J.WakamatsuK.ItoS.NolanP.M.JouventinP.DobsonF.S.AusticR.E.SafranR.J.SieffermanL.M.HillG.H.ParkerR.S. (2004). You can’t judge a pigment by its color: carotenoid and melanin content of yellow and brown feathers in swallows, bluebirds, penguins, and domestic chickens. — Condor 106: 390-395.

McGrawK.J.SafranR.J.WakamatsuK. (2005). How feather colour reflects its melanin content. — Funct. Ecol. 19: 816-821.

MøllerA.P. (1994). Sexual selection and the barn swallow. — Oxford University Press, Oxford.

PelegO.CharterM.LeshemY.IzhakiI.RoulinA. (2014). Conditional association between melanism and personality in Israeli Barn Owls. — Bird Stud. 61: 572-577.

ProtaG. (1992). Melanins and melanogenesis. — Academic Press, New York, NY.

QuesadaJ.SenarJ.C. (2007). The role of melanin- and carotenoid-based plumage colouration in nest defence in the Great Tit. — Ethology 113: 640-647.

RaccaS.SpaccamiglioA.EsculapioP.AbbadessaG.CangemiL.DiCarloF.PortaleoneP. (2005). Effects of swim stress and α-MSH acute pre-treatment on brain 5-HT transporter and corticosterone receptor. — Pharmacol. Biochem. Behav. 81: 894-900.

RéaleD.GallantB.Y.LeblancM.Festa-BianchetM. (2000). Consistency of temperament in bighorn ewes and correlates with behaviour and life history. — Anim. Behav. 60: 589-597.

RéaleD.ReaderS.M.SolD.McDougallP.T.DingemanseN.J. (2007). Integrating animal temperament within ecology and evolution. — Biol. Rev. 82: 291-318.

RomanoA.RomanoM.CaprioliM.CostanzoA.ParoliniM.RuboliniD.SainoN. (2015). Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica). — J. Evol. Biol. 28: 1234-1247.

RomanoA.BazziG.CaprioliM.CortiM.CostanzoA.RuboliniD.SainoN. (2016). Nestling sex and plumage color predict food allocation by barn swallow parents. — Behav. Ecol. 27: 1198-1205.

RomanoA.CostanzoA.RuboliniD.SainoN.MøllerA.P. (2017). Geographical and seasonal variation in the intensity of sexual selection in the barn swallow Hirundo rustica: a meta-analysis. — Biol. Rev. 92: 1582-1600.

RoulinA.BizeP.RavussinP.A.BrochL. (2004). Genetic and environmental effects on the covariation between colour polymorphism and a life-history trait. — Evol. Ecol. Res. 6: 1253-1260.

RoulinA.AlmasiB.Rossi-PedruzziA.DucrestA.L.WakamatsuK.MiksikI.BlountJ.D.Jenni-EiermannS.JenniL. (2008). Corticosterone mediates the condition-dependent component of melanin-based colouration. — Anim. Behav. 75: 1351-1358.

SafranR.J.NeumanC.R.McGrawK.J.LovetteI.J. (2005). Dynamic paternity allocation as a function of male plumage color in barn swallows. — Science. 309: 2210-2212.

SainoN.CalzaS.NinniP.MøllerA.P. (1999). Barn swallows trade survival against offspring condition and immunocompetence. — J. Anim. Ecol. 68: 999-1009.

SainoN.MartinelliR.RomanoM. (2008). Ecological and phenological covariates of offspring sex ratio in barn swallows. — Evol. Ecol. 22: 659-674.

SainoN.RomanoM.RuboliniD.TeplitskyC.AmbrosiniR.CaprioliM.CanovaL.WakamatsuK. (2013a). Sexual dimorphism in melanin pigmentation, feather colouration and its heritability in the barn swallow (Hirundo rustica). — PLoS ONE 8: e58024.

SainoN.CanovaL.CostanzoA.RuboliniD.RoulinA.MøllerA.P. (2013b). Immune and stress responses covary with melanin-based colouration in the barn swallow. — Evol. Biol. 40: 521-531.

SainoN.RomanoM.RuboliniD.AmbrosiniR.CaprioliM.MilzaniA.CostanzoA.ColomboG.CanovaL.WakamatsuK. (2013c). Viability is associated with melanin-based colouration in the barn swallow (Hirundo rustica). — PLoS ONE 8: e60426.

SainoN.RomanoM.ScandolaraC.RuboliniD.AmbrosiniR.CaprioliM.CostanzoA.RomanoA. (2014). Brownish, small and lousy barn swallows have greater natal dispersal propensity. — Anim. Behav. 87: 137-146.

SAS Institute (2006). The GLIMMIX procedure. — SAS Institute, Cary, NC.

SchielzethH.StoffelM.NakagawaS. (2017). rptR: Repeatability Estimation for Gaussian and Non-Gaussian Data. — R package version 0.9.1, available online at https://CRAN.R-project.org/package=rptR.

ScordatoE.S.SafranR.J. (2014). Geographic variation in sexual selection and implications for speciation in the Barn Swallow. — Avian Research 5: 8.

SearcyW.A.PetersS.NowickiS. (2004). Effects of early nutrition on growth rate and adult size in song sparrows Melospiza melodia. — J. Avian Biol. 35: 269-279.

SihA.BellA.JohnsonJ.C. (2004). Behavioral syndromes: an ecological and evolutionary overview. — Trends. Ecol. Evol. 19: 372-378.

SihA.CoteJ.EvansM.FogartyS.PruittJ. (2012). Ecological implications of behavioural syndromes. — Ecol. Lett. 15: 278-289.

SimonJ.D.PelesD.WakamatsuK.ItoS. (2009). Current challenges in understanding melanogenesis: bridging chemistry, biological control, morphology, and function. — Pigment Cell. Mel. Res. 22: 563-579.

StoddardM.C.PrumR.O. (2008). Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. — Am. Nat. 171: 755-776.

TordaG.LikerA.BartaZ. (2004). Dominance hierarchy and status signalling in captive tree sparrow (Passer montanus) flocks. — Acta Zool. Acad. Sci. Hung. 50: 35-44.

Van de PolM.WrightJ. (2009). A simple method for distinguishing within- versus between-subject effects using mixed models. — Anim. Behav. 77: 753-758.

van den BrinkV.DolivoV.FalourdX.DreissA.N.RoulinA. (2012). Melanic color-dependent antipredator behavior strategies in barn owl nestlings. — Behav. Ecol. 23: 473-480.

van OersK.de JongG.van NoordwijkA.KempenaersB.DrentP.J. (2005). Contribution of genetics to the study of animal personalities: a review of case studies. — Behaviour 142: 1185-1206.

WestP.M.PackerC. (2002). Sexual selection, temperature, and the lion’s mane. — Science 297: 1339-1343.

WhittinghamM.J.StephensP.A.BradburyR.B.FreckletonR.P. (2006). Why do we still use stepwise modelling in ecology and behaviour?. — J. Anim. Ecol. 75: 1182-1189.

WolfM.WeissingF.J. (2012). Animal personalities: consequences for ecology and evolution. — Trends Ecol. Evol. 27: 452-461.

XiaoE.Xia-ZhangL.VulliémozN.R.FerinM.WardlawS.L. (2003). Agouti-related protein stimulates the hypothalamic-pituitary-adrenal (HPA) axis and enhances the HPA response to interleukin-1 in the primate. — Endocrinology 144: 1736-1741.

Figures

  • Scatterplots of individual-level (below diagonal) and brood-level (mean value within-brood,above diagonal) correlations of the three behaviors used as proxies of the behavioral stress response: tonic immobility (0, no response within 45 s; 1, response within 45 s), breath rate and agitation (number of leg movements). Pearson’s r values are reported within each scatterplot.

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  • Variation in nestling tonic immobility (0, no response within 45 s; 1, response within 45 s), breath rate and agitation (number of leg movements) according to θ. θ values are centered within brood; positive θDEV values indicate nestlings that have larger θ compared to the brood mean.

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  • Histogram showing the distribution of nestling time of reaction during tonic immobility test (N=188).

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