Abstract
Behavioural phenotypes can be highly constrained by interdependent behavioural traits. Studies in different taxa showed that these behavioural phenotypic correlations are not universal within a species and can differ between populations exposed to different environmental pressures. Empirical studies are required to better understand the relative contributions of long-term adaptive processes and direct ontogenetic mechanisms in the development of these phenotypic behavioural correlations. In the present study, we investigated the role of postnatal nurturing care on the development of behavioural correlations in a precocial bird model, the Japanese quail (Coturnix coturnix japonica). We compared phenotypic correlations between two populations: 41 artificially reared birds (maternally deprived) and 36 birds fostered by unrelated females. Behavioural responses were measured at the age when birds naturally disperse, with three widely used behavioural tests to assess fearfulness and sociality: tonic immobility, open-field and emergence tests. Our results show that when quail chicks are reared by a foster mother, more phenotypic correlations appeared in the population including correlations within and across behavioural functions and between behavioural responses and chick mass. In contrast, chicks reared without a foster mother presented much fewer behavioural correlations and those were limited to functionally linked behaviours. Our results also highlight that the effect of mothering on phenotypic correlations is sex-specific, with a greater effect on males. We discuss the organisational role of parents on the development of behavioural correlations, the mechanisms likely to support this influence, as well as the reasons for sexual dimorphism.
Significance statement
Mothers deeply influence the behavioural development of their offspring during the postnatal stage. Whether maternal presence and nurturing behaviour also affect correlations between behavioural responses of their offspring at a population level remains underexplored and unclear. In the current study, we used an adoption procedure to demonstrate the critical role of maternal postnatal care for the development of behavioural correlations in a precocial bird model widely used for the study of behavioural ontogeny: the Japanese quail. Our findings highlight that the presence of a maternally behaving female during early life promotes the development of correlations between behavioural responses both within and across behavioural functions in males but not in females.
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Data availability
The dataset analysed during the current study is available from the corresponding author on reasonable request.
References
Aigueperse N, Houdelier C, Nicolle C, Lumineau S (2019) Mother-chick interactions are affected by chicks’ sex and brood composition in Japanese quail. Dev Psychobiol (published online). https://doi.org/10.1002/dev.21848)
Aigueperse N, Pittet F, Nicolle C, Houdelier C, Lumineau S (2018) Maternal care affects chicks’ development differently according to sex in quail. Dev Psychobiol 60:1048–1056. https://doi.org/10.1002/dev.21597
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723. https://doi.org/10.1109/TAC.1974.1100705
Archer J (1976) The organization of aggression and fear in vertebrates. In: Bateson PPG, Klopfer PH (eds) Perspectives in ethology, 2nd edn. Springer US, Boston, pp 231–298
Barna I, Bálint E, Baranyi J, Bakos N, Makara GB, Haller J (2003) Gender-specific effect of maternal deprivation on anxiety and corticotropin-releasing hormone mRNA expression in rats. Brain Res Bull 62:85–91. https://doi.org/10.1016/S0361-9230(03)00216-8
Beery AK, Francis DD (2011) Adaptive significance of natural variations in maternal care in rats: a translational perspective. Neurosci Biobehav Rev 35:1552–1561. https://doi.org/10.1016/j.neubiorev.2011.03.012
Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473. https://doi.org/10.1111/j.1420-9101.2004.00817.x
Bell AM (2007) Future directions in behavioural syndromes research. Proc R Soc Lond B 274:755–761. https://doi.org/10.1098/rspb.2006.0199
Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783
Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834. https://doi.org/10.1111/j.1461-0248.2007.01081.x
Bell AM, Stamps JA (2004) Development of behavioural differences between individuals and populations of sticklebacks, Gasterosteus aculeatus. Anim Behav 68:1339–1348. https://doi.org/10.1016/j.anbehav.2004.05.007
Bengston SE, Pruitt JN, Riechert SE (2014) Differences in environmental enrichment generate contrasting behavioural syndromes in a basal spider lineage. Anim Behav 93:105–110. https://doi.org/10.1016/j.anbehav.2014.04.022
Bertin A, Richard-Yris M-A (2005) Mothering during early development influences subsequent emotional and social behaviour in Japanese quail. J Exp Zool A 303:792–801. https://doi.org/10.1002/jez.a.202
Boon AK, Réale D, Boutin S (2007) The interaction between personality, offspring fitness and food abundance in north American red squirrels. Ecol Lett 10:1094–1104. https://doi.org/10.1111/j.1461-0248.2007.01106.x
Boulay J, Chaillou E, Bertin A, Constantin P, Arnould C, Leterrier C, Calendreau L (2013) A higher inherent trait for fearfulness is associated with increased anxiety-like behaviours and diazepam sensitivity in Japanese quail. Behav Brain Res 237:124–128. https://doi.org/10.1016/j.bbr.2012.09.026
Brommer JE, Class B (2015) The importance of genotype-by-age interactions for the development of repeatable behavior and correlated behaviors over lifetime. Front Zool 12:S2. https://doi.org/10.1186/1742-9994-12-S1-S2
Budaev SV (1999) Sex differences in the big five personality factors: testing an evolutionary hypothesis. Personal Individ Differ 26:801–813. https://doi.org/10.1016/S0191-8869(98)00179-2
Butler D, Cullis BR, Gilmour AR, Gogel BJ (2009) Asreml: asreml () fits the linear mixed model. R package version 3, https://www.vsni.co.uk/software/asreml-r/. Accessed Feb 2019
Cameron EZ, Linklater WL (2000) Individual mares bias investment in sons and daughters in relation to their condition. Anim Behav 60:359–367. https://doi.org/10.1006/anbe.2000.1480
Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653. https://doi.org/10.1111/j.0030-1299.2008.16513.x
Champagne FA, Francis DD, Mar A, Meaney MJ (2003) Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359–371
Cockrem JF (2007) Stress, corticosterone responses and avian personalities. J Ornithol 148:169–178. https://doi.org/10.1007/s10336-007-0175-8
D’Amore DM, Rios-Cardenas O, Morris MR (2015) Maternal investment influences development of behavioural syndrome in swordtail fish, Xiphophorus multilineatus. Anim Behav 103:147–151. https://doi.org/10.1016/j.anbehav.2015.02.013
Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138. https://doi.org/10.1111/j.1365-2656.2007.01284.x
Dochtermann NA, Dingemanse NJ (2013) Behavioral syndromes as evolutionary constraints. Behav Ecol 24:806–811. https://doi.org/10.1093/beheco/art002
Dufty AM, Clobert J, Møller AP (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190–196. https://doi.org/10.1016/S0169-5347(02)02498-9
Edelaar P, Serrano D, Carrete M, Blas J, Potti J, Tella JL (2012) Tonic immobility is a measure of boldness toward predators: an application of Bayesian structural equation modeling. Behav Ecol 23:619–626. https://doi.org/10.1093/beheco/ars006
Edgar J, Kelland I, Held S, Paul E, Nicol C (2015) Effects of maternal vocalisations on the domestic chick stress response. Appl Anim Behav Sci 171:121–127. https://doi.org/10.1016/j.applanim.2015.08.031
Ezard THG, Côté SD, Pelletier F (2009) Eco-evolutionary dynamics: disentangling phenotypic, environmental and population fluctuations. Philos Trans R Soc B 364:1491–1498. https://doi.org/10.1098/rstb.2009.0006
Fairbanks LA (1996) Individual differences in maternal style: causes and consequences for mothers and offspring. Adv Study Behav 25:579–611
Fält B (1978) Differences in aggressiveness between brooded and non-brooded domestic chicks. Appl Anim Ethol 4:211–221. https://doi.org/10.1016/0304-3762(78)90112-8
Forkman B, Boissy A, Meunier-Salaün M-C, Canali E, Jones RB (2007) A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiol Behav 92:340–374. https://doi.org/10.1016/j.physbeh.2007.03.016
Formanek L, Houdelier C, Lumineau S, Bertin A, Richard-Yris MA (2008) Maternal epigenetic transmission of social motivation in birds. Ethology 114:817–826. https://doi.org/10.1111/j.1439-0310.2008.01536.x
Francis DD, Meaney MJ (1999) Maternal care and the development of stress responses. Curr Opin Neurobiol 9:128–134
Francis DD, Young LJ, Meaney MJ, Insel TR (2002) Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J Neuroendocrinol 14:349–353. https://doi.org/10.1046/j.0007-1331.2002.00776.x
Fresneau N, Kluen E, Brommer JE (2014) A sex-specific behavioral syndrome in a wild passerine. Behav Ecol 25:359–367. https://doi.org/10.1093/beheco/aru008
Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86. https://doi.org/10.1037/0033-2909.127.1.45
Groothuis TGG, Maestripieri D (2013) Parental influences on offspring personality. In: Carere C, Maestripieri D (eds) Animal Personalities. University of Chicago Press, Chicago, pp 317–352
Guenther A, Finkemeier M-A, Trillmich F (2014) The ontogeny of personality in the wild Guinea pig. Anim Behav 90:131–139. https://doi.org/10.1016/j.anbehav.2014.01.032
Guenther A, Trillmich F (2013) Photoperiod influences the behavioral and physiological phenotype during ontogeny. Behav Ecol 24:402–411. https://doi.org/10.1093/beheco/ars177
Gunnar MR (1998) Quality of early care and buffering of neuroendocrine stress reactions: potential effects on the developing human brain. Prev Med 27:208–211. https://doi.org/10.1006/pmed.1998.0276
Guyomarc’h JC, Saint-Jalme M (1986) La reproduction chez la caille des blés (Coturnix c. coturnix). II: Croissance et développement sexuel des jeunes. Gibier Faune Sauvage, 3, 281e295
Han CS, Brooks RC (2013) Correlational selection does not explain the evolution of a behavioural syndrome. J Evol Biol 26:2260–2270. https://doi.org/10.1111/jeb.12223
Harding AMA, Kitaysky AS, Hamer KC, Hall ME, Welcker J, Talbot SL, Karnovsky LJ, Gabrielsen GW, Grémillet D (2009) Impacts of experimentally increased foraging effort on the family: offspring sex matters. Anim Behav 78:321–328. https://doi.org/10.1016/j.anbehav.2009.05.009
Hazard D, Couty M, Richard S, Guémené D (2008) Intensity and duration of corticosterone response to stressful situations in Japanese quail divergently selected for tonic immobility. Gen Comp Endocrinol 155:288–297. https://doi.org/10.1016/j.ygcen.2007.05.009
Herrington J, Vallin C, Lickliter R (2015) Increased yolk progesterone interferes with prenatal auditory learning and elevates emotional reactivity in bobwhite quail (Colinus virginianus) chicks. Dev Psychobiol 57:255–262. https://doi.org/10.1002/dev.21274
Hogg JT, Hass CC, Jenni DA (1992) Sex-biased maternal expenditure in Rocky Mountain bighorn sheep. Behav Ecol Sociobiol 31:243–251. https://doi.org/10.1007/BF00171679
Hope SF, Kennamer RA, Moore IT, Hopkins WA (2018) Incubation temperature influences the behavioral traits of a young precocial bird. J Exp Zool A Ecol Integr Physiol 329:191–202. https://doi.org/10.1002/jez.2176
Houdelier C, Lumineau S, Bertin A, Guibert F, de Margerie C Houdelier, S Lumineau, A Bertin, F Guibert, De Margerie E, Augery M, Richard-Yris MA (2011) Development of fearfulness in birds: genetic factors modulate non-genetic maternal influences. PLoS One 6(1):e14604
Houslay TM, Vierbuchen M, Grimmer AJ, Young AJ, Wilson AJ (2018) Testing the stability of behavioural coping style across stress contexts in the Trinidadian guppy. Funct Ecol 32:424–438. https://doi.org/10.1111/1365-2435.12981
Janczak AM, Pedersen LJ, Bakken M (2003) Aggression, fearfulness and coping styles in female pigs. Appl Anim Behav Sci 81:13–28. https://doi.org/10.1016/S0168-1591(02)00252-6
Jones RB (1986) The tonic immobility reaction of the domestic fowl: a review. World Poultry Sci J 42:82–96. https://doi.org/10.1079/WPS19860008
Jones RB, Mills AD, Faure JM (1991) Genetic and experiential manipulation of fear-related behavior in Japanese quail chicks (Coturnix coturnix japonica). J Comp Psychol 105:15–24
Juraska JM (1984) Sex differences in dendritic response to differential experience in the rat visual cortex. Brain Res 295:27–34. https://doi.org/10.1016/0006-8993(84)90812-6
Kanda LL, Louon L, Straley K (2012) Stability in activity and boldness across time and context in captive Siberian dwarf hamsters. Ethology 118:518–533. https://doi.org/10.1111/j.1439-0310.2012.02038.x
Ketterson ED, Nolan V Jr (1999) Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154:S4–S25. https://doi.org/10.1086/303280
Kooij EE, Kuijpers AH, Schrama JW, van Eerdenburg FJCM, Schouten WGP, Tielen MJM (2002) Can we predict behaviour in pigs?: searching for consistency in behaviour over time and across situations. Appl Anim Behav Sci 75:293–305. https://doi.org/10.1016/S0168-1591(01)00203-9
Koolhaas JM, Korte SM, de Boer SF, Van der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MA, Blokhuis SJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935. https://doi.org/10.1016/S0149-7634(99)00026-3
Laurence A, Houdelier C, Calandreau L, Arnould C, Favreau-Peigné A, Leterrier C, Boissy A, Lumineau S (2015) Environmental enrichment reduces behavioural alterations induced by chronic stress in Japanese quail. Animal 9:331–338. https://doi.org/10.1017/S1751731114002523
Lickliter R, Harshaw C (2010) Canalization and malleability reconsidered: the developmental basis of phenotypic stability and variability. In: Hood KE, Halpern CT, Greenberg G, Lerner RM (eds) Handbook of developmental science, behavior, and genetics. Blackwell Publishing, New York, pp 491–525
Macrì S, Würbel H (2006) Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav 50:667–680. https://doi.org/10.1016/j.yhbeh.2006.06.015
Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963. https://doi.org/10.1111/j.2007.0030-1299.16203.x
McIntosh J, Anisman H, Merali Z (1999) Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Res Dev Brain Res 113:97–106
Mignon-Grasteau S, Roussot O, Delaby C, Faure JM, Mills A, Leterrier C, Guéméné D, Constantin P, Mills M, Lepape G, Beaumont C (2003) Factorial correspondence analysis of fear-related behaviour traits in Japanese quail. Behav Process 61:69–75. https://doi.org/10.1016/S0376-6357(02)00162-6
Mills AD, Crawford LL, Domjan M, Faure JM (1997) The behavior of the japanese or domestic quail Coturnix japonica. Neurosci Biobehav Rev 21:261–281. https://doi.org/10.1016/S0149-7634(96)00028-0
Moore CL, Morelli GA (1979) Mother rats interact differently with male amd female offspring. J Comp Physiol Psychol 93:677–684. https://doi.org/10.1037/h0077599
Moreno E, Pérez-Martínez C, Conde-Porcuna JM (2019) Dispersal of rotifers and cladocerans by waterbirds: seasonal changes and hatching success. Hydrobiologia 834:145–162. https://doi.org/10.1007/s10750-019-3919-6
Morrison KE, Rodgers AB, Morgan CP, Bale TL (2014) Epigenetic mechanisms in pubertal brain maturation. Neuroscience 264:17–24. https://doi.org/10.1016/j.neuroscience.2013.11.014
Nakagawa S, Gillespie DOS, Hatchwell BJ, Burke T (2007) Predictable males and unpredictable females: sex difference in repeatability of parental care in a wild bird population. J Evol Biol 20:1674–1681. https://doi.org/10.1111/j.1420-9101.2007.01403.x
Nakayama S, Sasaki K, Matsumura K, Lewis Z, Miyatake T (2012) Dopaminergic system as the mechanism underlying personality in a beetle. J Insect Physiol 58:750–755. https://doi.org/10.1016/j.jinsphys.2012.02.011
Nephew B, Murgatroyd C (2013) The role of maternal care in shaping CNS function. Neuropeptides 47:371–378. https://doi.org/10.1016/j.npep.2013.10.013
Oomen CA, Girardi CEN, Cahyadi R, Verbeek EC, Krigers H, Joëls M, Lucassen PJ (2009) Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS One 4:e3675. https://doi.org/10.1371/journal.pone.0003675
Orcutt FS Jr, Orcutt AB (1976) Nesting and parental behavior in domestic common quail. Auk 93:135–141
Perré Y, Wauters A-M, Richard-Yris M-A (2002) Influence of mothering on emotional and social reactivity of domestic pullets. Appl Anim Behav Sci 75:133–146. https://doi.org/10.1016/S0168-1591(01)00189-7
Phillips PC, Arnold SJ (1999) Hierarchical comparison of genetic variance-covariance matrices . I Using the Flury hierarchy. Evolution 53:1506–1515. https://doi.org/10.1111/j.1558-5646.1999.tb05414.x
Pittet F (2012) Comportement maternel chez la caille japonaise (Coturnix C. japonica) : caractérisation, facteurs de variation et conséquences sur les jeunes. PhD thesis, Rennes 1
Pittet F, Coignard M, Houdelier C, Richard-Yris MA, Lumineau S (2012) Age affects the expression of maternal care and subsequent behavioural development of offspring in a precocial bird. PLoS One 7:e36835. https://doi.org/10.1371/journal.pone.0036835
Pittet F, Houdelier C, de Margerie E, LeBot O, Richard-Yris MA, Lumineau S (2014a) Maternal styles in a precocial bird. Anim Behav 87:31–37. https://doi.org/10.1016/j.anbehav.2013.10.025
Pittet F, Houdelier C, Lumineau S (2014b) Precocial bird mothers shape sex differences in the behavior of their chicks. J Exp Zool A 321:265–275. https://doi.org/10.1002/jez.1858
Pittet F, Le Bot O, Houdelier C, Richard-Yris MA, Lumineau S (2014c) Motherless quail mothers display impaired maternal behavior and produce more fearful and less socially motivated offspring. Dev Psychobiol 56:622–634. https://doi.org/10.1002/dev.21129
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318. https://doi.org/10.1111/j.1469-185X.2007.00010.x
Richard-Yris M-A (1994) Comportement parental chez les gallinacés : importance du facteur émotivité sur la vitesse d’émergence des réponses parentales : apport du modèle caille japonaise. In: Picard M, Porter JSPR (eds) Comportement et adaptation des animaux domestiques aux contraintes de l’élevage : bases techniques du bien-être animal. INRA Edition, Paris, pp 61–76
Roden C, Wechsler B (1998) A comparison of the behaviour of domestic chicks reared with or without a hen in enriched pens. Appl Anim Behav Sci 55:317–326. https://doi.org/10.1016/S0168-1591(97)00073-7
Schuett W, Tregenza T, Dall SRX (2010) Sexual selection and animal personality. Biol Rev 85:217–246. https://doi.org/10.1111/j.1469-185X.2009.00101.x
Schwagmeyer PL, Mock DW (2003) How consistently are good parents good parents? Repeatability of parental care in the house sparrow, Passer domesticus. Ethology 109:303–313. https://doi.org/10.1046/j.1439-0310.2003.00868.x
Shimmura T, Kamimura E, Azuma T, Kansaku N, Uetake K, Tanaka T (2010) Effect of broody hens on behaviour of chicks. Appl Anim Behav Sci 126:125–133. https://doi.org/10.1016/j.applanim.2010.06.011
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. https://doi.org/10.1016/j.tree.2004.04.009
Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289. https://doi.org/10.1111/j.1461-0248.2011.01731.x
Stamps J, Clark A, Kus B, Arrowood P (1987) The effects of parent and offspring gender on food allocation in budgerigars. Behaviour 101:177–199. https://doi.org/10.1163/156853987X00422
Taylor JH, Mustoe AC, French JA (2014) Behavioral responses to social separation stressor change across development and are dynamically related to HPA activity in marmosets. Am J Primatol 76:239–248. https://doi.org/10.1002/ajp.22228
Toms CN, Echevarria DJ, Jouandot DJ (2010) A methodological review of personality-related studies in fish: focus on the shy-bold axis of behavior. Int J Comp Psychol 23:1–25
Trillmich F, Günther A, Müller C, Reinhold K, Sachser N (2015) New perspectives in behavioural development: adaptive shaping of behaviour over a lifetime? Front Zool 12:S1. https://doi.org/10.1186/1742-9994-12-S1-S1
Urszán TJ, Garamszegi LZ, Nagy G, Hettyey A, Török J, Herczeg G (2015) No personality without experience? A test on Rana dalmatina tadpoles. Ecol Evol 5:5847–5856. https://doi.org/10.1002/ece3.1804
van Hasselt FN, Tieskens JM, Trezza V, Krugers HJ, Vanderschuren LJ, Joëls M (2012) Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats. Physiol Behav 106:701–706. https://doi.org/10.1016/j.physbeh.2011.12.007
van Oers K, de Jong G, van Noordwijk AJ, Kampenaers B, Drent PJ (2005) Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142:1185–1206
van Overveld T, Careau V, Adriaensen F, Matthysen E (2014) Seasonal- and sex-specific correlations between dispersal and exploratory behaviour in the great tit. Oecologia 174:109–120. https://doi.org/10.1007/s00442-013-2762-0
Vos DR (1995) The role of sexual imprinting for sex recognition in zebra finches: a difference between males and females. Anim Behav 50:645–653. https://doi.org/10.1016/0003-3472(95)80126-X
Webster DG, Lanthorn TH, Dewsbury DA, Meyer ME (1981) Tonic immobility and the dorsal immobility response in twelve species of muroid rodents. Behav Neural Biol 31:32–41. https://doi.org/10.1016/S0163-1047(81)91034-7
Wigger A, Neumann ID (1999) Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 66:293–302
Wilson ADM, Krause J (2012) Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol 23:1316–1323. https://doi.org/10.1093/beheco/ars123
Wuerz Y, Krüger O (2015) Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behavioural syndromes. Front Zool 12:S9. https://doi.org/10.1186/1742-9994-12-S1-S9
Acknowledgments
The authors would like to thank Tom Houslay for his critical statistical guidance and coding support. We thank Christophe Petton for his help rearing and maintaining the birds. We are grateful to Pr. Judy Stamps for her very helpful comments at the early stages of this work. We also thank the two anonymous reviewers and the editors whose suggestions helped improve this manuscript.
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All experiments were approved by the departmental direction of veterinary services (Ille et Vilaine, France, Permit number 005283) and were performed in accordance with the European Communities Council Directive of 24 November 1986 (86/609/EEC). Our breeding procedure and tests were approved by the regional ethics committee (agreement number: R-2011-SLU-02).
A particular care was taken to ensure animal welfare in this study. Adult females were transported by car in aluminium crates (70 × 30 cm and 22 cm high), each containing six individual boxes. The temperature was 20 °C during transportation and the journey lasted 20 min. Once at the laboratory, females used as adoptive mothers are routinely housed singly (Bertin and Richard-Yris 2005; Houdelier et al. 2011) because, under natural conditions, they incubate and care for their chicks alone (Guyomarc’h and Saint-Jalme 1986). We did not provide hiding places because we needed to monitor the chicks every day without disturbing the brood. Cages were behind one-way mirrors to limit disturbance, and we checked that the females showed no stereotypies, distress calls or flight attempts, and that they carried out normal comfort behaviours such as dust bathing, which was facilitated by plastic netting covering the cage floor.
We observed no cases of maternal abuse and one case of maternal induction failure resulting in the mother not warming the chicks once out of the induction box. M and NM chicks showing signs of hypothermia were all put under a heater in plastic cages (98 × 35 cm and 42 cm high) where they swiftly recovered (in less than 1 h).
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Pittet, F., Tyson, C., Herrington, J.A. et al. Postnatal care generates phenotypic behavioural correlations in the Japanese quail. Behav Ecol Sociobiol 73, 120 (2019). https://doi.org/10.1007/s00265-019-2735-3
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DOI: https://doi.org/10.1007/s00265-019-2735-3