Abstract
The developmental environment has strong and pervasive effects on animal phenotype. Exposure to stress during development (in the form of elevated glucocorticoid hormones or food restriction) is one environmental cue that can have strong formative effects on morphology, physiology, and behavior. Although many of the effects of developmental stress appear negative, there is increasing evidence for an adaptive role of developmental stress in shaping animal phenotype. Here, we take a three-pronged approach to review studies that have uncovered positive effects of developmental stress on phenotype in birds. We focus on studies that: (1) examine phenotypic effects likely to increase fitness in offspring, (2) directly identify increased fitness in offspring, or (3) provide evidence of fitness benefits to the mother, at a cost to the offspring. Throughout, we focus on studies that evaluate the environment when assessing the ‘costs/benefits’ of phenotype alterations and examine the effects of developmental stress across life-history stages. Finally, we consider the two common methods used to simulate developmental stress: food restriction and direct hormone manipulation. Although these methods are often considered to elicit equivalent responses, there has been very little discussion of this in the literature. To this end, we review the main methods used to implement developmental stress in experimental studies and discuss how they may simulate different environmental conditions. In light of our conclusions, we propose possible avenues for future research, stressing the need for a greater focus on direct fitness metrics, longitudinal studies, and experiments in free-living animals.
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References
Badyaev AV (2014) Epigenetic resolution of the “curse of complexity” in adaptive evolution of complex traits. J Physiol Lond 592:2251–2260. doi:10.1113/jphysiol.2014.272625
Banerjee SB, Arterbery AS, Fergus DJ, Adkins-Regan E (2012) Deprivation of maternal care has long-lasting consequences for the hypothalamic-pituitary-adrenal axis of zebra finches. P Roy Soc B Biol Sci 279:759–766. doi:10.1098/rspb.2011.1265
Blas J, Bortolotti GR, Tella JL, Baos R, Marchant TA (2007) Stress response during development predicts fitness in a wild, long lived vertebrate. P Natl Acad Sci 104:8880–8884. doi:10.1073/pnas.0700232104
Bonaparte KM, Riffle-Yokoi C, Burley NT (2011) Getting a head start: diet, sub-adult growth, and associative learning in a seed-eating passerine. Plos One 6:e23775
Breuner C (2008) Maternal stress, glucocorticoids, and the maternal/fetal match hypothesis. Horm Behav 54:485–487. doi:10.1016/j.yhbeh.2008.05.013
Buchanan KL, Spencer KA, Goldsmith AR, Catchpole CK (2003) Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). P Roy Soc B Biol Sci 270:1149–1156. doi:10.1098/rspb.2003.2330
Buchanan KL, Leitner S, Spencer KA, Goldsmith AR, Catchpole CK (2004) Developmental stress selectively affects the song control nucleus HVC in the zebra finch. P Roy Soc B Biol Sci 271:2381–2386
Cabezas S, Blas J, Marchant TA, Moreno S (2007) Physiological stress levels predict survival probabilities in wild rabbits. Horm Behav 51:313–320
Calandreau L et al (2011) Effect of one week of stress on emotional reactivity and learning and memory performances in Japanese quail. Behav Brain Res 217:104–110
Carmona-Isunza MC, Nunez-de la Mora A, Drummond H (2013) Chronic stress in infancy fails to affect body size and immune response of adult female blue-footed boobies or their offspring. J Avian Biol 44:390–398. doi:10.1111/j.1600-048X.2013.00057.x
Chin EH, Love OP, Verspoor JJ, Williams TD, Rowley K, Burness G (2009) Juveniles exposed to embryonic corticosterone have enhanced flight performance. P Roy Soc B Biol Sci 276:499–505. doi:10.1098/rspb.2008.1294
Chin EH, Quinn JS, Burness G (2013) Acute stress during ontogeny suppresses innate, but not acquired immunity in a semi-precocial bird (Larus delawarensis). Gen Comp Endocr 193:185–192. doi:10.1016/j.ygcen.2013.08.007
Coslovsky M, Richner H (2011) Predation risk affects offspring growth via maternal effects. Funct Ecol 25:878–888. doi:10.1111/j.1365-2435.2011.01834.x
Crino OL, Van Oorschot BK, Johnson EE, Malisch JL, Breuner CW (2011) Proximity to a high traffic road: glucocorticoid and life history consequences for nestling white-crowned sparrows. Gen Comp Endocr 173:323–332. doi:10.1016/j.ygcen.2011.06.001
Crino OL, Driscoll SC, Breuner CW (2014a) Corticosterone exposure during development has sustained but not lifelong effects on body size and total and free corticosterone responses in the zebra finch. Gen Comp Endocr 196:123–129. doi:10.1016/j.ygcen.2013.10.006
Crino OL, Driscoll SC, Ton R, Breuner CW (2014b) Corticosterone exposure during development improves performance on a novel foraging task in zebra finches. Anim Behav 91:27–32
Crino OL, Prather CT, Driscoll SC, Good JM, Breuner CW (2014c) Developmental stress increases reproductive success in male zebra finches, P Roy Soc B Biol Sci 281. doi:10.1098/Rspb.2014.1266(doi:Artn 20141266)
Fairhurst GD, Treen GD, Clark RG, Bortolotti GR (2012) Nestling corticosterone response to microclimate in an altricial bird. Can J Zool 90:1422–1430. doi:10.1139/cjz-2012-0096
Forstmeier W, Schielzeth H, Schneider M, Kempenaers B (2007) Development of polymorphic microsatellite markers for the zebra finch (Taeniopygia guttata). Mol Ecol Notes 7:1026–1028. doi:10.1111/j.1471-8286.2007.01762.x
Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158. doi:10.1126/science.286.5442.1155
Franzke A, Reinhold K (2013) Transgenerational effects of diet environment on life-history and acoustic signals of a grasshopper. Behav Ecol 24:734–739. doi:10.1093/beheco/ars205
Gil D, Naguib M, Riebel K, Rutstein A, Gahr M (2006) Early condition, song learning, and the volume of song brain nuclei in the zebra finch (Taeniopygia guttata). J Neurobiol 66:1602–1612. doi:10.1002/Neu.20312
Gluckman PD, Hanson MA (2004) Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res 56:311–317. doi:10.1203/01.Pdr.0000135998.08025.Fb
Goerlich VC, Natt D, Elfwing M, Macdonald B, Jensen P (2012) Transgenerational effects of early experience on behavioral, hormonal and gene expression responses to acute stress in the preococial chicken. Horm Behav 61:711–718
Grindstaff JL, Hunsaker VR, Cox SN (2012) Maternal and developmental immune challenges alter behavior and learning ability of offspring. Horm Behav 62:337–344. doi:10.1016/j.yhbeh.2012.04.005
Haussmann MF, Longenecker AS, Marchetto NM, Juliano SA, Bowden RM (2012) Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. P Roy Soc B Biol Sci 279:1447–1456. doi:10.1098/rspb.2011.1913
Hayward LS, Wingfield JC (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocr 135:365–371. doi:10.1016/j.ygcen.2003.11.002
Henriksen R, Rettenbacher S, Groothuis TGG (2011) Prenatal stress in birds: pathways, effects, function and perspectives. Neurosci Biobehav R 35:1484–1501. doi:10.1016/j.neubiorev.2011.04.010
Honarmand M, Goymann W, Naguib M (2010) Stressful dieting: nutritional conditions but not compensatory growth elevate corticosterone levels in zebra finch nestlings and fledglings. Plos One. doi:10.1371/journal.pone.0012930 ARTN e12930
Kitaysky AS, Kitaiskaia EV, Wingfield JC, Piatt JF (2001) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J Comp Physiol B 171:701–709. doi:10.1007/s003600100230
Kitaysky AS, Kitaiskaia EV, Wingfield JC (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Horm Behav 43:140–149
Kriengwatana B, Wada H, Schmidt KL, Taves MD, Soma KK, MacDougall-Shackleton SA (2014) Effects of nutritional stress during different developmental periods on song and the hypothalamic-pituitary-adrenal axis in zebra finches. Horm Behav 65:285–293. doi:10.1016/j.yhbeh.2013.12.013
Liu D et al (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662. doi:10.1126/science.277.5332.1659
Loiseau C, Sorci G, Dano S, Chastel O (2008) Effects of experimental increase of corticosterone levels on begging behavior, immunity and parental provisioning rate in house sparrows. Gen Comp Endocr 155:101–108. doi:10.1016/j.ygcen.2007.03.004
Love OP, Williams TD (2008a) The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. Am Nat 172:E135–E149. doi:10.1086/590959
Love OP, Williams TD (2008b) Plasticity in the adrenocortical response of a free-living vertebrate: the role of pre- and post-natal developmental stress. Horm Behav 54:496–505
Lucassen PJ, Naninck EFG, van Goudoever JB, Fitzsimons C, Joels M, Korosi A (2013) Perinatal programming of adult hippocampal structure and function; emerging roles of stress, nutrition and epigenetics. Trends Neurosci 36:621–631. doi:10.1016/j.tins.2013.08.002
Lynn SE, Kern MD (2014) Environmentally relevant bouts of cooling stimulate corticosterone secretion in free-living eastern bluebird (Sialia sialis) nestlings: potential links between maternal behavior and corticosterone exposure in offspring. Gen Comp Endocr 196:1–7. doi:10.1016/j.ygcen.2013.11.011
MacDougall-Shackleton SA, Spencer KA (2012) Developmental stress and birdsong: current evidence and future directions. J Ornithol 153:S105–S117. doi:10.1007/s10336-011-0807-x
Matthews SG (2002) Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrin Met 13:373–380. doi:10.1016/S1043-2760(02)00690-2
McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85:571–633. doi:10.1152/physrev.00053.2003
Metcalfe NB, Ure SE (1995) Diurnal-variation in-flight performance and hence potential predation risk in small birds. P Roy Soc B Biol Sci 261:395–400. doi:10.1098/rspb.1995.0165
Miller GM, Watson SA, Donelson JM, McCormick MI, Munday PL (2012) Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nat Clim Change 2:858–861. doi:10.1038/Nclimate1599
Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos T R Soc B 363:1635–1645. doi:10.1098/rstb.2007.0011
Monaghan P, Heidinger BJ, D’Alba L, Evans NP, Spencer KA (2012) For better or worse: reduced adult lifespan following early-life stress is transmitted to breeding partners. P Roy Soc B Biol Sci 279:709–714. doi:10.1098/rspb.2011.1291
Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407. doi:10.1016/S0169-5347(98)01472-4
Muller C, Jenni-Eiermann S, Jenni L (2009) Effects of a short period of elevated circulating corticosterone on postnatal growth in free-living Eurasian kestrels Falco tinnunculus. J Exp Biol 212:1405–1412. doi:10.1242/Jeb.024455
Nesan D, Vijayan MM (2013) Role of glucocorticoid in developmental programming: evidence from zebrafish. Gen Comp Endocr 181:35–44. doi:10.1016/j.ygcen.2012.10.006
Noble DWA, McFarlane SE, Keogh JS, Whiting MJ (2014) Maternal and additive genetic effects contribute to variation in offspring traits in a lizard. Behav Ecol. doi:10.1093/beheco/aru032
Nowicki S, Peters S, Podos J (1998) Song learning, early nutrition and sexual selection in songbirds. Am Zool 38:179–190
Nowicki S, Searcy WA, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Physiol A 188:1003–1014. doi:10.1007/s00359-002-0361-3
Patterson SH, Hahn TP, Cornelius JM, Breuner CW (2014) Natural selection and glucocorticoid physiology. J Evol Biol 27:259–274
Pravosudov VV, Kitaysky AS (2006) Effects of nutritional restrictions during post-hatching development on adrenocortical function in western scrub-jays (Aphelocoma californica). Gen Comp Endocr 145:25–31. doi:10.1016/j.ygcen.2005.06.011
Pravosudov VV, Lavenex P, Omanska A (2005) Nutritional deficits during early development affect hippocampal structure and spatial memory later in life. Behav Neurosci 119:1368–1374
Prudic KL, Jeon C, Cao H, Monteiro A (2011) Developmental plasticity in sexual roles of butterfly species drives mutational selection. Science 331:73–75
Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255
Roulin A et al (2008) Corticosterone mediates the condition-dependent component of melanin-based coloration. Anim Behav 75:1351–1358. doi:10.1016/j.anbehav.2007.09.007
Saino N, Romano M, Ferrari RP, Martinelli R, Moller AP (2005) Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. J Exp Zool Part A 303A:998–1006
Schmidt KL, MacDougall-Shackleton EA, Soma KK, MacDougall-Shackleton SA (2014) Developmental programming of the HPA and HPG axes by early-life stress in male and female song sparrows. Gen Comp Endocr 196:72–80
Schoech SJ, Rensel MA, Heiss RS (2011) Short- and long-term effects of developmental corticosterone exposure on avian physiology, behavioral phenotype, cognition, and fitness: a review. Curr Zool 57:514–530
Schutz KE, Forkman B, Jensen P (2001) Domestication effects on foraging strategy, social behaviour and different fear responses: a comparison between the red junglefowl (Gallus gallus) and a modern layer strain. Appl Anim Behav Sci 74:1–14
Sewall KB, Soha JA, Peters S, Nowicki S (2013) Potential trade-off between vocal ornamentation and spatial ability in a songbird. Biol Lett 9:2013. doi:10.1098/Rsbl.2013.0344 Unsp0344
Sheldon BC (2002) Adaptive maternal effects and rapid population differentiation. Trends Ecol Evol 17:247–249. doi:10.1016/S0169-5347(02)02459-X
Sheriff MJ, Love OP (2013) Determining the adaptive potential of maternal stress. Ecol Lett 16:271–280. doi:10.1111/Ele.12042
Spencer KA, MacDougall-Shackleton SA (2011) Indicators of development as sexually selected traits: the developmental stress hypothesis in context. Behav Ecol 22:1–9. doi:10.1093/beheco/arq068
Spencer KA, Verhulst S (2007) Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata). Horm Behav 51:273–280. doi:10.1016/j.yhbeh.2006.11.001
Spencer KA, Buchanan KL, Goldsmith AR, Catchpole CK (2003) Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm Behav 44:132–139. doi:10.1016/S0018-506x(03)00124-7
Spencer KA, Wimpenny JH, Buchanan KL, Lovell PG, Goldsmith AR, Catchpole CK (2005) Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata). Behav Ecol Sociobiol 58:423–428. doi:10.1007/s00265-005-0927-5
Spencer KA, Evans NP, Monaghan P (2009) Postnatal Stress in Birds: a Novel Model of Glucocorticoid Programming of the Hypothalamic-Pituitary-Adrenal Axis. Endocrinology 150:1931–1934. doi:10.1210/En.2008-1471
Stamps J (2003) Behavioural processes affecting development: Tinbergen’s fourth question comes of age. Anim Behav 66:1–13. doi:10.1006/anbe.2003.2180
Tissier ML, Williams TD, Criscuolo F (2014) Maternal effects underlie ageing costs of growth in the zebra finch (Taeniopygia guttata). Plos One. doi:10.1371/journal.pone.0097705
Tschirren B, Rutstein AN, Postma E, Mariette M, Griffith SC (2009) Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches. J Evolution Biol 22:387–395
Vallee M, Mayo M, Dellu F, LeMoal M, Simon H, Maccari S (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17:2626–2636
Wada H, Breuner CW (2008) Transient elevation of corticosterone alters begging behavior and growth of white-crowned sparrow nestlings. J Exp Biol 211:1696–1703. doi:10.1242/Jeb.009191
Walker BG, Boersma PD, Wingfield JC (2005a) Physiological and behavioral differences in Magellanic Penguin chicks in undisturbed and tourist-visited locations of a colony. Conserv Biol 19:1571–1577. doi:10.1111/j.1523-1739.2005.00104.x
Walker BG, Wingfield JC, Boersma PD (2005b) Age and food deprivation affects expression of the glucocorticosteroid stress response in magellanic penguin (Spheniscus magellanicus) chicks. Physiol Biochem Zool 78:78–89
Weaver ICG et al (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854. doi:10.1038/Nn1276
Wilsterman K, Mast AD, Luu TH, Haussmann MF (2015) The timing of embryonic exposure to elevated temperature alters stress endocrinology in domestic chickens (Gallus domesticus). Gen Comp Endocr 212:10–16
Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage”. Integr Comp Biol 38:191–206
Zimmer C, Spencer KA (2014) Reduced resistance to oxidative stress during reproduction as a cost of early-life stress. Comp Biochem Phys A 183:9–13
Zimmer C, Boogert NJ, Spencer KA (2013) Developmental programming: cumulative effects of increased pre-hatching corticosterone levels and post-hatching unpredictable food availability on physiology and behaviour in adulthood. Horm Behav 64:494–500. doi:10.1016/j.yhbeh.2013.07.002
Acknowledgments
We would like to thank Kendra Sewall, Haruka Wada and Brit Heidinger for organizing the symposium on developmental stress. The Wildlife Biology Program at the University of Montana provided travel support to CWB to attend the IOC.
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Communicated by E. Matthysen.
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Crino, O.L., Breuner, C.W. Developmental stress: evidence for positive phenotypic and fitness effects in birds. J Ornithol 156 (Suppl 1), 389–398 (2015). https://doi.org/10.1007/s10336-015-1236-z
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DOI: https://doi.org/10.1007/s10336-015-1236-z