An experimental analysis of the heritability of variation in glucocorticoid concentrations in a wild avian population

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1790, 2014, Pages

  Jenkins, Brittany R ^a,b   Vitousek, Maren N ^a,c   Hubbard, Joanna K ^a   Safran, Rebecca J ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF WYOMING   (United States)

^c Cornell University ^*  (United States)

Author keywords

Animal model; Barn swallow; Cross foster; Environmental variation; Glucocorticoids; Heritability

Indexed keywords

ADAPTATION; AVIFAUNA; CONCENTRATION (COMPOSITION); ECOLOGICAL MODELING; ENVIRONMENTAL FACTOR; EXPERIMENTAL DESIGN; HERITABILITY; HORMONE; PASSERINE; PHENOTYPE; POPULATION STRUCTURE; SECRETION; STEROID;

CORTICOSTERONE; GLUCOCORTICOID;

ADAPTATION; ANIMAL; BLOOD; FEMALE; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; MALE; NEWBORN; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SWALLOW (BIRD);

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; CORTICOSTERONE; FEMALE; GENOTYPE; GLUCOCORTICOIDS; MALE; STRESS, PHYSIOLOGICAL; SWALLOWS;

EID: 85003052695     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.1302     Document Type: Article

References (61)

1. Cockrem JF. 2013 Individual variation in glucocorticoid stress response in animals. Gen. Comp. Endocr. 181, 45-58. (doi: 10. 1016/j. ygcen. 2012. 11. 025)
2. Wingfield JC. 2003 Control of behavioural strategies for capricious environments. Anim. Behav. 66, 807-816. (doi: 10. 1006/anbe. 2003. 2298)
3. Blas J, Bortolotti GR, Tella JL, Baos R, Marchant TA. 2007 Stress response during development predicts fitness in a wild, long lived vertebrate. Proc. Natl Acad. Sci. USA104, 8880-8884. (doi: 10. 1073/pnas. 0700232104)
4. Angelier F, Holberton RL, Marra PP. 2009 Does stress response predict return rate in a migratory bird species? A study of American redstarts and their non-breeding habitat. Proc. R. Soc. B276, 3545-3551. (doi: 10. 1098/rspb. 2009. 0868)
5. Romero LM, Wikelski M. 2010 Stress physiology as a predictor of survival in Galapagos marine iguanas. Proc. R. Soc. B277, 3157-3162. (doi: 10. 1098/rspb. 2010. 0678)
6. Ouyang JQ, Hau M, Bonier F. 2011 Within seasons and among years: when are corticosterone levels repeatable? Horm. Behav. 60, 559-564. (doi: 10. 1016/j. yhbeh. 2011. 08. 004)
7. Ouyang JQ, Quetting M, Hau M. 2012 Corticosterone and brood abandonment in a passerine bird. Anim. Behav. 84, 261-268. (doi: 10. 1016/j. anbehav. 2012. 05. 006)
8. Angelier F, Wingfield JC, Weimerskirch H, Chastel O. 2010 Hormonal correlates of individual quality in a long-lived bird: a test of the 'corticosterone-fitness hypothesis'. Biol. Lett. 6, 846-849. (doi: 10. 1098/ rsbl. 2010. 0376)
9. Carere C, Caramaschi D, Fawcett TW. 2010 Covariation between personalities and individual differences in coping with stress: converging evidence and hypotheses. Curr. Zool. 56, 728-740.
10. 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.
11. Landys MM, Ramenofsky M, Wingfield JC. 2006 Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocr. 148, 132-149. (doi: 10. 1016/j. ygcen. 2006. 02. 013)
12. Sapolsky RM, Romero LM, Munck AU. 2000 How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55-89. (doi: 10. 1210/er. 21. 1. 55)
13. Bókony V, Lendvai AZ, Liker A, Angelier F, Wingfield JC, Chastel O. 2009 Stress response and the value of reproduction: are birds prudent parents?. Am. Nat. 173, 589-598. (doi: 10. 1086/597610)
14. Schultner J, Kitaysky AS, Gabrielsen GW, Hatch SA, Bech C. 2013 Differential reproductive responses to stress reveal the role of life-history strategies within a species. Proc. R. Soc. B280, 20132090. (doi: 10. 1098/rspb. 2013. 2090)
15. Goymann W, Geue D, Schwabl I, Flinks H, Schmidl D, Schwabl H, Gwinner E. 2006 Testosterone and corticosterone during the breeding cycle of equatorial and European stonechats (Saxicola torquata axillaris andS. t. rubicola). Horm. Behav. 50, 779-785. (doi: 10. 1016/j. yhbeh. 2006. 07. 002)
16. Hau M, Ricklefs RE, Wikelski M, Lee KA, Brawn JD. 2010 Corticosterone, testosterone and life-history strategies of birds. Proc. R. Soc. B277, 3203-3212. (doi: 10. 1098/rspb. 2010. 0673)
17. Eikenaar C, Husak J, Escallón C, Moore IT. 2012 Variation in testosterone and corticosterone in amphibians and reptiles: relationships with latitude, elevation, and breeding season length. Am. Nat. 180, 642-654. (doi: 10. 1086/667891)
18. Wingfield JC, Vleck CM, Moore MC. 1992 Seasonal changes of the adrenocortical response to stress in birds of the Sonoran Desert. J. Exp. Zool. 264, 419-428. (doi: 10. 1002/jez. 1402640407)
19. Wingfield JC, Deviche P, Sharbaugh S, Astheimer LB, Holberton R, Suydam R, Hunt K. 1994 Seasonal changes of the adrenocortical responses to stress in redpolls, Acanthis flammea, in Alaska. J. Exp. Zool. 270, 372-380. (doi: 10. 1002/jez. 1402700406)
20. Herring G, Cook MI, Gawlik DE, Call EM. 2011 Food availability is expressed through physiological stress indicators in nestling white ibis: a food supplementation experiment. Funct. Ecol. 25, 682-690. (doi: 10. 1111/j. 1365-2435. 2010. 01792. x)
21. Clinchy M, Zanette L, Charlier TD, Newman AEM, Schmidt KL, Boonstra R, Soma KK. 2011 Multiple measures elucidate glucocorticoid responses to environmental variation in predation threat. Oecologia166, 607-614. (doi: 10. 1007/s00442-011-1915-2)
22. Lynch M, Walsh B. 1998Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates Inc.
23. Satterlee DG, Johnson WA. 1988 Selection of Japanese quail for contrasting blood corticosterone response to immobilization. Poultry Sci. 67, 25-32. (doi: 10. 3382/ps. 0670025)
24. Pottinger TG, Carrick TR. 1999 Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen. Comp. Endocr. 116, 122-132. (doi: 10. 1006/gcen. 1999. 7355)
25. Odeh FM, Cadd GG, Satterlee DG. 2003 Genetic characterization of stress responsiveness in Japanese quail. 2. Analyses of maternal effects, additive sex linkage effects, heterosis, and heritability by diallel crosses. Poultry Sci. 82, 31-35. (doi: 10. 1093/ps/82. 1. 31)
26. Evans MR, Roberts ML, Buchanan KL, Goldsmith AR. 2006 Heritability of corticosterone response and changes in life history traits during selection in the zebra finch. J. Evol. Biol. 19, 343-352. (doi: 10. 1111/j. 1420-9101. 2005. 01034. x)
27. Touma Cet al. 2008 Mice selected for high versus low stress reactivity: a new animal model for affective disorders. Psychoneuroendocrinology33, 839-862. (doi: 10. 1016/j. psyneuen. 2008. 03. 013)
28. Hodgson ZG, Meddle SL, Roberts ML, Buchanan KL, Evans MR, Metzdorf R, Gahr M, Healy SD. 2007 Spatial ability is impaired and hippocampal mineralcorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress. Proc. R. Soc. B274, 239-245. (doi: 10. 1098/rspb. 2006. 3704)
29. Stöwe M, Rosivall B, Drent PJ, Möstl E. 2010 Selection for fast and slow exploration affects baseline and stress-induced corticosterone excretion in great tit nestlings, Parus major. Horm. Behav. 58, 864-871. (doi: 10. 1016/j. yhbeh. 2010. 08. 011)
30. Baugh AT, Schaper SV, Hau M, Cockrem JF, de Goede P, van Oers K. 2012 Corticosterone responses differ between lines of great tits (Parus major) selected for divergent personalities. Gen. Comp. Endocr. 175, 488-494. (doi: 10. 1016/j. ygcen. 2011. 12. 012)
31. Weaver ICG, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004 Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854. (doi: 10. 1038/ n10. 1038/nn1276 n1276)
32. Darnaudéry M, Maccari S. 2008 Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res. Rev. 57, 571-585. (doi: 10. 1016/j. brainresrev. 2007. 11. 004)
33. Romero LM, Reed JM. 2005 Collecting baseline corticosterone samples in the field: is under 3 min good enough?Comp. Biochem. Phys. A 140, 73-79. (doi: 10. 1016/j. cbpb. 2004. 11. 004)
34. Jenkins BR, Vitousek MN, Safran RJ. 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. (doi: 10. 1016/j. yhbeh. 2013. 08. 006)
35. Wada H, Hahn TP, Breuner CW. 2007 Development of stress reactivity in white-crowned sparrow nestlings: total corticosterone response increases with age, while free corticosterone response remains low. Gen. Comp. Endocr. 150, 405-413. (doi: 10. 1016/j. ygcen. 2006. 10. 002)
36. Neuman CR, Safran RJ, Lovette IJ. 2007 Male tail streamer length does not predict paternity in a population of North American barn swallows. J. Avian Biol. 38, 28-36. (doi: 10. 1111/j. 2007. 0908-8857. 03713. x)
37. Griffiths R, Double MC, Orr K, Dawson RJG. 1998 A DNA test to sex most birds. Mol. Ecol. 7, 1071-1075. (doi: 10. 1046/j. 1365-294x. 1998. 00389. x)
38. Hadfield JD. 2010 MCMC methods for multiresponse generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1-22.
39. Taylor RW, Boon AK, Dantzer B, Réale D, Humphries MM, Boutin S, Gorrell JC, Coltman DW, McAdam AG. 2012 Low heritabilities, but genetic and maternal correlations between squirrel behaviours. J. Evol. Biol. 25, 614-624. (doi: 10. 1111/j. 1420-9101. 2012. 02456. x)
40. Romero LM. 2002 Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocr. 128, 1-24. (doi: 10. 1016/S0016-6480(02)00064-3)
41. Charmantier A, Grant D. 2005 Environmental quality and evolutionary potential: lessons from wild populations. Proc. R. Soc. B272, 1415-1425. (doi: 10. 1098/rspb. 2005. 3117)
42. Kino T. 2012 Circadian rhythms of glucocorticoid hormone actions in target tissues: potential clinical implications. Sci. Signal5(pt4). (doi: 10. 1126/ scisignal. 2003333)
43. Cockrem JF, Silverin B. 2002 Variation within and between birds in corticosterone responses of great tits (Parus major). Gen. Comp. Endocr. 125, 197-206. (doi: 10. 1006/gcen. 2001. 7750)
44. Bonier F, Martin PR, Moore IT, Wingfield JC. 2009 Do baseline glucocorticoids predict fitness?Trends Ecol. Evol. 24, 634-642. (doi: 10. 1016/j. tree. 2009. 04. 013)
45. Bize P, Stocker A, Jenni-Eiermann S, Gasparini J, Roulin A. 2010 Sudden weather deterioration but not brood size affects baseline corticosterone levels in nestling alpine swifts. Horm. Behav. 58, 591-598. (doi: 10. 1016/j. yhbeh. 2010. 06. 020)
46. Kitaysky AS, Wingfield JC, Piatt JF. 2001 Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav. Ecol. 12, 619-625. (doi: 10. 1016/j. yhbeh. 2007. 10. 010)
47. Saino N, Suffritti C, Martinelli R, Rubolini D, Møller AP. 2003 Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica). Behav. Ecol. 14, 318-325. (doi: 10. 1093/beheco/14. 3. 318)
48. Gil D, Bulmer E, Celis P, Puerta M. 2008 Increased sibling competition does not increase testosterone or corticosterone levels in nestlings of the spotless starling (Sturnus unicolor). Horm. Behav. 54, 238-243. (doi: 10. 1016/j. yhbeh. 2007. 11. 013)
49. Kozlowski C, Ricklefs RE. 2011 The effects of brood size on growth and steroid hormone concentrations in nestling eastern bluebirds (Sialia sialis). Gen. Comp. Endocr. 173, 447-453. (doi: 10. 1016/j. ygcen. 2011. 07. 002)
50. Vitousek MN, Jenkins BR, Hubbard JK, Safran RJ. In preparation. Are corticosterone levels flexibly modulated based on brood value? An experimental test in breeding barn swallows.
51. Vitousek MN, Jenkins BR, Safran RJ. Submitted. Stress and success: individual differences in the glucocorticoid stress response predict behavior and reproductive success under high predation risk.
52. Kitaysky AS, Piatt JF, Wingfield JC, Romero M. 1999 The adrenocortical stress-response of black-legged kittiwake chicks in relation to dietary restrictions. J. Comp. Phys. B 169, 303-310. (doi: 10. 1007/ s003600050225)
53. Romero LM, Reed JM, Wingfield JC. 2000 Effects of weather on corticosterone responses in wild freeliving passerine birds. Gen. Comp. Endocrinol. 118, 113-122. (doi: 10. 1006/gcen. 1999. 7446)
54. Grissom N, Bhatnagar S. 2009 Habituation to repeated stress: get used to it. Neurobiol. Learn Mem. 92, 215-224. (doi: 10. 1016/j. nlm. 2008. 07. 001)
55. Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG. 2006 Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J. Physiol. 572, 31-44. (doi: 10. 1113/jphysiol. 2006. 105254)
56. Entringer S, Kumsta R, Hellhammer DH, Wadhwa PD, Wüst S. 2009 Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Horm. Behav. 55, 292-298. (doi: 10. 1016/j. yhbeh. 2008. 11. 006)
57. Hayward LS, Wingfield JC. 2004 Maternal corticosterone is transferred to avian yolk and may alter offspring growth and phenotype. Gen. Comp. Endocr. 135, 365-371. (doi: 10. 1016/j. ygcen. 2003. 11. 002)
58. Love OP, Chin EH, Wynne-Edwards KE, Williams TD. 2005 Stress hormones: a link between maternal condition and sex-biased reproductive investment. Am. Nat. 166, 751-766. (doi: 10. 1086/497440)
59. Saino N, Romano M, Ferrari RP, Martinelli R, Møller AP. 2005 Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. J. Exp. Zool. 303A, 998-1006. (doi: 10. 1002/jez. a. 224)
60. DuRant SE, Hepp GR, Moore IT, Hopkins BC, Hopkins WA. 2009 Slight differences in incubation temperature affect early growth and stress endocrinology of wood duck (Aix sponsa) ducklings. J. Exp. Biol. 213, 45-51. (doi: 10. 1242/jeb. 034488)
61. Nätt D, Rubin CJ, Wright D, Johnsson M, Beltéky J, Andersson L, Jensen P. 2012 Heritable genomewide variation in gene expression and promoter methylation between wild and domesticated chickens. BMC Genomics13, 59. (doi: 10. 1186/1471-2164-13-59)