Relationship between maternal environment and DNA methylation patterns of estrogen receptor alpha in wild Eastern Bluebird (Sialia sialis) nestlings: a pilot study

Ecology and Evolution

Volumn 6, Issue 14, 2016, Pages 4741-4752

  Bentz, Alexandra B ^a   Sirman, Aubrey E ^b   Wada, Haruka ^b   Navara, Kristen J ^a   Hood, Wendy R ^b  

^a UNIVERSITY OF GEORGIA   (United States)

^b AUBURN UNIVERSITY   (United States)

Author keywords

Breeding density; diencephalon; growth rate; maternal effect; yolk testosterone

Indexed keywords

EID: 84978204624     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.2162     Document Type: Article

References (91)

1. Addison, M. L., and E. F. Rissman. 2012. Sexual dimorphism of growth hormone in the hypothalamus: regulation by estradiol. Endocrinology 153:1898–1907.
2. Avtanski, D., H. J. Novaira, S. Wu, C. J. Romero, R. Kineman, R. M. Luque, et al. 2014. Both estrogen receptor α and β stimulate pituitary GH gene expression. Mol. Endocrinol. 28:40–52.
3. Bagamasbad, P., and R. J. Denver. 2011. Mechanisms and significance of nuclear receptor auto- and cross-regulation. Gen. Comp. Endocrinol. 170:3–17.
4. Balthazart, J., A. Foidart, C. Surlemont, A. Vockel, and N. Harada. 1990. Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: an immunocytochemical study. J. Comp. Neurol. 301:276–288.
5. Bentz, A. B., K. J. Navara, and L. Siefferman. 2013. Phenotypic plasticity in response to breeding density in tree swallows: an adaptive maternal effect? Horm. Behav. 64:729–736.
6. Buntin, J. D., and G. R. Figge. 1988. Prolactin and growth hormone stimulate food intake in ring doves. Pharmacol. Biochem. Behav. 31:533–540.
7. Carninci, P., A. Sandelin, B. Lenhard, S. Katayama, K. Shimokawa, J. Ponjavic, et al. 2006. Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet. 38:626–635.
8. Cartharius, K., K. Frech, K. Grote, B. Klocke, M. Haltmeier, A. Klingenhoff, et al. 2005. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21:2933–2942.
9. Champagne, F. A., I. C. G. Weaver, J. Diorio, S. Dymov, M. Szyf, and M. J. Meaney. 2006. Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology 147:2909–2915.
10. Childs, G. V., M. Iruthayanathan, N. Akhter, G. Unabia, and B. Whitehead-Johnson. 2005. Bipotential Effects of estrogen on growth hormone synthesis and storage in vitro. Endocrinology 146:1780–1788.
11. Cucco, M., B. Guasco, G. Malacarne, R. Ottonelli, and A. Tanvez. 2008. Yolk testosterone levels and dietary carotenoids influence growth and immunity of grey partridge chicks. Gen. Comp. Endocrinol. 156:418–425.
12. Dloniak, S. M., J. A. French, and K. E. Holekamp. 2006. Rank-related maternal effects of androgens on behavior in wild spotted hyaenas. Nature 440:1190–1193.
13. Duckworth, R. A., V. Belloni, and S. R. Anderson. 2015. Cycles of species replacement emerge from locally induced maternal effects on offspring behavior in a passerine bird. Science 347:875–877.
14. Eising, C. M., C. Eikenaar, H. Schwabl, and T. G. G. Groothuis. 2001. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc. Biol. Sci. 268:839–846.
15. Eising, C. M., W. Müller, and T. G. G. Groothuis. 2006. Avian mothers create different phenotypes by hormone deposition in their eggs. Biol. Lett. 2:20–22.
16. von Engelhardt, N., and T. Groothuis. 2011. Maternal hormones in avian eggs. Pp. 91–127 in D. Norris and K. Lopez, eds. Hormones and reproduction of vertebrates 4: birds. Academic Press, Amsterdam.
17. von Engelhardt, N., R. Henriks, and T. G. G. Groothuis. 2009. Steroids in chicken egg yolk: metabolism and uptake during early embryonic development. Gen. Comp. Endocrinol. 163:175–183.
18. Feil, R., and M. F. Fraga. 2012. Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Genet. 13:97–109.
19. Filby, A. L., G. C. Paull, T. F. A. Hickmore, and C. R. Tyler. 2010. Unravelling the neurophysiological basis of aggression in a fish model. BMC Genom. 11:498–515.
20. Fürst, R. W., H. Kliem, H. H. Meyer, and S. E. Ulbrich. 2012. A differentially methylated single CpG-site is correlated with estrogen receptor alpha transcription. J. Steroid Biochem. Mol. Biol. 130:96–104.
21. Goodson, J. L. 2005. The vertebrate social behavior network: evolutionary themes and variations. Horm. Behav. 48:11–22.
22. Gorman, K. B., and T. D. Williams. 2005. Correlated evolution of maternally derived yolk testosterone and early developmental traits in passerine birds. Biol. Lett. 1:461–464.
23. Gowaty, P. A., and J. H. Plissner. 1998. Eastern bluebird (Sialia sialis). Pp. 1–32 in A. Poole, ed. The birds of North America. The Birds of North America Online, Ithaca, New York.
24. Groothuis, T. G. G., and H. Schwabl. 2008. Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos. Trans. Biol. Sci. 363:1647–1661.
25. Groothuis, T. G. G., W. Müller, N. von Engelhardt, C. Carere, and C. Eising. 2005. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29:329–352.
26. Grubbs, F. E. 1950. Sample Criteria for testing outlying observations. Ann. Math. Stat. 21:27–58.
27. Hall, T. R., S. Harvey, and A. Chadwick. 1984. Oestradiol 17β modifies fowl pituitary prolactin and growth hormone secretion in vitro. Gen. Comp. Endocrinol. 56:299–307.
28. Hargitai, R., K. E. Arnold, M. Herenyi, J. Prechl, and J. Torok. 2009. Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher. Behav. Ecol. Sociobiol. 63:869–882.
29. Harvey, S. 1985. Neuroendocrine regulation of growth hormone secretion in birds. Pp. 105–109 in B. Lofts and W. N. Holmes, eds. Current trends in comparative endocrinology. Hong Kong University Press, Hong Kong, China.
30. Hassan, H. A., W. J. Enright, H. A. Tucker, and R. A. Merkel. 2001. Estrogen and androgen elicit growth hormone release via dissimilar patterns of hypothalamic neuropeptide secretion. Steroids 66:71–80.
31. Hegyi, G., and H. Schwabl. 2010. Do different yolk androgens exert similar effects on the morphology or behaviour of Japanese quail hatchlings Cotrunix japonica? J. Avian Biol. 41:258–265.
32. Holliday, R. 1994. Epigenetics: an overview. Dev. Genet. 15:453–457.
33. Jiang, M., Y. Zhang, J. Fei, X. Chang, W. Fan, X. Qian, et al. 2010. Rapid quantification of DNA methylation by measuring relative peak heights in direct bisulfite-PCR sequencing traces. Lab. Invest. 90:282–290.
34. Johnson, D. H. 1999. The insignificance of statistical significance testing. J. Wildl. Manag. 63:763–772.
35. Kamegai, J., H. Tamura, T. Shimizu, S. Ishii, H. Sugihara, and I. Wakabayashi. 2001. Estrogen receptor ERα, but not ERβ, gene is expressed in growth hormone-releasing hormone neurons of the male rat hypothalamus. Endocrinology 142:538–543.
36. Kitazawa, R., and S. Kitazawa. 2007. Methylation status of a single CpG locus 3 bases upstream of TATA-box of receptor activator of nuclear factor-κb ligand (RANKL) gene promoter modulates cell- and tissue-specific RANKL expression and osteoclastogenesis. Mol. Endocrinol. 21:148–158.
37. Koller, M., and W. A. Stahel. 2011. Sharpening wald-type inference in robust regression for small samples. Comput. Stat. Data Anal. 55:2504–2515.
38. Komsta, L. 2011. outliers: Tests for outliers. R package version 0.14.
39. Lam, K. S. L., M. F. Lee, S. P. Tam, and G. Srivastava. 1996. Gene expression of the receptor for growth-hormone-releasing hormone is physiologically regulated by glucocorticoids and estrogen. Neuroendocrinology 63:475–480.
40. Love, O. P., K. E. Wynne-Edwards, L. Bond, and T. D. Williams. 2008. Determinants of within-and among-clutch variation in yolk corticosterone in the European starling. Horm. Behav. 53:104–111.
41. Matsuda, K. I., H. Mori, B. M. Nugent, D. W. Pfaff, M. M. McCarthy, and M. Kawata. 2011. Histone deacetylation during brain development is essential for permanent masculinization of sexual behavior. Endocrinology 152:2760–2767.
42. Mazuc, J., C. Bonneaud, O. Chastel, and G. Sorci. 2003. Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol. Lett. 6:1084–1090.
43. Mcadam, A. G., S. Boutin, D. Réale, and D. Berteaux. 2002. Maternal effects and the potential for evolution in a natural population of animals. Evolution 56:846–851.
44. Meinhardt, U. J., and K. K. Y. Ho. 2006. Modulation of growth hormone action by sex steroids. Clin. Endocrinol. 65:413–422.
45. Mori, H., K. I. Matsuda, S. Tsukahara, and M. Kawata. 2010. Intrauterine position affects estrogen receptor α expression in the ventromedial nucleus of the hypothalamus via promoter DNA methylation. Endocrinology 151:5775–5781.
46. Mousseau, T. A., and C. W. Fox. 1998. The adaptive significance of maternal effects. Trends Ecol. Evol. 13:403–407.
47. Müller, W., T. G. G. Groothuis, C. Dijkstra, H. Siitari, and R. V. Alatalo. 2004. Maternal antibody transmission and breeding densities in the black-headed gull Larus ridibundus. Funct. Ecol. 18:719–724.
48. Müller, W., T. G. G. Groothuis, C. M. Eising, and C. Dijkstra. 2005. An experimental study on the causes of sex-biased mortality in the black-headed gull − the possible role of testosterone. J. Anim. Ecol. 74:735–741.
49. Müller, W., C. Dijkstra, and T. G. G. Groothuis. 2009. Maternal androgens stimulate territorial behaviour in black-headed gull chicks. Biol. Lett. 5:586–588.
50. Müller, M. S., Y. Roelofs, K. E. Erikstad, and T. G. Groothuis. 2012. Maternal androgens increase sibling aggression, dominance, and competitive ability in the siblicidal black-legged kittiwake (Rissa tridactyla). PLoS One 7:e47763.
51. Murgatroyd, C., A. V. Patchev, Y. Wu, V. Micale, Y. Bockmuhl, D. Fischer, et al. 2009. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 12:1559–1566.
52. Navara, K. J., G. E. Hill, and M. T. Mendonça. 2005. Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol. Biochem. Zool. 78:570–578.
53. Navara, K. J., G. E. Hill, and M. T. Mendonça. 2006a. Yolk testosterone stimulates growth and immunity in house finch chicks. Physiol. Biochem. Zool. 79:550–555.
54. Navara, K. J., L. M. Siefferman, G. E. Hill, and M. T. Mendonça. 2006b. Yolk androgens vary inversely to maternal androgens in Eastern bluebirds: an experimental study. Funct. Ecol. 20:449–456.
55. Parren, S. G. 1991. Evaluation of nest-box sites selected by eastern bluebirds, tree swallows, and house wrens. Wildl. Soc. Bull. 19:270–277.
56. Parsons, I. C. 1970. The metabolism of testosterone by early chick embryonic blastoderm. Steroids 16:59–65.
57. Partecke, J., and H. Schwabl. 2008. Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Dev. Neurobiol. 68:1538–1548.
58. Perlman, W. R., and A. P. Arnold. 2003. Expression of estrogen receptor and aromatase mRNAs in embryonic and posthatch zebra finch brain. J. Neurobiol. 55:204–219.
59. Petersenn, S., A. C. Rasch, M. Heyens, and H. M. Schulte. 1998. Structure and regulation of the human growth hormone-releasing hormone receptor gene. Mol. Endocrinol. 12:233–247.
60. Pfannkuche, K. A., M. Gahr, I. M. Weites, B. Riedstra, C. Wolf, and T. G. G. Groothuis. 2011. Examining a pathway for hormone mediated maternal effects – yolk testosterone affects androgen receptor expression and endogenous testosterone production in young chicks (Gallus gallus domesticus). Gen. Comp. Endocrinol. 172:487–493.
61. Pilz, K. M., and H. G. Smith. 2004. Egg yolk androgen levels increase with breeding density in the European Starling, Sturnus vulgaris. Funct. Ecol. 18:58–66.
62. Pilz, K. M., M. Quiroga, H. Schwabl, and E. Adkins-Regan. 2004. European starling chicks benefit from high yolk testosterone levels during a drought year. Horm. Behav. 46:179–192.
63. Pinheiro, J., D. Bates, S. DebRoy, and D. Sarkar. 2015. nlme: Linear and nonlinear mixed effects models. R package version 3.1-121.
64. Pinkowski, B. C. 1976. Use of tree cavities by nesting Eastern bluebirds. J. Wildl. Manag. 40:556–563.
65. R Development Core Team 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
66. Räsänen, K., and L. E. B. Kruuk. 2007. Maternal effects and evolution at ecological time-scales. Funct. Ecol. 21:408–421.
67. Reiner, A., D. J. Perkel, L. L. Bruce, A. B. Butler, A. Csillaq, W. Kuenzel, et al. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473:377–414.
68. Remeš, V., B. Matysioková, and B. Klejdus. 2011. Egg yolk antioxidant deposition as a function of parental ornamentation, age, and environment in great tits Parus major. J. Avian Biol. 42:387–396.
69. Rosvall, K. A., C. M. B. Burns, J. Barske, J. L. Goodson, B. A. Schlinger, D. R. Sengelaub, et al. 2012. Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution. Proc. R. Soc. B 279:3547–3555.
70. Rothman, K. J. 1990. No adjustments are needed for multiple comparisons. Epidemiology 1:43–46.
71. Rousseeuw, P. J., and A. M. Leroy. 1987. Robust regression and outlier detection. John Wiley & Sons Inc, New York, NY.
72. Rousseeuw, P., C. Croux, V. Todorov, A. Ruckstuhl, M. Salibian-Barrera, T. Verbeke, et al. 2015. robustbase: Basic Robust Statistics. R package version 0.92-5.
73. Safran, R. J., K. J. McGraw, K. M. Pilz, and S. M. Correa. 2010. Egg-yolk androgen and carotenoid deposition as a function of maternal social environment in barn swallows Hirundo rustica. J. Avian Biol. 41:470–478.
74. Scanes, C. G., and J. Balthazart. 1981. Circulating concentrations of growth hormone during growth, maturation, and reproductive cycles in ring doves (Streptopelia risoria). Gen. Comp. Endocrinol. 45:381–385.
75. Scanes, C. G., S. V. Radecki, and S. Malamed. 1992. Mechanisms involved in the avian patterns of growth hormone secretion during growth and development. Ornis Scandinavica 23:214–221.
76. Schew, W. A., F. M. A. McNabb, and C. G. Scanes. 1996. Comparison of the ontogenesis of thyroid hormones, growth hormone, and insulin-like growth factor-i in ad libitum and food-restricted (altricial) european starlings and (precocial) Japanese quail. Gen. Comp. Endocrinol. 101:304–316.
77. Schlinger, B. A., and G. V. Callard. 1990. Aromatization mediates aggressive behavior in quail. Gen. Comp. Endocrinol. 79:39–53.
78. Schwabl, H. 1993. Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. 90:11446–11450.
79. Schwabl, H. 1996. Maternal testosterone in the avian egg enhances postnatal growth. Comp. Biochem. Physiol. A Physiol. 114:271–276.
80. Schwarz, J. M., B. M. Nugent, and M. M. McCarthy. 2010. Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology 151:4871–4881.
81. Soma, K. K. 2006. Testosteorne and aggression: berthold, birds and beyond. J. Neuroendocrinol. 18:543–551.
82. Strasser, R., and H. Schwabl. 2004. Yolk testosterone organizes behavior and male plumage coloration in house sparrows. Behav. Ecol. Sociobiol. 56:491–497.
83. Tennenbaum, G. S. 1980. Evidence for autoregulation of growth hormone secretion via the central nervous system. Endocrinology 107:2117–2120.
84. Verboven, N., N. P. Evans, L. D'Alba, R. G. Nager, J. D. Blount, P. F. Surai, et al. 2005. Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus). Behav. Ecol. Sociobiol. 57:357–365.
85. Vickaryous, N., and E. Whitelaw. 2005. The role of the early embryonic environment on epigeotype and phenotype. Reprod. Fertil. Dev. 17:335–340.
86. Walters, M. J., and C. F. Harding. 1988. The effects of an aromatization inhibitor on the reproductive behavior of male zebra finches. Horm. Behav. 22:207–218.
87. Warren, W. C., D. F. Clayton, H. Ellegren, A. P. Arnold, L. W. Hillier, A. Künstner, et al. 2010. The genome of a songbird. Nature 464:757–762.
88. Weaver, I. C. G., N. Cervoni, F. A. Champagne, A. C. D'Alessio, S. Sharma, J. R. Seckl, et al. 2004. Epigenetic programming by maternal behavior. Nat. Neurosci. 7:847–854.
89. Whittingham, L. A., and H. Schwabl. 2001. Maternal testosterone in tree swallow eggs varies with female aggression. Animal Behavior 63:63–67.
90. Wingfield, J. C., and D. S. Farner. 1975. The determination of 5 steroids in avian plasma by radioimmunoassay and competitive-protein-binding. Steroids 3:311–327.
91. Yan, M., M. E. E. Jones, M. Hernandez, D. Liu, E. R. Simpson, and C. Chen. 2004. Functional modification of pituitary somatotropes in the aromatase knockout mouse and the effect of estrogen replacement. Endocrinology 145:604–612.