Differential effects of maternal yolk androgens on male and female offspring: A role for sex-specific selection?

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Tschirren, Barbara ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLOGICAL TRAIT; BODY MASS; BODY SIZE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EGG YOLK; FEMALE; FLEDGING MASS; FLEDGING SIZE; GENDER AND SEX; GROWTH; HATCHING; MALE; NESTLING; NONHUMAN; PARUS MAJOR; PHENOTYPE; PRENATAL EXPOSURE; PROGENY; QUANTITATIVE ANALYSIS; SEX; SEX DIFFERENCE; SEX RATIO; SEX SPECIFIC SELECTION; SURVIVAL; ANIMAL; CHEMISTRY; PASSERIFORMES; PHYSIOLOGY; SEXUAL DEVELOPMENT; SPECIES DIFFERENCE; WILD ANIMAL;

ANDROGENS; ANIMALS; ANIMALS, WILD; BODY SIZE; EGG YOLK; FEMALE; MALE; PASSERIFORMES; PHENOTYPE; SEX CHARACTERISTICS; SEX FACTORS; SPECIES SPECIFICITY; TESTOSTERONE;

EID: 84941768942     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133673     Document Type: Article

References (38)

1. Mousseau TA, Fox CW. Maternal Effects As Adaptations. New York: Oxford University Press; 1998.
2. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol. 2001; 65: 427-451. PMID: 11689280
3. Hines M. Prenatal endocrine influences on sexual orientation and on sexually differentiated childhood behavior. Front Neuroendocrinol. 2011; 32:170-182. doi: 10.1016/j.yfrne.2011.02.006 PMID:21333673
4. Schwabl H. Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA. 1993; 90:11446-11450. PMID: 8265571
5. Gil D. Hormones in avian eggs: Physiology, ecology and behavior. Adv Study Behav. 2008; 38: 337-398.
6. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev. 2005; 29: 329-352. PMID: 15811503
7. Balthazart J, Adkins-Regan E. Sexual differentiation of brain and behaviour in birds. In: Pfaff DW, Arnold AP, Fahrbach SE, Etgen AM, Rubin RT, editors. Hormones, Brain and Behavior. San Diego: Academic Press; 2002. pp. 223-301.
8. Carere C, Balthazart J. Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Endocrinol Metab. 2007; 18:73-80. PMID: 17276694
9. Badyaev AV. Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol. 2002; 17: 369-378.
10. Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H. Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J Anim Ecol. 2005; 74: 675-682.
11. Tschirren B, Richner H, Schwabl H. Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc R Soc B. 2004; 271:1371-1375. PMID: 15306335
12. Griffiths R, Double MC, Orr K, Dawson RJG. A DNA test to sex most birds. Mol Ecol. 1998; 7:1071-1075. PMID: 9711866
13. Tschirren B, Fitze PS, Richner H. Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. J Anim Ecol. 2003; 72: 839-845.
14. Bates D, Maechler M, BolkerB(2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42.
15. Lande R, Arnold SJ. The measurement of selection on correlated characters. Evolution. 1983; 37: 1210-1226.
16. Stinchcombe JR, Agrawal AF, Hohenlohe PA, Arnold SJ, Blows MW. Estimating nonlinear selection gradients using quadratic regression coefficients: Double or nothing? Evolution. 2008; 62: 2435-2440. doi: 10.1111/j.1558-5646.2008.00449.x PMID: 18616573
17. Lovich JE, Gibbons JW. A review of techniques for quantifying sexual size dimorphism Growth Dev Aging. 1992; 56: 269-281. PMID: 1487365
18. Dunning JB. Handbook of Avian Body Masses. Boca Raton, FL: CRC Press; 2007.
19. R Development Core Team. R: A language and environment for statistical computing. 2011. Available: http://www.R-project.org.
20. Sockman KW, Weiss J, Webster MS, Talbott V, Schwabl H. Sex-specific effects of yolk-androgens on growth of nestling American kestrels. Behav Ecol Sociobiol. 2008; 62: 617-625.
21. Saino N, Ferrari RP, Romano M, Martinelli R, Lacroix A, Gil D, et al. Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters. Behav Ecol. 2006; 17:172-181.
22. Schwabl H. Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A. 1996; 114: 271-276.
23. Müller W, Vergauwen J, Eens M. Yolk testosterone, postnatal growth and song in male canaries. Horm Behav. 2008; 54:125-133. doi: 10.1016/j.yhbeh.2008.02.005 PMID: 18353330
24. Müller W, Vergauwen J, Eens M. Long-lasting consequences of elevated yolk testosterone levels on female reproduction. Behav Ecol Sociobiol. 2009; 63: 809-816.
25. Müller W, Boonen S, Groothuis TGG, Eens M. Maternal yolk testosterone in canary eggs: toward a better understanding of mechanisms and function. Behav Ecol. 2010; 21: 493-500.
26. Pitala N, Ruuskanen S, Laaksonen T, Doligez B, Tschirren B, Gustafsson L. The effects of experimentally manipulated yolk androgens on growth and immune function of male and female nestling collared flycatchers Ficedula albicollis. J Avian Biol. 2009; 40: 225-230.
27. Ruuskanen S, Doligez B, Pitala N, Gustafsson L, Laaksonen T. Long-term fitness consequences of high yolk androgen levels: sons pay the costs. Funct Ecol. 2012; 26: 884-894.
28. Ruuskanen S, Doligez B, Gustafsson L, Laaksonen T. Long-term effects of yolk androgens on pheno-typeand parental feeding behavior in a wild passerine. Behav Ecol Sociobiol. 2012; 66:1201-1211.
29. Rice AM, Vallin N, Kulma K, Arntsen H, Husby A, Tobler M, et al. Optimizing the trade-off between offspring number and quality in unpredictable environments: Testing the role of differential androgen transfer to collared flycatcher eggs. Horm Behav. 2013; 63: 813-822. doi: 10.1016/j.yhbeh.2013.03. 019 PMID: 23602767
30. Benowitz-Fredericks ZM, Hodge M. Yolk androstenedione in domestic chicks (Gallus gallus domesti-cus): Uptake and sex-dependent alteration of growth and behavior. Gen Comp Endocrinol. 2013; 193: 48-55. doi: 10.1016/j.ygcen.2013.07.005 PMID: 23871777
31. Schwabl H, Holmes D, Strasser R, Scheuerlein A. Embryonic exposure to maternal testosterone influences age-specific mortality patterns in a captive passerine bird. Age. 2012; 34: 87-94. doi: 10.1007/s11357-011-9222-8 PMID: 21409557
32. Ruuskanen S, Laaksonen T. Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca). Horm Behav. 2010; 57:119-127. doi: 10.1016/j.yhbeh.2009.09.017 PMID: 19804778
33. Müller W, Deptuch K, Lopez-Rull I, Gil D. Elevated yolk androgen levels benefit offspring development in a between-clutch context. Behav Ecol. 2007; 18: 929-936.
34. Muriel J, Perez-Rodriguez L, Puerta M, Gil D. Differential effects of yolk testosterone and androstenedione in embryo development and nestling growth in the spotless starling (Sturnus unicolor). Gen Comp Endocrinol. 2013; 194:175-182. doi: 10.1016/j.ygcen.2013.09.013 PMID: 24090611
35. Rubolini D, Romano M, Martinelli R, Saino N. Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behav Ecol Sociobiol. 2006; 59: 344-352.
36. von Engelhardt N, Carere C, Dijkstra C, Groothuis TGG. Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc R Soc B. 2006; 273: 65-70. PMID: 16519236
37. Boncoraglio G, Groothuis TGG, von Engelhardt N. Differential maternal testosterone allocation among siblings benefits both mother and offspring in the Zebra Finch Taeniopygia guttata. Am Nat. 2011; 178: 64-74. doi: 10.1086/660278 PMID: 21670578
38. Kempenaers B, Verheyen GR, van der Broeckhoven C, Dhondt AA. Extra-pair paternity results from female preference for high-quality males in blue tit. Nature. 1992; 357: 494496.