A broad variability of yolk androgen levels is considered as an important source of adaptive phenotypic plasticity. This variability of maternal androgen deposition is explained by environmental variation and also by genetic differences among avian mothers. We experimentally investigated such heritable variation of testosterone (T) levels in the egg through the bidirectional selection of Japanese quail. The response to selection for yolk T concentrations was evaluated in downward (low egg T, LET) and upward (high egg T, HET) directions over five generations. Moreover, the correlative response of circulating sex steroids to selection was examined by a comparison of plasma T and estradiol levels between the HET and LET females. We observed a distinct pattern of the response to selection in the HET and LET lines with the stronger response occurring in the upward direction and a limited potential for selection in the downward direction. In the HET line, the population mean increased more than double as compared to the initial population but it seems to be still below its plateau. The LET line reached the selection limit in the second generation suggesting that yolk T concentrations were close to their physiological minimum. Estradiol levels were higher in the circulation of the HET than LET females without changes in plasma T concentrations underlying specific control mechanisms for yolk and plasma hormone levels.
Adkins-ReganE., OttingerM. A., and ParkJ. (1995) Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J. Exp. Zool. Part A, 271, 466–470.
2.
CainK. E., and KettersonE. D. (2012) Competitive females are successful females; phenotype, mechanism and selection in a common songbird. Behav. Ecol. Sociobiol., 66, 241–252.
3.
CuccoM., GuascoB., MalacarneG., OttonelliR., and TanvezA. (2008) Yolk testosterone levels and dietary carotenoids influence growth and immunity of grey partridge chicks. Gen. Comp. Endocrinol., 156, 418–425.
4.
ElekonichM. M., and WingfieldJ. C. (2000) Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia). Ethology, 106, 493–510.
5.
FalconerD. S., and MackayT. F. C. (1996) Introduction to quantitative genetics, 4th edn. London: Longman.
6.
GaspariniJ., BoulinierT., GillV. A., GilD., HatchS. A., and RoulinA. (2007) Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird. J. Evol. Biol., 20, 874–880.
7.
GilD., and FaureJ. M. (2007) Correlated response in yolk testosterone levels following divergent genetic selection for social behaviour in Japanese quail. J. Exp. Zool. Part A, 307A, 91–94.
8.
GilD., MarzalA., de LopeF., PuertaM., and MollerA. P. (2006) Female house martins (Delichon urbica) reduce egg androgen deposition in response to a challenge of their immune system. Behav. Ecol. Sociobiol., 60, 96–100.
9.
GilD., BiardC., LacroixA., SpottiswoodeC. N., SainoN., PuertaM., and MollerA. P. (2007) Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism. Am. Nat., 169, 802–819.
10.
GroothuisT. G. G., and SchwablH. (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them?Philos. Trans. R. Soc. B, 363, 1647–1661.
11.
GroothuisT. G. G., MullerW., von EngelhardtN., CarereC., and EisingC. (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurisci. Biobehav. Rev., 29, 329–352.
12.
GuibertF., Richard-YrisM. A., LumineauS., KotrschalK., GuemeneD., BertinA., MostlE., and HoudelierC. (2010) Social instability in laying quail: consequences on yolk steroids and offspring's phenotype. PLoS One, 5, e14069.
13.
JohnsonA. L. (2000) Reproduction in the female. In: WhittowG.C. (ed.), Sturkie's avian physiology, 5th edn, pp. 569–596. Academic Press, New York.
14.
KatoM., ShimadaK., SaitoN., NodaK., and OhtaM. (1995) Expression of P450 17 alpha-hydroxylase and P450aromatase genes in isolated granulosa, theca interna, and theca externa layers of chicken ovarian follicles during follicular growth. Biol. Reprod., 52, 405–410.
15.
KingmaS. A., KomdeurJ., VedderO., von EngelhardtN., KorstenP., and GroothuisT. G. G. (2009) Manipulation of male attractiveness induces rapid changes in avian maternal yolk androgen deposition. Behav. Ecol., 20, 172–179.
16.
OkuliarovaM., SkrobanekP., and ZemanM. (2009) Variability of yolk testosterone concentrations during the reproductive cycle of Japanese quail. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 154, 530–534.
17.
OkuliarovaM., GroothuisT. G. G., SkrobanekP., and ZemanM. (2011) Experimental evidence for genetic heritability of maternal hormone transfer to offspring. Am. Nat., 177, 824–834.
18.
RangelP. L., RodriguezA., RojasS., SharpP. J., and GutierrezC. G. (2009) Testosterone stimulates progesterone production and STAR, P450 cholesterol side-chain cleavage and LH receptor mRNAs expression in hen (Gallus domesticus) granulosa cells. Reproduction, 138, 961–969.
19.
RutkowskaJ., CichonM., PuertaM., and GilD. (2005) Negative effects of elevated testosterone on female fecundity in zebra finches. Horm. Behav., 47, 585–591.
20.
SatterleeD. G., and JohnsonW. A. (1988) Selection of Japanese quail for contrasting blood corticosterone response to immobilization. Poult. Sci., 67, 25–32.
21.
StaubN. L., and De BeerM. (1997) The role of androgens in female vertebrates. Gen. Comp. Endocrinol., 108, 1–24.
22.
TanvezA., ParisotM., ChastelO., and LeboucherG. (2008) Does maternal social hierarchy affect yolk testosterone deposition in domesticated canaries?Anim. Behav., 75, 929–934.
23.
ToblerM., GranbomM., and SandellM. (2007) Maternal androgens in the pied flycatcher: timing of breeding and within-female consistency. Oecologia, 151, 731–740.
24.
TschirrenB., RichnerH., and SchwablH. (2004) Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc. R. Soc. B, 271, 1371–1375.
25.
TschirrenB., SendeckaJ., GroothuisT. G. G., GustafssonL., and DoligezB. (2009) Heritable Variation in Maternal Yolk Hormone Transfer in a Wild Bird Population. Am. Nat., 174, 557–564.
26.
VeigaJ. P., and PoloV. (2008) Fitness consequences of increased testosterone levels in female spotless starlings. Am. Nat., 172, 42–53.
27.
VerbovenN., MonaghanP., EvansD. M., SchwablH., EvansN., WhitelawC., and NagerR. G. (2003) Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proc. R. Soc. B270, 2223–2232.
28.
WolfJ. B., BrodieE. D.III, CheverudJ. M., MooreA. J., and WadeM. J. (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol. Evol., 13, 64–69.
29.
ZemanM., KosutzkyJ., and BobakovaE. (1986) Testosterone concentration in the seminal plasma of cocks. Brit. Poultry Sci., 27, 261–266.
30.
ZemanM., SkrobanekP., and OkuliarovaM. (2013) Genetic differences in yolk testosterone levels influence maternal hormone deposition in the second laying cycle in Japanese quails. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 164, 271–275.
