A polymorphism in the oestrogen receptor gene explains covariance between digit ratio and mating behaviour

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1698, 2010, Pages 3353-3361

  Forstmeier, Wolfgang ^a   Mueller, Jakob C ^a   Kempenaers, Bart ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

2D:4D; Finger length; HOX genes; Sex hormones; Sexual behaviour

Indexed keywords

BLOOD; COVARIANCE ANALYSIS; EMBRYONIC DEVELOPMENT; ESTROGENIC COMPOUND; GENE EXPRESSION; LIFE HISTORY TRAIT; LIMB; MATING BEHAVIOR; PASSERINE; PHYSIOLOGY; POLYMORPHISM; SEX HORMONE;

TAENIOPYGIA GUTTATA; VERTEBRATA;

EID: 77958147880     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.1007     Document Type: Article

References (56)

1. Abecasis, G. R., Cookson, W. O. C. & Cardon, L. R. 2000 Pedigree tests of transmission disequilibrium. Eur. J. Hum. Genet. 8, 545-551. (doi:10.1038/sj.ejhg. 5200494)
2. Abramovich, D. R. 1974 Human sexual differentiation: in-u-tero influences. J. Obstet. Gynaecol. Br. Commonw. 81, 448-453.
3. Adkins-Regan, E. 2009 Hormones and sexual differentiation of avian social behavior. Dev. Neurosci. 31, 342-350. (doi:10.1159/000216545)
4. Akbas, G. E., Song, J. & Taylor, H. S. 2004 A HOXA10 estrogen response element (ERE) is differentially regulated by 17 beta-estradiol and diethylstilbestrol (DES). J. Mol. Biol. 340, 1013-1023.
5. Backström, N. et al. 2010 The recombinational landscape of the zebra finch Taeniopygia guttata genome. Genome Res. 20, 485-495.
6. Balthazart, J., Taziaux, M., Holloway, K., Ball, G. F. & Cornil, C. A. 2009 Behavioral effects of brain-derived estrogens in birds. Trends Comp. Endocrinol. Neurobiol. 1163, 31-48.
7. Bates, D., Maechler, M. & Dai, B. 2008 lme4: linear mixed-effects models using S4 classes. R package v. 0999375-26. See http://r-forge.r-project. org/projects/lme4/.
8. Berenbaum, S. A., Bryk, K. K., Nowak, N., Quigley, C. A. & Moffat, S. 2009 Fingers as a marker of prenatal androgen exposure. Endocrinology 150, 5119-5124. (doi:10.1210/en.2009-0774)
9. Brana, F. 2008 Sex of incubation neighbours influences hatchling sexual phenotypes in an oviparous lizard. Oecologia 156, 275-280. (doi:10.1007/s00442- 008-0996-z)
10. Brown, W. M., Finn, C. J. & Breedlove, S. M. 2002a Sexual dimorphism in digit-length ratios of laboratory mice. Anat. Rec. 267, 231-234. (doi:10.1002/ar.10108)
11. Brown, W. M., Hines, M., Fane, B. A. & Breedlove, S. M. 2002b Masculinized finger length patterns in human males and females with congenital adrenal hyper-plasia. Horm. Behav. 42, 380-386. (doi:10.1006/hbeh. 2002.1830)
12. Burley, N. T. & Foster, V. S. 2004 Digit ratio varies with sex, egg order and strength of mate preference in zebra finches. Proc. R. Soc. Lond. B 271, 239-244. (doi:10.1098/rspb. 2003.2562)
13. Campbell, B. & Lack, E. 1985 A dictionary of birds. Calton, UK: Poyser.
14. Cermik, D., Selam, B. & Taylor, H. S. 2003 Regulation of HOXA-10 expression by testosterone in vitro and in the endometrium of patients with polycystic ovary syndrome. J. Clin. Endocrinol. Metabol. 88, 238-243. (doi:10.1210/jc.2002-021072)
15. Chang, J. L. 2008 Sexual dimorphism of the second-to-fourth digit length ratio (2D: 4D) in the strawberry poison dart frog (Oophaga pumilio) in Costa Rica. J. Herpetol. 42, 414-416. (doi:10.1670/07-153.1)
16. Chang, J. L., Doughty, S., Wade, J. & Lovern, M. B. 2006 Sexual dimorphism in the second-to-fourth digit length ratio in green anoles, Anolis carolinensis (Squamata: Polychrotidae), from the southeastern United States. Can. J. Zool. Rev. Can. Zool. 84, 1489-1494. (doi:10. 1139/Z06-144)
17. Cutler, G. B. 1997 The role of estrogen in bone growth and maturation during childhood and adolescence. J. Steroid Biochem. Mol. Biol. 61, 141-144. (doi:10.1016/S0960-0760(97)80005-2)
18. Daftary, G. S. & Taylor, H. S. 2006 Endocrine regulation of HOX genes. Endocr. Rev. 27, 331-355. (doi:10.1210/er. 2005-0018)
19. Dreiss, A. N., Navarro, C., de Lope, F. & Moller, A. P. 2008 Digit ratios, secondary sexual characters and condition in barn swallows Hirundo rustica. Behav. Ecol. 19, 16-21. (doi:10.1093/beheco/arm095)
20. Forstmeier, W. 2005 Quantitative genetics and behavioural correlates of digit ratio in the zebra finch. Proc. R. Soc. B 272, 2641-2649. (doi:10.1098/rspb.2005.3264)
21. Forstmeier, W., Coltman, D. W. & Birkhead, T. R. 2004 Maternal effects influence the sexual behavior of sons and daughters in the zebra finch. Evolution 58, 2574-2583.
22. 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)
23. Forstmeier, W., Rochester, J. & Millam, J. R. 2008 Digit ratio unaffected by estradiol treatment of zebra finch nestlings. Gen. Comp. Endocrinol. 156, 379-384. (doi:10.1016/j. ygcen.2008.01.007)
24. Galis, F., Ten Broek, C. M. A., Van Dongen, S. & Wijnaendts, L. C. D. 2010 Sexual dimorphism in the prenatal digit ratio (2D: 4D). Arch. Sexual Behav. 39, 57-62. (doi:10.1007/s10508-009-9485-7)
25. Groeneveld, E., Kovač, M. & Mielenz, N. 2008 VCE user's guide and reference manual: institute of farm animal genetics, Friedrich Loeffler Institute (FLI) Germany: Mariensee.
26. Hönekopp, J. & Watson, S. 2010 Meta-analysis of digit ratio 2D: 4D shows greater sex difference in the right hand. Am. J. Hum. Biol. (doi:10.1002/ajhb.21054).
27. Hönekopp, J., Bartholdt, L., Beier, L. & Liebert, A. 2007 Second to fourth digit length ratio (2D: 4D) and adult sex hormone levels: new data and a meta-analytic review. Psychoneuroendocrinology 32, 313-321. (doi:10. 1016/j.psyneuen.2007.01.007)
28. Jü rimäe, T., Voracek, M., Jürimäe, J., Lätt, E., Haljaste, K., Saar, M. & Purge, P. 2008 Relationships between finger-length ratios, ghrelin, leptin, IGF axis, and sex steroids in young male and female swimmers. Eur. J. Appl. Physiol. 104, 523-529. (doi:10.1007/s00421- 008-0801-z)
29. Kondo, T., Zakany, J., Innis, J. W. & Duboule, D. 1997 Of fingers, toes and penises. Nature 390, 29-29. (doi:10.1038/36234)
30. Leoni, B., Canova, L. & Saino, N. 2005 Sexual dimorphism in metapodial and phalanges length ratios in the wood mouse. Anat. Rec. Part Discov. Mol. Cell. Evol. Biol. 286A, 955-961. (doi:10.1002/ar.a.20226)
31. Lutchmaya, S., Baron-Cohen, S., Raggatt, P., Knickmeyer, R. & Manning, J. T. 2004 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Hum. Dev. 77, 23-28. (doi:10.1016/j.earlhumdev.2003.12.002)
32. Lynch, M. & Walsh, B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Association.
33. Malas, M. A., Dogan, S., Evcil, E. H. & Desdicioglu, K. 2006 Fetal development of the hand, digits and digit ratio (2D: 4D). Early Hum. Dev. 82, 469-475. (doi:10. 1016/j.earlhumdev.2005.12.002)
34. Manning, J. T. 2002 Digit ratio: a pointer to fertility, behavior, and health. New Brunswick, NJ: Rutgers University Press.
35. Manning, J. T., Scutt, D., Wilson, J. & Lewis-Jones, D. I. 1998 The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Hum. Reprod. 13, 3000-3004. (doi:10.1093/humrep/13.11.3000)
36. Manning, J. T., Bundred, P. E., Newton, D. J. & Flanagan, B. F. 2003 The second to fourth digit ratio and variation in the androgen receptor gene. Evol. Hum. Behav. 24, 399-405. (doi:10.1016/S1090-5138(03)00052-7)
37. McIntyre, M. H. 2006 The use of digit ratios as markers for perinatal androgen action. Reprod. Biol. Endocrinol. 4, 10.(doi:10.1186/1477-7827-4-10)
38. Medland, S. E., Loehlin, J. C. & Martin, N. G. 2008 No effects of prenatal hormone transfer on digit ratio in a large sample of same- and opposite-sex dizygotic twins. Pers. Indiv. Differ. 44, 1225-1234. (doi:10.1016/j.paid. 2007.11.017)
39. Navarro, C., de Lope, F. & Moller, A. P. 2007 Digit ratios (2D: 4D), secondary sexual characters and cell-mediated immunity in house sparrows Passer domesticus. Behav. Ecol. Sociobiol. 61, 1161-1168. (doi:10.1007/s00265-006-0329- 3)
40. Okten, A., Kalyoncu, M. & Yaris, N. 2002 The ratio of second- and fourth-digit lengths and congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Early Hum. Dev. 70, 47-54. (doi:10.1016/S0378-3782(02)00073-7)
41. Oz, O. K., Millsaps, R., Welch, R., Birch, J. & Zerwekh, J. E. 2001 Expression of aromatase in the human growth plate. J. Mol. Endocrinol. 27, 249-253. (doi:10.1677/jme.0.0270249)
42. Reyes, F. I., Borodits, R. S., Winter, J. S. D. & Faiman, C. 1974 Studies on human sexual development. 2. Fetal and maternal serum gonadotropin and sex steroid concentrations. J. Clin. Endocrinol. Metabol. 38, 612-617. (doi:10.1210/jcem-38-4-612)
43. Rochira, V., Granata, A. R. M., Madeo, B., Zirilli, L., Rossi, G. & Carani, C. 2005 Estrogens in males: what have we learned in the last 10 years? Asian J. Androl. 7, 3-20. (doi:10.1111/j.1745-7262.2005.00018.x)
44. Rodeck, C. H., Gill, D., Rosenberg, D. A. & Collins, W. P. 1985 Testosterone levels in midtrimester maternal and fetal plasma and amniotic-fluid. Prenat. Diagn. 5, 175-181. (doi:10.1002/pd.1970050303)
45. Romano, M., Rubolini, D., Martinelli, R., Bonisoli-Alquati, A. & Saino, N. 2005 Experimental manipulation of yolk testosterone affects digit length ratios in the ring-necked pheasant (Phasianus colchicus). Horm. Behav. 48, 342-346. (doi:10.1016/j.yhbeh.2005.03.007)
46. Rubolini, D., Pupin, F., Sacchi, R., Gentilli, A., Zuffi, M. A. L., Galeotti, P. & Saino, N. 2006 Sexual dimorphism in digit length ratios in two lizard species. Anat. Rec. Part Discov. Mol. Cell. Evol. Biol. 288A, 491-497. (doi:10.1002/ar.a.20323)
47. Saino, N., Rubolini, D., Romano, M. & Boncoraglio, G. 2007 Increased egg estradiol concentration feminizes digit ratios of male pheasants (Phasianus colchicus). Naturwissenschaften 94, 207-212. (doi:10.1007/s00114-006-0188-9)
48. Schielzeth, H. & Forstmeier, W. 2009 Conclusions beyond support: overconfident estimates in mixed models. Behav. Ecol. 20, 416-420. (doi:10.1093/beheco/arn145)
49. Sobel, E., Sengul, H. & Weeks, D. E. 2001 Multipoint estimation of identity-by-descent probabilities at arbitrary positions among marker loci on general pedigrees. Hum. Hered. 52, 121-131. (doi:10.1159/000053366)
50. Talarovičová, A., Kršková, L. & Blažeková, J. 2009 Testosterone enhancement during pregnancy influences the 2D: 4D ratio and open field motor activity of rat siblings in adulthood. Horm. Behav. 55, 235-239. (doi:10.1016/j.yhbeh.2008.10.010)
51. Tan, U. 2008 Ratio of fourth to second fingertip extensions in relation to serum estradiol and testosterone levels in men and women. Percept. Mot. Skills 107, 3-13. (doi:10. 2466/PMS.107.5.3-13)
52. Taylor, H. S., Arici, A., Olive, D. & Igarashi, P. 1998 HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J. Clin. Invest. 101, 1379-1384.
53. von Engelhardt, N., Henriksen, R. & Groothuis, T. G. G. 2009 Steroids in chicken egg yolk: metabolism and uptake during early embryonic development. Gen. Comp. Endocrinol. 163, 175-183. (doi:10.1016/j.ygcen. 2009.04.004)
54. Wallen, K. 2009 Does finger fat produce sex differences in second to fourth digit ratios? Endocrinology 150, 4819-4822. (doi:10.1210/en.2009-0986)
55. Walters, M. J., Collado, D. & Harding, C. F. 1991 Estrogenic modulation of singing in male Zebra finches: differential-effects on directed and undirected songs. Anim. Behav. 42, 445-452. (doi:10.1016/S0003-3472(05) 80043-0)
56. Wilson, J. D. 2001 Androgens, androgen receptors, and male gender role behavior. Horm. Behav. 40, 358-366. (doi:10.1006/hbeh.2001.1684)