Abstract
Although high testosterone (T) levels inhibit paternal behaviour in birds breeding in temperate zones many paternal mammals have a very different breeding biology, characterized by a post-partum oestrus. In species with post-partum oestrus, males may engage in T-dependent behaviours such as aggression and copulation simultaneously with paternal behaviour. We previously found that T promotes paternal behaviour in the California mouse, Peromyscus californicus. We examine whether this effect is mediated by the conversion of T to oestradiol (E(2)) by aromatase. In the first experiment, gonadectomized males treated with T or E(2) implants showed higher levels of huddling and pup grooming behaviour than gonadectomized males treated with dihydrotestosterone or empty implants. In the second experiment, we used an aromatase inhibitor (fadrozole) (FAD) to confirm these results. Gonadectomized males treated with T + vehicle or E(2) + FAD showed higher levels of huddling and pup grooming behaviour than gonadectomized males treated with T + FAD or empty implants. Although E(2) is known to promote the onset of maternal behaviour to our knowledge our results are the first to demonstrate that E(2) can promote paternal behaviour in a paternal mammal. These results may explain how mammals express paternal behaviour while T levels are elevated.
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- Bentvelsen F. M., McPhaul M. J., Wilson C. M., Wilson J. D., George F. W. Regulation of immunoreactive androgen receptor in the adrenal gland of the adult rat. Endocrinology. 1996 Jul;137(7):2659–2663. doi: 10.1210/endo.137.7.8770883. [DOI] [PubMed] [Google Scholar]
- Berg S. J., Wynne-Edwards K. E. Changes in testosterone, cortisol, and estradiol levels in men becoming fathers. Mayo Clin Proc. 2001 Jun;76(6):582–592. doi: 10.4065/76.6.582. [DOI] [PubMed] [Google Scholar]
- Bester-Meredith J. K., Young L. J., Marler C. A. Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav. 1999 Aug;36(1):25–38. doi: 10.1006/hbeh.1999.1522. [DOI] [PubMed] [Google Scholar]
- Brown R. E., Murdoch T., Murphy P. R., Moger W. H. Hormonal responses of male gerbils to stimuli from their mate and pups. Horm Behav. 1995 Dec;29(4):474–491. doi: 10.1006/hbeh.1995.1275. [DOI] [PubMed] [Google Scholar]
- Clancy A. N., Michael R. P. Effects of testosterone and aromatase inhibition on estrogen receptor-like immunoreactivity in male rat brain. Neuroendocrinology. 1994 Jun;59(6):552–560. doi: 10.1159/000126705. [DOI] [PubMed] [Google Scholar]
- Clark M. M., Galef B. G., Jr A testosterone-mediated trade-off between parental and sexual effort in male mongolian gerbils (Meriones unguiculatus). J Comp Psychol. 1999 Dec;113(4):388–395. doi: 10.1037/0735-7036.113.4.388. [DOI] [PubMed] [Google Scholar]
- Clark M. M., Galef B. G., Jr Effects of experience on the parental responses of male Mongolian gerbils. Dev Psychobiol. 2000 Apr;36(3):177–185. doi: 10.1002/(sici)1098-2302(200004)36:3<177::aid-dev1>3.0.co;2-w. [DOI] [PubMed] [Google Scholar]
- Dixson A. F., George L. Prolactin and parental behaviour in a male New World primate. Nature. 1982 Oct 7;299(5883):551–553. doi: 10.1038/299551a0. [DOI] [PubMed] [Google Scholar]
- Fleming A. S., Vaccarino F., Luebke C. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol Behav. 1980 Nov;25(5):731–743. doi: 10.1016/0031-9384(80)90377-7. [DOI] [PubMed] [Google Scholar]
- French J. A., Abbott D. H., Scheffler G., Robinson J. A., Goy R. W. Cyclic excretion of urinary oestrogens in female tamarins (Saguinus oedipus). J Reprod Fertil. 1983 May;68(1):177–184. doi: 10.1530/jrf.0.0680177. [DOI] [PubMed] [Google Scholar]
- Gubernick D. J., Alberts J. R. The biparental care system of the California mouse, Peromyscus californicus. J Comp Psychol. 1987 Jun;101(2):169–177. [PubMed] [Google Scholar]
- Gubernick D. J., Nelson R. J. Prolactin and paternal behavior in the biparental California mouse, Peromyscus californicus. Horm Behav. 1989 Jun;23(2):203–210. doi: 10.1016/0018-506x(89)90061-5. [DOI] [PubMed] [Google Scholar]
- Hutchison R. E., Hutchison J. B., Steimer T., Steel E., Powers J. B., Walker A. P., Herbert J., Hastings M. H. Brain aromatization of testosterone in the male Syrian hamster: effects of androgen and photoperiod. Neuroendocrinology. 1991 Feb;53(2):194–203. doi: 10.1159/000125718. [DOI] [PubMed] [Google Scholar]
- Jones J. S., Wynne-Edwards K. E. Paternal hamsters mechanically assist the delivery, consume amniotic fluid and placenta, remove fetal membranes, and provide parental care during the birth process. Horm Behav. 2000 Mar;37(2):116–125. doi: 10.1006/hbeh.1999.1563. [DOI] [PubMed] [Google Scholar]
- Kirkpatrick B., Kim J. W., Insel T. R. Limbic system fos expression associated with paternal behavior. Brain Res. 1994 Sep 26;658(1-2):112–118. doi: 10.1016/s0006-8993(09)90016-6. [DOI] [PubMed] [Google Scholar]
- Lonstein J. S., De Vries G. J. Sex differences in the parental behaviour of adult virgin prairie voles: independence from gonadal hormones and vasopressin. J Neuroendocrinol. 1999 Jun;11(6):441–449. doi: 10.1046/j.1365-2826.1999.00361.x. [DOI] [PubMed] [Google Scholar]
- McNeilly A. S., Abbott D. H., Lunn S. F., Chambers P. C., Hearn J. P. Plasma prolactin concentrations during the ovarian cycle and lactation and their relationship to return of fertility post partum in the common marmoset (Callithrix jacchus). J Reprod Fertil. 1981 Jul;62(2):353–360. doi: 10.1530/jrf.0.0620353. [DOI] [PubMed] [Google Scholar]
- Numan M., Numan M. J., English J. B. Excitotoxic amino acid injections into the medial amygdala facilitate maternal behavior in virgin female rats. Horm Behav. 1993 Mar;27(1):56–81. doi: 10.1006/hbeh.1993.1005. [DOI] [PubMed] [Google Scholar]
- Nunes S., Fite J. E., Patera K. J., French J. A. Interactions among paternal behavior, steroid hormones, and parental experience in male marmosets (Callithrix kuhlii). Horm Behav. 2001 Feb;39(1):70–82. doi: 10.1006/hbeh.2000.1631. [DOI] [PubMed] [Google Scholar]
- Orpen B. G., Fleming A. S. Experience with pups sustains maternal responding in postpartum rats. Physiol Behav. 1987;40(1):47–54. doi: 10.1016/0031-9384(87)90184-3. [DOI] [PubMed] [Google Scholar]
- Reburn C. J., Wynne-Edwards K. E. Hormonal changes in males of a naturally biparental and a uniparental mammal. Horm Behav. 1999 Apr;35(2):163–176. doi: 10.1006/hbeh.1998.1509. [DOI] [PubMed] [Google Scholar]
- Roky R., Paut-Pagano L., Goffin V., Kitahama K., Valatx J. L., Kelly P. A., Jouvet M. Distribution of prolactin receptors in the rat forebrain. Immunohistochemical study. Neuroendocrinology. 1996 May;63(5):422–429. doi: 10.1159/000127067. [DOI] [PubMed] [Google Scholar]
- Roselli C. E., Horton L. E., Resko J. A. Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology. 1985 Dec;117(6):2471–2477. doi: 10.1210/endo-117-6-2471. [DOI] [PubMed] [Google Scholar]
- Roselli C. E., Stadelman H., Horton L. E., Resko J. A. Regulation of androgen metabolism and luteinizing hormone-releasing hormone content in discrete hypothalamic and limbic areas of male rhesus macaques. Endocrinology. 1987 Jan;120(1):97–106. doi: 10.1210/endo-120-1-97. [DOI] [PubMed] [Google Scholar]
- Rosenblatt J. S., Ceus K. Estrogen implants in the medial preoptic area stimulate maternal behavior in male rats. Horm Behav. 1998 Feb;33(1):23–30. doi: 10.1006/hbeh.1997.1430. [DOI] [PubMed] [Google Scholar]
- Rosenblatt J. S., Hazelwood S., Poole J. Maternal behavior in male rats: effects of medial preoptic area lesions and presence of maternal aggression. Horm Behav. 1996 Sep;30(3):201–215. doi: 10.1006/hbeh.1996.0025. [DOI] [PubMed] [Google Scholar]
- Roy B. N., Wynne-Edwards K. E. Progesterone, estradiol, and prolactin involvement in lactation, including lactation following a postpartum mating, in the Djungarian hamster (Phodopus campbelli). Biol Reprod. 1995 Apr;52(4):855–863. doi: 10.1095/biolreprod52.4.855. [DOI] [PubMed] [Google Scholar]
- Sakaguchi K., Tanaka M., Ohkubo T., Doh-ura K., Fujikawa T., Sudo S., Nakashima K. Induction of brain prolactin receptor long-form mRNA expression and maternal behavior in pup-contacted male rats: promotion by prolactin administration and suppression by female contact. Neuroendocrinology. 1996 Jun;63(6):559–568. doi: 10.1159/000127085. [DOI] [PubMed] [Google Scholar]
- Simerly R. B., Swanson L. W. Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J Comp Neurol. 1988 Apr 8;270(2):209–242. doi: 10.1002/cne.902700205. [DOI] [PubMed] [Google Scholar]
- Stern J. M., Lehrman D. S. Role of testosterone in progesterone-induced incubation behaviour in male ring doves (Streptopelia risoria). J Endocrinol. 1969 May;44(1):13–22. doi: 10.1677/joe.0.0440013. [DOI] [PubMed] [Google Scholar]
- Storey AE, Walsh CJ, Quinton RL, Wynne-Edwards KE. Hormonal correlates of paternal responsiveness in new and expectant fathers. Evol Hum Behav. 2000 Mar 1;21(2):79–95. doi: 10.1016/s1090-5138(99)00042-2. [DOI] [PubMed] [Google Scholar]
- Trainor B. C., Marler C. A. Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus). Horm Behav. 2001 Aug;40(1):32–42. doi: 10.1006/hbeh.2001.1652. [DOI] [PubMed] [Google Scholar]
- Wang Z., De Vries G. J. Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster). Brain Res. 1993 Dec 17;631(1):156–160. doi: 10.1016/0006-8993(93)91203-5. [DOI] [PubMed] [Google Scholar]
- Ziegler T. E., Snowdon C. T. Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus. Horm Behav. 2000 Nov;38(3):159–167. doi: 10.1006/hbeh.2000.1617. [DOI] [PubMed] [Google Scholar]
- Ziegler T. E., Wegner F. H., Carlson A. A., Lazaro-Perea C., Snowdon C. T. Prolactin levels during the periparturitional period in the biparental cotton-top tamarin (Saguinus oedipus): interactions with gender, androgen levels, and parenting. Horm Behav. 2000 Sep;38(2):111–122. doi: 10.1006/hbeh.2000.1606. [DOI] [PubMed] [Google Scholar]
- Zumpe D., Bonsall R. W., Michael R. P. Effects of the nonsteroidal aromatase inhibitor, fadrozole, on the sexual behavior of male cynomolgus monkeys (Macaca fascicularis). Horm Behav. 1993 Jun;27(2):200–215. doi: 10.1006/hbeh.1993.1015. [DOI] [PubMed] [Google Scholar]
- Zwain I. H., Yen S. S. Dehydroepiandrosterone: biosynthesis and metabolism in the brain. Endocrinology. 1999 Feb;140(2):880–887. doi: 10.1210/endo.140.2.6528. [DOI] [PubMed] [Google Scholar]