Increased serotonin concentration and tryptophan hydroxylase activity in reproductive organs of copulator males: a case of adaptive plasticity

Abstract

Individual male rats may systematically display or not copulatory behavior when paired with receptive females. Although these phenotypes are associated with differences in brain organization and function, they might also do so at the level of the reproductive organs. We then used high performance liquid chromatography to quantify serotonin concentration and the activity of tryptophan hydroxylase in the reproductive organs of copulator and non-copulator males. Sexual behavior display was compared between groups and parameters of fertility and reproductive fitness were determined for copulator males. Copulator males had higher concentrations of serotonin in the epididymis, testicle and ventral prostate than their non-copulator counterparts, as it was found for epididymal and testicular tryptophan hydroxylase activity. However, preliminary data shows that serotonin elevation occurs in copulator males only until they have accumulated several sexual encounters, so it might be a response to genital gratification or sexual rewarding. Interestingly, only epididymal serotonin concentration correlated with reproductive fitness, offspring number, mating success and seminal plug volume in copulator males. Our results support that copulator and non-copulator male rats feature a phenotype-specific serotoninergic tone in the epididymis, testicle and ventral prostate gland. The observation documenting that epididymal serotonin concentration correlated with parameters that monitor male fertility and reproductive fitness in copulator males predicts that epididymal factors increase their chances of parenting offspring.

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Pichardo, A. , Tlachi-López, J. , Jiménez-Trejo, F. , Fuentes-Farías, A. , Báez-Saldaña, A. , Molina-Cerón, M. , Manjarréz-Gutiérrez, G. , Gutiérrez-Ospina, G. and Lucio, R. (2011) Increased serotonin concentration and tryptophan hydroxylase activity in reproductive organs of copulator males: a case of adaptive plasticity. Advances in Bioscience and Biotechnology, 2, 75-84. doi: 10.4236/abb.2011.22012.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Pfaus, J.G., Kippin, T.E. and Centeno, S. (2001) Condi-tioning and sexual behavior: A review. Hormones and Behavior, 40, 291-321. doi:10.1006/hbeh.2001.1686
[2] Whalen, R.E., Beach, F.A. and Kuehn, R.E. (1961) Ef-fects of exogenous androgens of sexually responsive and unresponsive male rats. Endocrinology, 69, 373-380. doi:10.1210/endo-69-2-373
[3] Portillo, W. and Paredes, R.G. (2003) Sexual and olfac-tory preference in non copulating male rats. Physiology and Behavior, 80, 155-162. doi:10.1016/S0031-9384(03)00231-2
[4] Portillo, W. and Paredes, R.G. (2004) Sexual incentive motivation, olfactory preference and activation of the vomeronasal projection pathway by sexually relevant cues in non-copulating and naive male rats. Hormones and Behavior, 46, 330-340. doi:10.1016/j.yhbeh.2004.03.001
[5] Portillo, W., Diaz, N.F., Cabrera, E.A., Fernandez-Guasti A. and Paredes, R.G. (2006) Comparative analysis of in-munoreactive cells for androgen receptors and oestrogen receptor α in copulating and non copulating male rats. Journal of Neuroendocrinology, 18, 168-176. doi:10.1111/j.1365-2826.2005.01401.x
[6] Portillo, W., Castillo, C.G., Retana-Márquez, S., Roselli, C.E. and Paredes, R.G. (2007) Neuronal activity of aro-matase enzyme in non copulatory male rats. Journal of Neuroendocrinology, 19, 139-141. doi:10.1111/j.1365-2826.2006.01513.x
[7] Jiménez-Trejo, F., Tapia-Rodríguez, M., Queiroz, D.B., Padilla, P., Avellar, M. C., Manzano, P.R., Manjarrez, G. and Gutiérrez-Ospina, G. (2007) Serotonin concentration synthesis cell origin and targets in the rat caput epidi-dymis during sexual maturation and variations associated whit adult mating status: Morphological and biochemical studies. Journal of Andrology, 28, 136-149.
[8] Frungeri, M.B., Gonzalez-Calvar, S.I., Rubio, M., Ozu, M., Lustig, L. and Calandras, R.S. (1999) Serotonin in golden hamster testes: Testicular levels, inmunolocaliza-tion and role during sexual development and photoperi-odic regression-recrudescence transition. Neuroendocri-nology, 69, 299-308. doi:10.1159/000054431
[9] Chaturvedi, C.M. and Singh, A.B. (1992) Suppression of annual testicular development in Indian palm squirrel, Funambulus pennati by 8 hrs temporal relationship of serotonin and dopamine precursor drugs. Journal of Neural Transmission, 88, 53-60.
[10] doi:10.1007/BF01245036 Kim, S.W. and Paick, J.S. (2004) Peripheral effects of serotonin on the contractile responses of rat seminal ve-sicles and vasa deferentia. Journal of Andrology, 25, 893- 899.
[11] Piner, J., Sutherland, M., Millar, M., Turner, K., Newall, D. and Sharpe, R.M. (2002) Changes in vascular dynam-ics of the adult rat testis leading to transient accumulation of seminiferous tubule fluid after administration of a novel 5-hidroxycriptamine (5-HT) agonist. Reproductive Toxicology, 16, 141-150. doi:10.1016/S0890-6238(02)00008-4
[12] Leung, G.P., Dun, S.L., Dun, N.J. and Wong, P.Y. (1999) Serotonin via 5-HT1B and 5-HT2B receptors stimulates anion secretion in the rat epididimal epithelium. Journal of Physiology, 519, 657-667. doi:10.1111/j.1469-7793.1999.0657n.x
[13] Killam, A.L., Watts, S.W. and Cohen, M.L. (1995) Role of the alpha 1-adrenoreceptors and 5-HT2 receptors in serotonin-induced contraction of rat prostate: Autoradio-graphical and functional studies. European Journal of Pharmacology, 273, 7-14. doi:10.1016/0014-2999(94)00613-C
[14] Gerendai, I., Banzerowski, P., Csernus, V. and Halasz, B. (2007) Innervation and serotoninergic receptors of the testis interact with local action of interleukin-1beta on steroidogenesis. Autonomic Neuroscience, 131, 21-27. doi:10.1016/j.autneu.2006.06.002
[15] Das, T.K., Mazumder, R. and Biswas, N.M. (1982) Spermatogenesis in rat: Effect of L-typtophan loading. Andrologia, 14, 242-249.
[16] Lucio, R.A., Tlachi, J.L., López, A.A., Zempoalteca, R. and Velázquez-Moctezuma, J. (2009) Analisis of the pa-rameters of the ejaculate in the laboratory wistar rat: Technical description. Veterinaria México, 40, 205-215.
[17] Lucio, R.A., Manzo, J., Martínez-Gómez, M., Sachs, B.D. and Pacheco, P. (1994) Participation of pelvic nerve in male rat copulatory behavior. Physiology and Behavior, 55, 241-246. doi:10.1016/0031-9384(94)90129-5
[18] Portillo, W. and Paredes, R.G. (2009) Conditioned place preference induced by morphine in non-copulating male rats. Behavioral Brain Research, 203, 308-311.
[19] Ramm, S.A. and Stockley, P. (2009) Adaptative plasticity of mammalian spremproduction in response to social experience. Proceedings of the Royal Society B: Biologi-cal Sciences, 276, 741-755. doi:10.1016/j.bbr.2009.04.037
[20] Lemaitre, J.F., Ramm, S.A., Horst, J.L. and Stockley, P. (2010) Social cues of sperm competition influence ac-cessory reproductive gland size in a promiscuous mam-mal. Proceedings of the Royal Society B: Biological Sci-ences, Epub ahead of print. http://rspb.royalsocietypiblishing.org/conten/early/2010/09/24/rspb..1828.long
[21] Jones, R.C. (1998) Evolution of the vertebrate epidi-dymis. Journal of Reproduction and Fertility Supplement, 53, 163-182.
[22] Rodríguez, R., Pozuelo, J. M., Martin, R., Henriques-Gil, N., Haro, M., Arriazu, R. and Santamaria, L. (2003) Presence of neuroendocrine cells during postnatal devel-opment in rat prostate: Immunohistochemical, molecular and quantitative study. Prostate, 57, 176-185.
[23] Di Sant’Agnese, P.A., Davis, N.S., Chen, M. and De Mesy Jensen, K.L. (1987) Age-related changes in the neuroendocrine (endocrine-paracrine) cell population and the serotonin content of the guinea pig prostate. Labora-tory Investigation, 57, 729-736.
[24] Mathews, M. and Adler, N.T. (1977) Facilitative and inhibitory influences of reproductive behavior on sperm transport in rats. Journal of Comparative and Physio-logical Psychology, 91, 727-741. doi:10.1037/h0077364
[25] Carballada, R. and Esponda, P. (1992) Role of fluid from seminal vesicles and coagulating glands in sperm trans-port into the uterus and fertility in rats. Journal of Re-production and Fertility, 95, 639-648. doi:10.1530/jrf.0.0950639
[26] Cukierski, M.A., Sina, J.L., Prahalada, S. and Robertson, R.T. (1991) Effects of seminal vesicle and coagulating gland ablation on fertility in rats. Reproductive Toxicol-ogy, 5, 347-352. doi:10.1016/0890-6238(91)90093-U
[27] Jones, R.C., Dacheux, J.L., Nixon, B. and Ecroyd, H.W. (2007) Role of the epididymis in sperm competition. Asian Journal of Andrology, 9, 493-499. doi:10.1111/j.1745-7262.2007.00284.x
[28] Zhou, Y., Zheng, M., Shi, Q., Zhang, L., Zhen, W., Chen, W. and Zhang, Y. (2008) An epididymis-specific secre-tory protein hongrES1 critically regulates sperm capaci-tation and male fertility. PLoS ONE, 3, 12. doi:10.1371/journal.pone.0004106
[29] Leung, G.P., Dun, S.L., Dun, N.J. and Wong, P.Y. (1999) Serotonin via 5-HT1B and 5-HT2B receptors stimulates anion secretion in the rat epididymal epithelium. The Journal of Physiology, 519, 657-670. doi:10.1111/j.1469-7793.1999.0657n.x
[30] Parisi, E., De Prisco, P., Capasso, A. and Del Prete, M. (1984) Serotonin and sperm motility. Cell Biology Inter-national Reports, 8, 95.
[31] Waldinger, M.D., Berendsen, H.H.G., Blok, B.F.M., Olivier, B. and Holstege, G. (1998) Premature ejaculation and serotonergic antidepressants-induced delayed ejacu-lation: the involvement of the serotonergic system. Be-havioral Brain Research, 92, 111-118. doi:10.1016/S0166-4328(97)00183-6
[32] Wilson, N., Tubman, S.C., Eady, P.E. and Robertson, G.W. (1997) Female genotype affects male success in sperm competition. Proceedings of the Royal Society B: Biological Sciences, 264, 1491-1495. doi:10.1098/rspb.1997.0206
[33] Ball, M.A. and Parker, G.A (2003) Sperm competition games: sperm selection by females. Journal of Theoreti-cal Biology, 224, 27-42. doi:10.1530/rep.1.00598
[34] Coria-ávila, G.A., Jones, S.L., Solomon, C.E., Gavrila, A.M., Jordan, G.J. and Pfaus, J.G. (2006) Conditioned partner preference in female rats for strain of male. Physiology and Behavior, 88, 529-537.
[35] Aragon, M.A., Ayala, M.E., Marin, M., Aviles, Da-mian-Matsumara, A.P. and Rodriguez, R. (2005) Sero-toninergic system blockage in the prepubertal rat inhibits spermatogenesis development. Reproduction, 129, 717- 727.
[36] Csaba, C., Csernus, V. and Gerendai, I. (1998) Intrates-ticular serotonin affects stereidogenesis in the rat testis. Journal of Neuroendocrinology, 10, 371-376.
[37] Frungieri, M.B., Zita, K., Pignataro, O.P., Gonzalez- Calvar, S.I. and Calandra, R.S. (2002) Interactions be-tween testicular serotoninergic, catecolaminergic and corticotropi-releasing hormone systems modulating cAMP and testosterone production in the Golden Hamster. Neu- roendocrinology, 76, 35-46. doi:10.1159/000063682
[38] Cheng, C.Y. and Mruk, D.D. (2010) A local autocrine axis in the testes that regulates spermatogenesis. Nature Reviews Endocrinology, 6, 380-395. doi:10.1038/nrendo.2010.71
[39] Buvat, J., Maggi, M., Gooren, L., Gudy, A.T., Kaufman, J., Morgentaler, A., Schulman, C., Tan, H.M., Torres, L.O., Yassin, A. and Zitzmann, M. (2010) Endocrine aspects of male sexual dysfunctions. Journal of Sex Medicine, 7, 1627-1656. doi:10.1111/j.1743-6109.2010.01780.x

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