Endocrine correlates of partner preference behavior in rams.

We studied a unique group of rams that would not mate with estrous ewes during extensive testing for sexual behavior. The same rams courted males in preference to females in 30-min sexual preference tests and were classified as male-oriented (n = 6). We compared the following endocrine profiles: systemic steroid concentrations, the capacity of the testes to biosynthesize 17 alpha-hydroxyprogesterone and testosterone from 3H-progesterone in vitro, and the levels of brain aromatase activity (AA) in male-oriented rams vs. rams that were proven breeders and designated as female-oriented (n = 7). After the last behavioral test, sera were collected, and males in each experimental group were killed. Brains and testes were obtained for subsequent determinations of AA and measurements of steroidogenic enzyme activity. All dissections and subsequent assays were performed without knowledge of experimental group assignments. Serum concentration of testosterone (T), dihydrotestosterone (DHT), androstenedione, estrone (E1), and estradiol-17 beta (E2) were determined by RIA. AA was quantified by a 3H2O assay validated for neural tissue of the ram. We studied frontal, parietal and cingulate cortex, cerebellum, hippocampus, olfactory bulb, septum, amygdala, infundibulum-median eminence, and preoptic area (POA). Serum T, E1, and E2 concentrations of female-oriented subjects were significantly higher (p < 0.05) than those in male-oriented subjects (SEM: 1559 +/- 228, 46 +/- 2, and 15 +/- 3 pg/ml vs. 874 +/- 196, 40 +/- 2, and 8 +/- 1 pg/ml serum, respectively). DHT and androstenedione concentrations in the systemic circulation did not differ between groups. Likewise, biosynthesis of labeled T and 17 alpha-hydroxyprogesterone from 3H-progesterone by testicular homogenates in vitro was significantly higher (p < 0.05) in female-oriented than in male-oriented subjects (28.8 +/- 8.1 vs. 12.1 +/- 2.3 mumol.h-1.mg protein-1 for T and 416.9 +/- 100.8 vs. 186.3 +/- 30.7 mumol.h-1.mg protein-1 for 17 alpha-hydroxyprogesterone). The highest level of AA was found in the POA, which was significantly greater in female-oriented than in male-oriented rams (472 +/- 34 vs. 296 +/- 24 fmol 3H2O.h-1.mg protein-1, p < 0.05). AA in other brain areas did not differ between experimental groups. Our data suggest that the testes of the male-oriented ram have reduced capacity for T production. In other species, T controls in situ estrogen formation not only by providing substrate for aromatization but also by up-regulating P450arom mRNA in the POA. Because the POA is part of a neural circuitry that mediates male sexual behavior in many species, we hypothesize that the capacity for aromatization influences sexual orientation of these rams.