We studied the dynamics of steroid secretion during the luteal-placental shift of early pregnancy in rhesus monkeys. Daily blood samples were obtained from six pregnant rhesus monkeys during the cycle of conception and for the first 44 days of pregnancy to examine the relationships among aromatizable androgens, estrogens, progesterone (P), and CG in the peripheral circulation. To elucidate the biosynthetic mechanisms involved in the changes in hormonal patterns, minces of placentae and corpora lutea (CL) were incubated in vitro with [3H]pregnenolone ([3H]P5) and [3H]androstenedione ([3H]A), and steroid metabolites were isolated and identified by reverse isotope dilution. After a brief rise (corresponding to the approximate time of implantation of the blastocyst), serum P levels declined despite rising serum CG levels and reached a nadir at the time of maximal CG secretion. In contrast, serum androstenedione (A), testosterone (T), estrone (E1), and estradiol (E2) concentrations rose and fell in parallel with CG and reached peak levels near day 24 of pregnancy 2- to 10-fold higher than those during the luteal phase. The CL of early pregnancy produced less than one third as much P from [3H]P5 as did the CL of the cycle, but had a 9-fold greater capacity for estrogen biosynthesis. Total CL aromatase activity did not differ between the nonfertile cycle and early pregnancy. 17-Hydroxylase and C17-20 lyase activities increased in the CL during early pregnancy, since 17-hydroxyprogesterone and A (but not T) syntheses were 3- to 5-fold greater in the CL of early pregnancy than in the CL of the cycle. Although serum E1 and E2 concentrations during early pregnancy were similar, E1 was the predominant estrogen produced from [3H]P5 or [3H] A by luteal tissue in vitro. Placental tissue obtained on days 23-27 of pregnancy produced large amounts of P from [3H]P5, but only trace amounts of estrogens were formed from [3H]A. By day 45 of pregnancy, however, the placenta had acquired substantial amounts of aromatase activity. Neither estrogens nor androgens were formed from [3H]P5 by the placenta.(ABSTRACT TRUNCATED AT 400 WORDS)