Alterations in follicular maturation associated with within-breed variation in ovulation rate in Chios sheep

Within-breed comparisons may be helpful to identify, in a given genetic background (Chios sheep), ovarian strategies and control mechanisms associated with altered ovulation rate. High and low ewes were identified from two large groups (n = 27 and n = 33 in Exp. 1 and Exp. 2 respectively) of Chios ewes submitted to repeated laparoscopies (24 times in Exp. 1 and six times in Exp. 2). High ovulatory ewes (n = 6 and n = 7 in Exp. 1 and Exp. 2 respectively) had mean ovulation rates of 4.3 (Exp. 1) and 4.2 (Exp. 2) while low ovulatory ewes (n = 6 and n = 7 in Exp. 1 and Exp. 2 respectively) had mean ovulation rates of 2.5 (Exp. 1) and 1.9 (Exp. 2). In Exp. 1, follicular function was compared in these two groups of ewes using follicles obtained at 30 h following luteolysis in the same ewes before and after unilateral ovariectomy (ULO). In Exp. 2, circulating follicle stimulating hormone (FSH) concentrations were measured from the end of the luteal phase up to the preovulatory surge in high and low ewes. Thereafter, to demonstrate a causal link between high FSH and high ovulation rate, pituitary downregulation was achieved by a 17-day gonadotrophin releasing hormone (GnRH) agonist treatment and the ovarian response to similar amounts of exogenous gonadotrophins compared between high and low ewes. Numbers of oestrogenic (in vitro oestradiol > 250 pg ml-1 h-1) follicles on the first ovary removed (Exp. 1) were 2.16 +/- 0.5 vs. 1.33 +/- 0.17 in high and low ewes (P = 0.1). Following ULO, these numbers were 3.33 +/- 0.33 and 2.5 +/- 0.18 (P < 0.05 between high and low ewes). There were no significant differences between the first and second ovaries for any of the parameters studied. Follicles from high ovulatory ewes (n = 33) differed from those of low ovulatory ewes (n = 23) by a smaller size (P < 0.01), a reduced number of granulosa cells (P < 0.01) together with decreased oestradiol (P < 0.05) and testosterone (P < 0.01) production in vitro. However, steroid production per cell (oestradiol per granulosa cell, testosterone per thecal cell) was similar in the two groups of sheep. FSH concentrations (Exp. 2) in high ovulatory ewes were significantly higher than those of low ovulatory ewes during the late luteal phase, and the decrease in FSH concentrations was steeper (1.4 ng) during the early follicular phase for high ovulatory ewes than low ovulatory ewes. Chemical hypophysectomy achieved by a 17-day treatment with a GnRH agonist demonstrated that these high FSH concentrations may be important to generate the high ovulation rate of the 'high' ewes as ovulation rate of high and low ewes was similar following chemical hypophysectomy followed by administration of similar amounts of exogenous gonadotropins to both groups of ewes. It is concluded that, despite different genetic control of their high ovulation rate (Chios-polygenic; Booroola-major gene), alterations in follicular function and its control are very similar in high ovulatory Chios and in FecB carriers.