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M. A. Driancourt

Summary. In Exp. 1, ovulation rate was measured in three groups of Romanov ewes given two injections of 600 i.u. PMSG 3 weeks apart with the ewes intact (Group I, N = 8), a similar treatment with the ewes intact at the first injection and unilaterally ovariectomized at the second (Group II, N = 8), or unstimulated ewes which were hemispayed at the same time as Group II ewes (Group III, N = 6).

In Exp. 2, the follicular population of one ovary was correlated with the number of ovulations induced by 600 i.u. PMSG in the contralateral ovary (10 Romanov ewes).

From 8·4 ± 1·8 (Group I) and 8·2 ± 3·3 (Group II) CL at the first injection, PMSG-induced ovulation rate at the second injection decreased to 3·9 ± 1·8 and 3·7 ± 1·2 in Groups I and II respectively, a value similar for ewes with 1 or 2 ovaries. Furthermore, despite no major changes in the number of antral follicles after the first injection, there was no correlation (r = −0·09) between the response to the two successive injections in intact ewes.

Comparison of the ovarian status of the ovary removed before the PMSG injection (Group II ewes of Exp. 1, ewes of Exp. 2) to the number of CL found in the remaining ovary demonstrated that PMSG-induced ovulation rate was (i) not correlated with the overall antral follicle population (r = 0·62 in Exp. 1, r = 0·49 in Exp. 2), (ii) significantly correlated (r = 0·74, P < 0·05, in Exp. 1; r = 0·85, P < 0·01, in Exp. 2) with the number of healthy follicles 0·8–2·0 mm in diameter, and (iii) negatively correlated with the number of healthy follicles >2 mm in diameter (r = −0·29 in Exp. 1;r = −0·61, P < 0·05 in Exp. 2).

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H. Sonjaya and M. A. Driancourt

Summary. The ovaries of new born lambs (15 Ile-de-France and 19 Romanov, 34 ovaries) and of 4-week-old lambs (6 Ile-de-France and 12 Romanov, 18 ovaries) were examined histologically to compare ovarian follicular development in infant lambs of breeds differing in their prolificacy. Breed was the major factor affecting follicular population at birth. Ile-de-France lambs had a higher total number of growing follicles (P < 0·001), and more preantral (P < 0·001) and antral (P < 0·005) follicles than did Romanov lambs. Furthermore, the size of the largest follicles was also reduced in Romanov compared to Ile-de-France lambs. At 4 weeks of age, most of the features of the ovarian follicular population except the mean size of the third largest follicle were similar between the two breeds. However, atresia of antral follicles had appeared only in Ile-de-France and not in Romanov lambs.

When a challenge with exogenous gonadotrophins (1000 i.u. PMSG followed by 1500 i.u. hCG) was attempted, ovulation was triggered in 2/6 and 0/12 Ile-de-France and Romanov lambs respectively. Massive follicular development was noted in 3/6 Ile-de-France lambs but in none of 12 Romanov lambs.

Retardation of follicular development together with retardation in the establishment of ovarian sensitivity to gonadotrophins are therefore features typical of the ovaries of Romanov lambs compared to Ile-de-France lambs during the post-natal period.

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H. Sonjaya and M. A. Driancourt

Summary. Plasma FSH concentration was significantly higher in Romanov than Ile-de-France ewe lambs at 5, 6 and 7 weeks of age (P < 0·001, P < 0·02 and P < 0·02, respectively) and at 5, 6 and 7 weeks of age (P < 0·001, P < 0·01 and P < 0·05, respectively) compared to Finn lambs. FSH concentrations were similar and unaffected by time in Ile-de-France and Finn lambs. Ovariectomy at 5 weeks of age produced similar increases in FSH concentrations in Romanov and Ile-de-France ewe lambs, but at 3 months of age the increase in FSH concentrations after ovariectomy was significantly steeper (P < 0·02) in Romanov than Ile-de-France lambs. Sensitivity to oestradiol feedback was related to the age of the lambs. At 5 weeks of age, oestradiol (30 μg in oil per lamb) produced a significant decrease (P < 0·001) in FSH concentrations in Romanov and Ile-de-France lambs, demonstrating that negative feedback can be triggered by oestradiol at this age. Positive feedback after an oestradiol challenge was identified in lambs of both breeds at 6 weeks of age. Sensitivity to the negative feedback of follicular fluid compounds was also established at 5–6 weeks and did not differ between breeds. At 9–10 weeks of age, while there was no breed effect of an oestradiol challenge on FSH concentrations, suppression of FSH concentrations by follicular fluid was shorter in Finn than in the other lambs.

As all the feedback mechanisms are functional at 5–6 weeks of age, it is likely that the between breed differences of FSH profile during infancy are linked to differences in gonadal development.

Keywords: FSH; oestradiol; follicular fluid; lambs; prolificacy

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B. W. Brown and M. A. Driancourt

Summary. Radioactive microspheres (15 μm diameter) were used to measure capillary blood flow rates in the ovaries and ovarian follicles (Qf) in high fecund Romanov and low fecund Préalpes-du-Sud ewes at the preovulatory stage of the oestrous cycle. Additionally, assessments of the percentage of arterial blood passing through ovarian arterio-venous anastomoses were obtained.

The mean ± s.e.m. Qf per unit volume of theca ((ml/min) × 104/mm3) for non-atretic follicles in Romanov ewes was significantly greater (P < 0·05) than that in Préalpes ewes (365·8 ± 42·4, n = 19, compared with 241·3 ± 30·1, n = 14). For each breed, the mean Qf value for non-atretic follicles was 8–10 times greater than that for atretic follicles.

In Romanov ewes, total Qf ((ml/min) × 104) and Qf per unit volume of theca was greatest in small-sized follicles (3· 1–5·0 mm) while in Préalpes ewes, maximum flow was attained in larger-sized follicles (5·1–7·0 mm). The elevated Qf in small-sized follicles in Romanov ewes may be conducive to more follicles achieving maturation at a smaller diameter in this breed than occurs in the Préalpes ewes.

The absence of flow through ovarian arterio-venous anastomoses in the Romanov, but not in the Préalpes, ewes suggests different mechanisms for controlling the distribution of the total ovarian blood supply in the 2 breeds.

Keywords: follicles; blood flow; sheep; prolificacy

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M. A. Driancourt and L. P. Cahill

Summary. To investigate the number, size and fate of the follicles > 2 mm in diameter involved in the differentiation of the preovulatory follicle in-vivo monitoring of growth and regression of individual follicles was performed at different times after a PG-induced follicular phase.

In Exp. 1, the 3 largest follicles of each ovary were labelled with ink in the peripheral stroma at 0,4,8,12,24 or 48 h after a PG injection. At a second laparotomy, it was assessed which follicles had ovulated. In Exp. 2, a similar procedure was applied in 12 ewes which underwent repeated laparotomies at 6, 30 and 54 h after PG and after ovulation.

At all times, there was a huge variability in the size at the time of ink labelling of the follicles that finally ovulated ('ovulatory' follicles). A single measurement of follicle size is therefore a poor prediction of the ovulatory follicles. However, a significant reduction in the proportion of non-ovulatory follicles within the size range of ovulatory follicles occurred at 12–24 h after PG, together with a change in follicle hierarchy at 8-24 h after PG.

The results of repeated laparotomies showed that only 60% of follicles > 2 mm at 6 h after PG had grown by 30 h. Selection occurred between 30 and 54 h after PG as indicated by a significant drop in the number of growing follicles to a level at 54 h that equalled the ovulation rate. The growth rate of the ovulatory follicles was 1·4 and 0·4 mm per day between 6 and 30 h and 30 and 54 h after PG respectively. The shrinkage rate of non-ovulatory follicles was 1·6 mm/day.

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K. Reynaud, J. P. Hanrahan, A. Donovan and M. A. Driancourt

High prolificacy due to a gene that has a large effect on ovulation rate has been noted in Booroola and Inverdale ewes. High prolificacy in the Belclare breed (a composite developed from stocks selected for very large litter size or high ovulation rate) may be related to the segregation of two genes. The aims of this study were (i) to compare the morphological and functional features of ovulatory follicles from carriers (which could only be heterozygous for the genes of interest) and non-carriers, and (ii) to identify markers of the Belclare genes among secreted or cellular ovarian proteins. Belclare carrier ewes had more ovulatory follicles (4.9 ± 0.4) than did non-carrier ewes (2.0 ± 0.2) (P < 0.001). Ovulatory follicles from carriers were also smaller (4.4 ± 0.1 mm versus 5.7 ± 0.2 mm, P < 0.001) and contained a significantly reduced number of granulosa cells (P < 0.001). However, the proportion of proliferating granulosa cells in ovulatory follicles was similar in both groups. The in vitro secretion of steroids per follicle was only marginally lower in follicles from Belclare carriers compared with non-carriers. Furthermore, similar concentrations of steroidogenic enzymes were present in both groups, indicating that steroidogenic potential per granulosa cell is similar between carriers and non-carriers. Possible markers of the Belclare genes were identified among cellular proteins of follicular walls by two-dimensional PAGE and image analysis. Two spots at 78 and 49 kDa were always absent in samples from non-carriers. When secreted proteins in follicles from carriers were compared with those from non-carriers, two spots at 53 and 41 kDa were restricted to samples from carriers and three spots at 97, 91 and 45 kDa were unique to samples from non-carriers. Interestingly, the spot at 91 kDa is also affected by the Booroola gene.

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M. A. Driancourt, I. K. Gauld, M. Terqui and R. Webb

Summary. Prolific breeds of sheep (Romanov, Finn and Booroola Romanov crosses heterozygous for the Booroola gene (F +) were compared with breeds of lower prolificacy (Ile-de-France, Finn × Scottish Blackface, Merino × Blackface and Booroola × Romanov not carrying a copy of Booroola gene (++)) by in-vivo monitoring of follicular kinetics by ink labelling during the late luteal phase and follicular phase of the oestrous cycle followed by histological examination of the ovaries or follicle dissection. At each of 3 successive laparotomies, the 3 largest follicles of each ovary were measured and ink labelled. At the final laparotomy, around the beginning of oestrus, all ewes were ovariectomized.

High ovulation rate was not associated with the total number of antral follicles in any of the breeds. However, there were more follicles > 2 mm in diameter in Romanov and Booroola × Romanov crosses (F +) compared to their respective controls. Such a feature was not observed in Finnish Landrace compared to Finn × Blackface and Merino × Blackface ewes. A more numerous population of recruitable follicles, together with a similar incidence of selection through atresia, were the features associated with the high ovulation rate of Romanov compared to Ile-de-France ewes. The high ovulatory potential of the Finn ewes resulted from a markedly reduced incidence of selection through atresia. Booroola × Romanov ewes carrying a copy of the Booroola gene (F +) appeared to possess features of both parental breeds, including high numbers of recruitable follicles, smaller follicular size when recruitment occurs and an extended time for recruitment. Booroola × Romanov (++) ewes, not carrying the gene, appeared to have lost part of the 'Romanov characteristics' of a more numerous population of recruitable follicles. The variability in the kinetics of preovulatory enlargement, seen in these breeds of sheep, demonstrates that there are a number of pathways through which high ovulation rate can be achieved and hence through which ovulation rate might be manipulated.

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M. A. Driancourt, L. P. Cahill and B. M. Bindon

Summary. To investigate the factors contributing to the different ovulation rates observed in two strains of sheep (Booroola 5·2, Merino 1·2), in-vivo monitoring of follicular kinetics followed by histological examination of both ovaries was performed during the late luteal and follicular phases. Ewes of both strains were either ovariectomized at Day 13, or had the 3 largest follicles of each ovary ink-labelled at Day 13 and were ovariectomized at Day 15, or had the 3 largest follicles of each ovary ink-labelled at Days 13 and 15 and were ovariectomized 16 h after the beginning of oestrus (N = 6 per time per strain). In another experiment, the age effects on the follicular populations of these two strains were also studied.

There were 2–4 times more primordial follicles and 1·–2 times more preantral follicles in the ovaries of Booroola than in control Merino ewes, although the number of antral follicles was the same. The percentage of normal follicles in this population was higher in Merino than Booroola ovaries. In Booroola ewes, there was no correlation between the number of antral follicles per ovary and the ovulation rate at the previous cycle (r = 0·22). This suggests that follicle numbers do not play a key role in the high ovulation rate of the Booroola strain. The number of follicles initiating growth from the primordial pool, the number of growing follicles disappearing at the preantral stage, the pattern of antrum development, granulosa cell multiplication and appearance of atresia differed between strains.

The reasons for the high ovulation rate of the Booroola strain became clear when preovulatory enlargement was followed by ink labelling. An extended period of time during which recruitment of ovulatory follicles takes place, together with a low incidence of selection and the ability of the follicles to wait for ovulation are the features involved in this high ovulation rate.

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M. A. Driancourt, R. Webb and R. C. Fry

Summary. The process by which a single follicle is selected to ovulate while others regress is unknown in ewes. If the dominant follicle secretes substances that directly inhibit the growth of other follicles, the superovulatory response to the administration of exogenous gonadotrophins may be blunted. Administration of 1250 iu pregnant mares' serum gonadotrophin (PMSG) before or after the emergence of the dominant follicle in the follicular phase, or 1000 iu PMSG in the presence or absence of a large healthy or atretic follicle during the luteal phase did not affect the induced ovulatory response. Comparisons between the ovary with or without the dominant follicle did not reveal any differences in ovulatory response to PMSG. The in-vitro features (i.e. mitotic index, oestradiol and testosterone production) of follicles ipsilateral or contralateral to the dominant follicle during the early and late follicular phases were also similar.

If the dominant follicle secretes substances detrimental to the other follicles, this could be mimicked in vitro. Co-culture of small follicles with the largest follicles in a closed system did not reduce their incorporation of 3H thymidine in granulosa cells, compared with small follicles cultured alone.

These data suggest that dominance is probably not operative in sheep. The administration of 500 iu of PMSG during the midfollicular phase increased ovulation rate in Merino ewes, indicating that dominance is essentially passive in ewes and can easily be overcome by raising gonadotrophin concentration.

Keywords: follicle; ovulation; gonadotrophin; paracrine regulation; sheep

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R. Webb, I. K. Gauld and M. A. Driancourt

Summary. Morphological and functional features of large ovarian follicles from three breeds of sheep, with different ovulation rates (Finnish Landrace N = 12, Finnish Landrace × Scottish Blackface N = 16, Merino × Scottish Blackface N = 16) were compared by integrating three techniques; ink labelling, in-vitro oestradiol production and morphological classification. The follicles were removed at two stages of the follicular phase, 1 (PG + 1) or 2 (PG +2) days after PGF-2α treatment and compared after monitoring their rates of growth with the use of ink labelling. After ovariectomy all follicles ≥ 1 mm in diameter were dissected, and the 8 largest were incubated individually for 2 h to assess their ability to secrete oestradiol and testosterone. After incubation the follicles were processed for histological examination and checked for atresia. An analysis of the follicle population was based on in-vitro oestradiol secretion rates in all three breeds; an oestrogen-active population producing 500–8100 pg oestradiol/ml/h and an oestrogen-inactive population producing 0–499 pg oestradiol/ml/h. A comparison of the 3 approaches demonstrated agreement on 94·3 ± 1 ·2% of occasions. Ink-labelling demonstrated that all follicles identified as oestrogen-active were increasing in size. Within oestrogen-active follicles significant correlations were detected between oestradiol production and testosterone production (r = 0·42), oestradiol production and granulosa cell number (r = 0·45) and between oestradiol production and mitotic index (r = −0·38). A regression model fitting breed, stage of atresia, granulosa cell number, in-vitro testosterone production and mitotic index demonstrated that granulosa cell number is a characteristic which contributes significantly to the variation of in-vitro oestradiol production in oestrogen-active and oestrogen-inactive follicles. There was no significant difference between breeds in the mean number of ink-labelled follicles growing from Day PG − 1 to Day PG +1. There was a significant difference between the breeds in the number of ink-labelled follicles growing between Days PG + 1 and PG +2 (Days 1 and 2 of the follicular phase), the number being similar to the ovulation rate for the breed. The majority of the oestrogen-active follicles had been recruited by Day PG − 1, although in the Finnish Landrace genotypes more than 30% were recruited on or after Day PG + 1 compared to less than 10% in Merino × Scottish Blackface ewes. Although mean oestradiol production by oestrogen-active follicles was similar in all three breeds, oestrogen-active follicles in Finnish Landrace ewes had significantly reduced granulosa cell number and mitotic index compared to the other breeds.

These results demonstrate: (1) a good agreement between the three criteria used to characterize follicles, (2) that the mechanisms controlling follicular recruitment into the population of gonadotrophin-dependent follicles are different from the mechanisms controlling the selection of the follicles destined to ovulate and (3) that despite no