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Title: Size of Ovulatory Follicles in Cattle Expressing Multiple Ovulations Naturally and Its Influence on Corpus Luteum Development and Fertility

Author
item Echternkamp, Sherrill
item Cushman, Robert - Bob
item Allan, Mark

Submitted to: Journal of Animal Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/3/2009
Publication Date: 11/1/2009
Citation: Echternkamp, S.E., Cushman, R.A., Allan, M.F. 2009. Size of Ovulatory Follicles in Cattle Expressing Multiple Ovulations Naturally and Its Influence on Corpus Luteum Development and Fertility. Journal of Animal Science. 87(11):3556-3568.

Interpretive Summary: The most important factors contributing to reproductive inefficiency in beef cattle are failure to become pregnant and low prolificacy. Selection of cattle for the production of fraternal twin births increased twins and altered ovarian activity resulting in an increased frequency of twin and triplet ovulations, the first prerequisite for fraternal twin and triplet births. Cattle expressing spontaneous twin and triplet ovulations provide an experimental model to assess the contribution of ovulation and oocyte (egg) competency to conception failure in beef cattle. Although cattle with twin and triplet ovulations have increased pregnancy rates, the ratio between number of calves per parturition and number of ovulation sites (a predictor of eggs released for fertilization) was 1.6 and 2.0 calves for twin and triplet ovulations, respectively, rather than the anticipated 2 and 3 calves. Such fertility losses for individual twin and triplet ovulations are similar to the 20 to 30% conception losses observed in cattle expressing single ovulations and suggest that a significant portion of these losses result from ovulation or oocyte anomalies causing increased fertilization failure or early embryonic mortality. A comparison of ovulatory follicle size at time of artificial insemination (AI) among cattle with spontaneous single, twin, or triplet ovulations revealed a general reduction in size of the dominant follicles with increasing ovulation rate as a result of a greater proportion of the twin and triplet ovulatory follicles being <12 mm in diameter; these small follicles were absent from cows with single ovulations. These small 8- to 10-mm follicles were likely the result of some twin and triplet ovulatory follicles being recruited at a less mature stage of development or subordinated follicles being rescued from atresia; either situation could account for the 20-35% lower fertility of these follicles at AI. Conversely, fertility of single ovulatory follicles was reduced when diameter was >22 mm. Thus, size of the ovulatory follicle has a significant effect on its fertility, being reduced when size is too large or too small. Current results also revealed that size of spontaneously ovulating follicles has a positive influence on size of the corpus luteum (CL) evolving from the ovulation site and its future level of progesterone secretion. Although maintenance of adequate progesterone concentrations in the blood is critical to the establishment of pregnancy, the increased progesterone from 2 CL did not increase pregnancy rate, suggesting that the lower fertility of small or very large ovulatory follicles was not linked with progesterone output by the CL(s). Collectively, because 20-30% of the twin and triplet ovulations in pregnant females failed to yield a conceptus, findings of this study suggest that low quality gametes and abnormal ovulations also contribute significantly to the 20-30% conception losses found in beef cattle with single ovulations by compromising fertilization or early embryonic development. Females gestating two or more fetuses also had a greater incidence of pregnancy losses during the last two-thirds of gestation as an apparent result of uterine crowding, especially when two or more fetuses were contained within one uterine horn, suggesting animal differences in uterine capacity.

Technical Abstract: Long-term genetic selection of cattle for fraternal twins has increased the frequency of twin and triplet ovulations. Although twin and triplet ovulations increased pregnancy rates initially, ratio of fetal number:ovulation site in pregnant females with twin (0.83) or triplet (0.73) ovulations was <1.0 and number of calves per parturition was 1.6 and 2.0, respectively. Failure of individual twin or triplet ovulations to yield a conceptus in fertile females indicates a significant contribution of ovulation or oocyte anomalies to increased fertilization failure or early embryonic mortality. The present objective was to identify physiological parameters affecting conception in cyclic cattle expressing spontaneous multiple ovulations, including effect of ovulation rate on follicle or corpus luteum (CL) size and their relationship to conception. Diameter of all individual ovulatory follicles was measured by transrectal ultrasonography at AI and ranged from 8-30 mm with a trend for diameter of the individual follicles, and associated CL, to decrease with increasing ovulation rate. Independent of ovulation rate, ovulatory follicles were smaller for nulliparous heifers (1.5 yr) compared with primiparous (2.5 yr; P<0.05) or multiparous (>/= 3 yr; P<0.01) cows. Fetal status was diagnosed by transrectal ultrasonography at 42-72 d after AI. Fertility was reduced (P<0.05) for twin or triplet ovulatory follicles 8-9.9 mm vs >/= 11 mm in diameter, whereas fertility was reduced (P<0.01) for large ovulatory follicles (>/= 22 vs 14-17.9 mm) in monovular females. Plasma progesterone concentrations increased with ovulation rate and were correlated positively with total CL or follicle volume, indicating that CL size and function were influenced by size of follicle of origin. Progesterone was greater (P<0.01) in blood of nulliparous heifers compared with parous cows (>/= 3 yr). The increased proportion of small ovulatory follicles associated with twin and triplet ovulations suggests that some ovulatory follicles were either recruited at a lesser stage of maturity or rescued while undergoing atresia, thus compromising oocyte competency or ovulation. Of greatest importance for reduced fertility was the greater incidence of pregnancy losses occurring in the middle of gestation in females gestating two or more fetuses as an apparent effect of uterine crowding, especially when two or more fetuses were contained within one uterine horn.