EFFECTS OF GENETIC SELECTION AND FOOD RESTRICTION ON OVARIAN FUNCTION IN POULTRY. Roslin Institute (Edinburgh), Roslin, Midlothian, EH25 9PS, UK.
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1 EFFECTS OF GENETIC SELECTION AND FOOD RESTRICTION ON OVARIAN FUNCTION IN POULTRY P.M. Hocking Roslin Institute (Edinburgh), Roslin, Midlothian, EH25 9PS, UK. Abstract The prevalence of multiple ovulation and the consequent disruption of normal egg production increases as birds become larger through genetic selection for higher growth rates. Multiple ovulation is controlled by substantially reducing body weight during rearing. Recent research suggests that food intake during the period immediately before the onset of lay is more important than body weight per se. Large ovarian follicles from broiler breeders are more sensitive to stimulation by gonadotrophins than those from layers. The physiological bases for the changes in ovarian function with selection and the control of multiple ovulation by food restriction are not known. There is no evidence that the control of obesity is related to the mechanism by which food restriction increases productivity in heavy breeding birds. Introduction The body weights of commercial broiler breeders are carefully controlled by restricting food intake throughout life. Compared with birds fed ad libitum, restricted broiler breeders produce more hatching eggs and have a greater viability (Whitehead et al., 1987; Katanbaff et al., 1989). A major part of the improved productivity of restricted birds is attributable to the control of multiple ovulations, particularly during early lay (Hocking et al., 1987). Multiple ovulations decrease rates of lay by interfering with normal shell formation and some ova are lost into the body cavity (van Middelkoop, 1971; Hocking, 1993). The evidence for the existence of a positive relationship between body weight and the prevalence of multiple ovulation will be reviewed. Research in our laboratory over the past 10 years has established some of the relationships between the number of yellow follicles at first egg, which has been used as an index of the potential for multiple ovulation, and body weight, food intake, fatness and age. Yellow follicles require 6-7 days to grow to ovulable size in chickens and ducks and 9-10 days in turkeys. A summary of the results will be given followed by an outline of initial investigations into some of the underlying physiological bases for the increased ovulation rate in birds selected for high growth rate. Selection and ovulation rate Evidence that the prevalence of multiple ovulation increases with selection for body weight comes from two sources. The first is from selection experiments and there is collaborating data from two other experimental sources. The second line of evidence comes from comparisons of large and small commercial lines. 97
2 TABLE 1 Body weight, yellow follicles and abdominal fat at first egg in four strains of turkeys fed ad libitum (AL) or restricted (R) from 4 weeks to photostimulation at 30 weeks of age (from Hocking, 1993) Body weight Yellow follicles Abdominal fat Strain Rearing (kg) (Number) (g/kg) T5 AL R B5 AL R B6 AL R M6 AL R sed TABLE 2 Body weight, yellow follicles and abdominal fat at first egg in selected (S) and relaxed (R) lines of broiler breeders Body weight Yellow follicles Abdominal fat Line Selection (kg) (Number) (g/kg) Sire S R Dam S R sed
3 Reddy and Siegel (1977) showed that tile number of yellow follicles was greater in their high body weight line than in their low body weight line. A similar result was reported in turkeys by Nestor et al. (1982). Abplanalp et al. (1987) Selected a population of White Leghorns for the production of double yolked eggs and obtained a correlated increase in body weight of 20%. Moreover, when the sex-linked dwarfing gene dw was crossed into this line there was a decrease in both body weight and the incidence of multiple ovulations (Abplanalp et al., 1988). Several workers have reported that the reduction in body weight of birds with the dw gene is associated with a decrease in the number of yellow follicles (Jaap and Mohammadian, 1969; van Middlekoop, 1973; Reddy and Siegel, 1977; Hocking et al., 1987). The dw gene causes a reduction in the responsiveness to growth hormone (Burnside et al. 1991), suggesting a role for GH in both growth and ovarian function which will be examined in a later section. Comparisons of commercial lines of ducks (Hocking, 1990) and turkeys (Table 1) at first egg confirmed that large lines had more yellow follicles than smaller lines. A recent comparison of two current commercial lines of broiler breeder with their respective "control" lines maintained for 20 years without selection showed an increase in the number of yellow follicles (Table 2). There is thus a considerable body of evidence that ovarian function changes with selection for high growth rates. It is probable that this is a major component of the well known negative genetic correlation between growth rate and egg production. It was noteworthy that abdominal fatness in the larger genotypes was similar to that in the smaller lines in each of the three species. Food restriction and ovulation rate If food restriction is continued until the onset of lay, a linear relationship exists between body weight and the number of yellow follicles at first egg (Hocking, 1990, 1992; Hocking and Whitehead, 1990). However, when food restriction was terminated before 14 weeks of age by transferring birds to ad libitum feeding, there was no effect on the number of yellow follicles at first egg (Fig. 1). The ovaries of birds fed ad libitum showed follicular development from 14 weeks of age (Hocking et al., 1989) and taken together these results suggested that there was a critical period of ovarian development which could be influenced by food restriction. There was no relationship between the number of yellow follicles and abdominal fat or food intake (Fig. 1). In a subsequent experiment, the role of body weight and the degree of restriction (maintenance, gaining or losing 0.5kg) from and weeks of age was studied. There was a simple linear relationship between the number of yellow follicles and body weight at first egg and no evidence of an effect of the degree of restriction or of the age at which the restriction was applied (Hocking, 1993). The birds in this experiment were photostimulated at 22 weeks of age and treatments resulting in similar body weights at 22 weeks were fed the same quantity of food. This confounding of final body weight and food intake was separated in a 3x3 factorial experiment of body weight (ad libitum, 0.7 and 0.4 of ad libitum-fed body weight) and food intake (ad libitum, 145 or 115g/d). The birds were photostimulated on caging at 18 weeks when the different feeding treatments commenced. The results are summarised in Fig. 2. Food intake had a major influence whereas body weight during rearing had a comparatively small effect on the number of yellow follicles at first egg. The results confirm earlier conclusions that food restriction should be maintained until the onset of lay. 99
4 12 z 10 n O o _- m > "- o _ E 8 _" _ o >- -_. _ _" :3' """ "_ 200 E m -_ "0 u3" 6 _ ,,-. I I I I I I I Weeks on restrictedfeeding Fig. i. Number of ovarian follicles, body weight and abdominal fat at sexual maturity in broiler breeders released from restricted to ad libitum feeding at different ages (from Hocking et al., 1989). 12 AL z Q) tj.m o 9 -- [] 140 g/d [] 115 g/d 0 6 -J A L 70 % AL 40 % AL Rearing Fig. 2. The number of yellow follicles at first egg in broiler breeder hens fed ad libitum, 70 or 40% of ad libitum-fed body weight. The birds were photostimulated and fed ad libitum, 140 or ll5g/d after caging at 18 weeks. The AL-AL (n=6) group were atypical ' similar birds on another experiment had 12 yellow follicles.physiological basis of multiple ovulations i00
5 We noted earlier that selection for high growth rate is associated with an increase in the potential for multiple ovulation. Growth hormone (GH) is lower in large compared with small lines during growth and plasma concentrations of GH and insulin-like growth factor-1 (IGF1) are affected by food restriction (see Hocking et al., 1994). There is now a considerable body of evidence that various growth factors, particularly GH and IGF1, are involved in ovarian function (Giudice, 1992). We therefore determined the plasma concentrations of GH and IGF1 in broiler breeders fed ad libitum or restricted from 17 to 30 weeks of age. As expected, plasma GH was higher in restricted birds until the onset of lay when they were fed ad libitum. IGF1 concentrations were higher in restricted compared with ad libitum-fed birds throughout the period of observation and this was the opposite of the anticipated result. It is likely that hormone concentrations in the general circulation are associated with changes in body weight and do not reflect activity in the ovary. It is possible that rapid growth in broilers is partly a consequence of greater sensitivity to circulating growth hormones which could also affect ovarian responses to gonadotrophins. The sensitivity of three different sizes of ovarian follicles from broiler and layer strains to gonadotrophin stimulation was evaluated by comparing the activity of the enzyme ornithine decarboxylase 3 hours after injection of saline or 200 IU of pregnant mare serum gonadotrophin (PMSG) (Armstrong, 1986). There were no differences in the basal or stimulated activity of small white follicles 1-2 mm diameter (Fig. 3a) but the responses to PMSG were greater in white follicles 5-6 mm and yellow follicles 8-10 mm diameter from the broiler breeders compared to those from layers (Fig. 3b and 3c)_ This result is consistent with the suggestions that the follicles of broiler breeders are more sensitive to hormonal stimulation and that this could be related to the prevalence of multiple ovulation in ad libitum-fed broiler breeders. t-. A B C,-" o O_ F- - E O O o d _ 0 Broiler Layer Broiler Layer Broiler Layer Fig. 3. Activity of ornithine decarboxylase (ODC) in ovarian follicles of different sizes from broiler and layer females 3 hours after being injected with saline or 200 IU PMSG/kg bodyweight. Solid bars-saline; open bars - PMSG. 101
6 Conclusion The incidence of multiple ovulations increases as adult birds become larger through selection for higher growth rate. The physiological basis of this correlation is not known. The interaction of growth factors with steroid hormones and gonadotrophins is a promising area for future research into ovarian mechanisms and the possible role of positive and inhibitory feedback mechanisms involving the hypothalamus and pituitary should not be overlooked. In broiler breeders, multiple ovulations are controlled by a substantial reduction in food intake which must be continued at least until the onset of lay. The lack of a consistent association between the number of yellow follicles and fatness in feeding experiments and the similarity in fatness among large and small lines of broiler breeders and turkeys suggest that a reduction in obesity does not explain why food restriction improves egg production. The evidence clearly supports the conclusion that the control of multiple ovulation is the major reason for the effectiveness of food restriction in increasing the rate of lay in broiler breeders. The reason why food restriction has not generally increased productivity in turkeys may be related to the existence of an optimum number of yellow follicles in the turkeys in which much of the research was done. Food restriction may decrease the number of follicles in "traditional" lines (e.g. strain T5, Table 1), resulting in fewer ovulations and lower egg production than in ad libitum-fed birds. Food restriction may be more effective in current, larger strains which have more than the optimum number of follicles (Table 1). However, the expected decrease in the largest (male) line did not occur and food restriction may not be effective in these birds. Acknowledgement The research conducted by the author was part of a commission from MAFF. References Abplanalp, H., Lowry, D.C. & van Middelkoop, J.H. (1977) British Poultry Science, 18: Abplanalp, H., Napolitano, D. & Tai, C. (1987) Journal of Animal Breeding and Genetics, 104: Armstrong, D.G. (1986)JournalofEndocrinology, 110: Burnside, J., Liou, S.S. & Cogburn, L.A. (1991). Endocrinology, 128: Guidice, L.C. (1992) Endocrine Reviews, 13: Hocking, P.M. (1990) British Poultry Science, 31: Hocking, P.M. (1992) British Poultry Science, 33: Hocking, P.M. (1993) British Poultry Science, 34: Hocking,P.M., Bernard, R., Wilkie, R.S. and Goddard, C. (1994) British Poultry Science, 35: (in press). Hocking,P.M., Waddington,D., Walker, M.A. & Gilbert,A.B. (1987)British Poultry Science, 28: Hocking,P.M., Waddington,D., Walker, M.A. & Gilbert,A.B. (1989)British Poultry Science, 30: Hocking, P.M. & Whitehead, C.C. (1990) British Poultry Science, 31: Jaap, R.G. & Mohammadian, M. (1969) Poultry Science, 48: Katanbaf M.N., Dunnington E.A. & Siegel P.B. (1989)Poultry Science, 68: Nester, K.E. & Bacon, W. (1972) PoultryScience, 51: Reddy, P.R.K. & Siegel, P.B. (1977)Poultry Science, 56: van Middelkoop, J.H. (1973)Archivfur Geflungelkunde, 37: van Middelkoop, J.H. (1971)Archivfur Geflungelkunde, 35: Whitehead, C.C., Herron, K.M. and Waddington, D. (1987) British Poultry Science, 28:
7 Question: D. Zelenka Can you comment on your feelings about the minimum weight, minimum age, and body composition required for lay to begin? I believe these relationships indicate an underlying maturity if the hypothalamus - pituitary - guarded axis which coincides with a typical body weight and age at the onset of lay. I think that a minimum body fat is related to steroid output. Question: D. Zelenka It appears to me that your data shows very well that the adolescent pullet may be able to develop ova, but does not permit ovipositing when heavy, while those which are more synchronized exhibit a normal ova hierarchy and hence normal lay sequence. This is a comment. I think I agree but I'm not sure about "synchronized". I suggest this is not published! 103
8 Question: E. Buss Have you looked at families, white on full feed, to see if some families do not have the "increased ova" condition? No we have not. I have never seen an ad libitum - fed female and early lay which has only a single hierarchy of yellow follicles. That does not mean they do not exist or that selection may not counteract the hypothesized link between growth rate and ovulation rate. Question: J. Kirby What was the time of day that growth hormone measurements were taken? Are the circadian differences in GH cycles between full fed and restricted fed pullets? Blood samples were taken 3-4 hours after the morning food allocation to restricted birds. These could be circadian differences but it is not? that the result were consistent with restricted feeding in young growing birds which were sampled at different times during the day. 104
9 Question: G.F. Barbato Do you think reproductive performance is a question of energy flux or at least energy allocation between growth + reproduction, or as opposed to a single "slice in time" of body weight, carcass composition etc.? Results from the factorial experiment (Fig. 2) indicated that ovarian function at first egg was more closely related to food intake than body weight. Higher body weight had a small effect suggesting that energy balance may be the critical factor affecting ovarian function. Body weight and carcass composition probably reflect energy balance in the majority of experiments. 105
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