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Review article

Endocrine changes and management factors affecting puberty in

gilts

*

A.C.O. Evans , J.V. O’Doherty

Department of Animal Science and Production, Faculty of Agriculture, Conway Institute for Biomolecular and Biomedical Research, University College Dublin, Belfield, Dublin 4, Ireland

Received 16 September 1999; received in revised form 17 February 2000; accepted 19 May 2000

Abstract

Puberty in gilts is the occurrence of first oestrus and the onset of reproductive capability (usually at between 200 and 220 days of age). It is the combined effect of genetic factors and management factors (including nutrition, boar exposure and season) that contribute to the age at puberty. Consumer demands for leaner pork have lead to genetic selection for increased lean tissue growth rate and reduced body fat. This has resulted in a delay in the age at puberty and a decrease in energy stores for subsequent growth, pregnancy and lactation. Restriction of dietary protein during the prepubertal period is a way to enhance body-fat reserves; however, this has detrimental effects on the age at puberty and ovulation rates, but can be overcome by restoring dietary protein in the weeks before the induction of puberty. Luteinizing hormone (LH) is a key hormone in regulating ovarian follicular growth and, hence, the age at which puberty occurs. Concentrations of LH in the blood fluctuate during the prepubertal period in association with ovarian development. The nutritional modulation of hormone secretion is not clear. Future management strategies to enhance both reproductive performance and to satisfy consumer demands need to consider hypothalamo-pituitary maturation in association with body weight and body-composition parameters.  2001 Elsevier Science B.V. All rights reserved.

Keywords: Gilt; Puberty; Hormone; Nutrition; Management

1. Introduction vals than sows, the percentage of gilts in a herd has a marked effect on overall productivity.

Reducing the number of non-productive sow days The first management decision to be made about is an important component of productivity in current animals entering the breeding herd is the timing of pig-production enterprises. It has been estimated that first breeding. Breeding at a younger age is associ-between 15 and 25% of litters produced in pig units ated with fewer non-productive days and, conse-are from gilts (Gordon, 1997). Since gilts have quently, with lower initial costs. However, when smaller litters and longer weaning-to-service inter- deciding whether or not to bred gilts early, two consequences must be considered: firstly, the effect on subsequent reproductive performance and, sec-*Corresponding author. Tel.: 1353-1-706-7771; fax:1

353-1-ondly, the effect on longevity of these gilts in the 706-1103.

E-mail address: alex.evans@ucd.ie (A.C.O. Evans). herd. It has been shown that, as the age at first

farrowing increases, there is an increase in the average number of piglets born alive and weaned per litter, but that there is also a decrease in the average number of litters at culling (Le Cozler et al., 1998). In practical terms, this effect is only significant for gilts that are successfully mated at greater than 270 days of age (Le Cozler et al., 1998). Extreme leanness increases the age at puberty and has detri-mental effects on lifetime reproductive performance (Gaughan et al., 1995).

Puberty in gilts is the occurrence of first oestrus and the onset of reproductive capability. Once puber-ty has been reached, gilts will normally exhibit regular oestrous cycles of around 21 days duration. Age at puberty is regulated by internal (breed, live weight, backfat depth) and management factors (nutrition, boar exposure, environmental factors), both of which are mediated via the endocrine

Fig. 1. Changes in mean luteinizing hormone (LH) concentrations reproductive axis. There is increasing awareness of

(after Pelletier et al., 1981; Diekman et al., 1983; Camous et al., the possible conflict between that of increasingly _{1985), oestrogen concentrations (after Lutz et al., 1984; Camous et} leaner pigs and of maintaining or increasing re- _{al., 1985) and numbers of follicles greater than 3 mm in diameter} productive performance. The aim of this paper is to (after Dyck and Swierstra, 1983; Grieger et al., 1986) in gilts

during sexual maturation. review the hormonal changes that precede puberty in

gilts and the management options available to

producers with particular reference to modern, frequency (Pelletier et al., 1981; Lutz et al., 1984; leaner, highly growth-efficient gilts. Prunier et al., 1993a). This final increase is associ-ated with final maturation of ovarian follicles (Bel-tranena et al., 1993) and culminates in a preovulatory

2. Endocrine changes surge that successfully stimulates ovulation. Follicle-stimulating hormone (FSH) concentrations are high 2.1. Hormone profiles and ovarian development early in life and decrease after 70 to 125 days of age,

before puberty and it is clear that mean FSH concentrations do not

1993b), as has been suggested for cattle (Evans et in LH concentrations may occur because of the al., 1994; Day and Anderson, 1998). In Meishan establishment of oestradiol negative feedback, which gilts, ovarian development is more rapid than in is first seen at about 100 days of age (see Christenson commercial breeds, with antral follicles first appear- et al., 1985). FSH also appears to be regulated by ing between 30 and 60 days of age (Miyano et al., negative feedback from at least 84 days of age

1990). (Prunier and Louveau, 1997).

Oestradiol concentrations (Fig. 1) are low In some species (rats and primates in particular), throughout the majority of the prepubertal period but the final maturational events leading to the increase increase prior to puberty (Esbenshade et al., 1982; in LH concentrations and puberty appear to occur as Lutz et al., 1984; Camous et al., 1985). Progesterone a result of positive stimulation to the hypothalamus concentrations only increase after puberty with the via activation of a central drive component to GnRH formation of the first corpora lutea (Esbenshade et neurones (Ojeda, 1991). Endogenous opioid peptides al., 1982; Prunier et al., 1993a). Puberty usually regulate LH secretion in some farm animals (Haynes occurs between 200 and 220 days of age, although et al., 1989); however, opioidergic systems do not considerable variation exists according to internal appear to regulate tonic LH secretion during the (including genetic) and management factors. peripubertal period in gilts (Barb et al., 1988; Kuneke et al., 1993). None-the-less, opioidergic 2.2. Regulation of gonadotrophin secretion systems may play a role in the preovulatory LH surge in pubertal gilts (Asanovich et al., 1998). The Puberty occurs only when gilts reach a certain excitatory amino acids, glutamate and aspartate, are stage of physiological maturation (i.e., when physio- important neurotransmitters in the central control of logical development is adequate to support success- gonadotrophin secretion in many species (Brann, ful reproduction). While this involves physical 1995). However, like opioidergic systems, it is growth attributes, it is reliant on the culmination of a unlikely that excitatory amino-acid stimulation of the series of maturational events in the endocrine system hypothalamus is the cause of increased gonado-that regulate hormone secretion, resulting in be- trophin secretion before puberty in gilts (Barb et al., havioural oestrus and ovulation. 1992; Chang et al., 1993; Estienne et al., 1995; The regulation of gonadotrophin secretion occurs Popwell et al., 1996). During the weeks preceding via changes in inhibitory (negative feedback) and / or puberty, the prevailing theory is that the sensitivity stimulatory actions at the hypothalamus and pitui- to steroid negative feedback diminishes (gonadostat tary. The exact importance of these two contrasting hypothesis; see Day and Anderson, 1998). This actions is unclear during sexual maturation in gilts. allows LH secretion to increase (Pelletier et al., During the early prepubertal period, it is likely that 1981; Prunier et al., 1993a) in the face of low or the central mechanisms (i.e., above the pituitary) that increasing oestradiol concentrations (Esbenshade et regulate reproduction are immature. During this time, al., 1982; Lutz et al., 1984; Camous et al., 1985). the pituitary is responsive to exogenous gonado- While there is evidence to support this theory trophin releasing hormone (GnRH) stimulation (Berardinelli et al., 1984; Lutz et al., 1984), others (Chakraborty et al., 1973; Foxcroft et al., 1975; have been unable to demonstrate a reduction in Pressing et al., 1992), indicating that the pituitary is oestradiol negative feedback prior to first ovulation functional at a young age. Negative feedback by (Elsaesser et al., 1991). It has also been suggested ovarian steroids is weak, as shown by a lack of that increases (Pearce et al., 1988) or decreases increase in LH following ovariectomy (Elsaesser et (Prunier et al., 1993a) in corticosteroid concentra-al., 1978). The early transient increase in LH con- tions may increase LH secretion at about the time of centrations may occur due to maturation of the puberty.

ovula-tion; this is absent at 6 days of age, weak at 60 days appears to be related to the genetic background of of age (Kuneke et al., 1993) and evident at 160 days the gilts and to other aspects of the environment in of age (Elsaesser and Foxcroft, 1978; Foxcroft et al., which they are kept. Consequently, age is not

1984). considered to be an accurate predictor of puberty in

In summary, fluctuations in LH concentrations are gilts (Rozeboom et al., 1995).

closely related to maturation of the reproductive tract Gilts must reach a minimum weight of about 75 and first ovulation in gilts. The control of LH kg before puberty can be attained (Hughes and Cole, secretion is complex. The initial increase in LH 1975; Young et al., 1990); however, like age, great concentrations may be due to maturation of hypo- variability exists. Recently, it was suggested that live thalamic activity and / or factors regulating the hypo- weight on its own does not account for the induction thalamus, and the increase in the immediate peripub- of puberty, but contributes as one of the factors ertal period appears to be due to a resetting of the leading to puberty (Gaughan et al., 1997). Body sensitivity to oestradiol negative feedback. weight is a measure of the combined components of the different elements of body composition, and consideration needs to be given to the fatness and

3. Influence of genetic factors on age at puberty leanness of gilts (see Section 3.3).

3.1. Age and weight 3.2. Breed

Some authors suggested that age is the most Large differences between breeds in the age at important factor determining puberty attainment puberty have been reported, with the average age (Prunier et al., 1987; Newton and Mahan, 1992). being greatest in Duroc gilts and lowest in Meishan However, it is widely recognised that unstimulated gilts (Table 1). Crossbred gilts reach puberty earlier gilts may reach puberty from as early as 170 days to and have fewer non-productive days compared with as late as 260 days of age (Dyck, 1988; Eliasson et purebred animals (Bidanel et al., 1996). Besides al., 1991). Part of the variability of age at puberty these differences between breeds, considerable

vari-Table 1

Mean age (6S.D., where available) at puberty of different breeds of gilts

Breed Overall Mean6S.D. Reference

mean age

Duroc 235 195617 Haines et al., 1959

224620 Christenson and Ford, 1979

259625 Bryan and Hagen, 1991

263 Good et al., 1965

Hampshire 207 207628 Christenson and Ford, 1979

Large White 205 173613 Gaughan et al., 1997

200620 Allrich et al., 1985 206621 Sterning et al., 1998

208620 Rydhmer et al., 1994

211621 Christenson and Ford, 1979 211620 Eliasson et al., 1991 215649 Bidanel et al., 1996

215 Kerr and Cameron, 1997

Landrace 185 173625 Christenson and Ford, 1979

185620 Allrich et al., 1985 198635 Bidanel et al., 1996

Meishan 97 8169 Legault and Caritez, 1983

ation exists within breeds, as demonstrated by the shorter oestrus and decreased reddening and swelling variability within studies (one standard deviation of the vulva compared with fatter gilts (Rydhmer et about the mean age at puberty is about 20 days) and al., 1994). It has been suggested that puberty is between studies for a given breed (Table 1). These delayed in extremely fast-growing gilts because the differences may be explained by variations in geno- increase in growth rate is primarily due to a more types within breeds and in management regimens. rapid accumulation of lean rather than fat tissue Therefore, breed influences age at puberty, but, (Beltranena et al., 1991). It has been determined that among commercial breeds, management factors can a minimum fatness threshold of about 6 mm in have a greater effect than breed on the onset of backfat thickness needs to be achieved for the reproductive capability. attainment of puberty (Beltranena et al., 1993). However, it is considered that gilts need at least 13 3.3. Modern genotypes and body composition mm of backfat before first mating (Yang et al., 1989). Hence, body fat and muscle content are The 1970s were a period of rapid change in the associated with age at puberty, and there appears to pig industry, with consumers in many countries be genotype-specific minimum levels of body fat and demanding less fat and leaner meat. The industry muscle required for the onset of puberty to occur responded by selecting its breeding animals for low (Kerr and Cameron, 1997). More recently, the rate of backfat and the genotype of the animals changed. fat and / or protein deposition has been linked to Animals that are selected for lower backfat grow physiological maturity and reproductive performance bigger and, compared with animals of small mature of gilts (Edwards, 1998), and this rate is suggested to size, are leaner at the same body weight because they be a more important determinant for puberty than have a lower proportion of their mature body size age, weight or boar exposure (Gaughan et al., 1997). and are physiologically younger (Gaughan et al., In conclusion, to most efficiently meet customer 1997). As well as reduced backfat, voluntary food demands, selection for future genotypes of pigs intake of the selected animals has been reduced needs to concentrate on daily food intake, high lean (Webb, 1989). Based on measures of live weight, growth rate and consideration needs to be given to a backfat thickness and average daily gain, it has been minimum level of fatness in order to avoid pubertal proposed that puberty occurs only after the attain- retardation.

ment of a minimum level of leanness (Cunningham et al., 1974), fatness (den Hartog and van Kempen,

1980) or the ratio of fat to lean (Kirkwood and 4. Influence of management factors on age at

Aherne, 1985). puberty

Genetic changes in body composition and

appe-tites are associated with reduced reproductive per- 4.1. Nutrition formance in contemporary comparisons of lines of

et al., 1999a). Modern pig genotypes are extremely sensitive to modest reductions in feed intake, which can delay puberty by more than 3 weeks (van Lunen and Aherne, 1987). The plane of nutrition used in rearing gilts influences the age at which first oestrus is shown (Dzuik, 1991; Prunier, 1991).

The improved genotype of modern sows codes for increased lean growth and decreased body-fat con-tent. This decrease in fat has partly resulted in gilts that are less able to deal with the simultaneous demands of growth, pregnancy and subsequent lacta-tion. There are two possible approaches to overcome this problem: firstly, increase the plane of nutrition of gilts prior to puberty as a way of increasing fat reserves or, secondly, use dietary protein restriction to limit lean tissue growth and increase body-fat reserves (Edwards, 1998). The first strategy is

unde-Fig. 2. Effects of protein restriction on backfat thickness ([a], sirable as it leads to an increase in mature body size

after Cia et al., 1998), age at puberty ([b], after Gill, 1997) and (O’Dowd et al., 1997), which increases management _{ovulation rate at the second cycle ([c], after Crisol et al., 1997) in} problems associated with oversized animals and _{gilts. Gilts were fed high protein ([a] and [c]: 0.9 g lysine / MJ} leads to higher feed maintenance costs and a reduced digestible energy; [b]: 1% lysine) or low protein ([a] and [c]: 0.3 g lysine / MJ digestible energy; [b]: 0.5% lysine) diets from 118, 87 feed intake in the first lactation (Le Cozler et al.,

or 130 days ([a], [b] and [c], respectively). In [c], puberty was 1999b). A 50% restriction of dietary lysine to

induced by exogenous gonadotrophin treatment (PG600) at 180 growing gilts is an effective way of restricting lean _{days of age, and flushed gilts were fed the low diet from 130 days} tissue growth and increasing body lipid content (den _{and the high diet from 175 days of age. Bars within groups with} Hartog and Verstegen, 1990; Gill, 1997; Cia et al., no common superscript are significantly different (P,0.05). 1998; Fig. 2). However, this method reduces growth

rate, delays age at puberty and decreases ovulation rate (Fig. 2). This negative effect of protein

restric-tion on ovularestric-tion rate in gilts can be overcome by omic gains of feed restriction during rearing may be protein flushing in the weeks prior to the induction of lost after the first two parities (Le Cozler et al., puberty (Fig. 2). Such short-term changes in food 1999b).

intake can modify reproductive function in the The complicated link between nutrition and re-absence of changes in body weight or body com- productive hormones has previously been reviewed position (Booth et al., 1994). (Booth, 1990; Cox, 1997; Cosgrove, 1998). The Decreasing the amount of food made available to most likely hormonal links between nutrition and the animals will reduce feed costs. While severe restric- reproductive axis are insulin and insulin-like growth tions during the prepubertal period will have detri- factor I (IGF-I), which may act at either the hypo-mental effects on reproductive performance (van thalamic–pituitary level or directly at the ovarian Lunen and Aherne, 1987; Dzuik, 1991; Prunier, level.

4.2. Boar effect

The timing of puberty in gilts is markedly in-fluenced by the age at which they first come in contact with a boar (reviewed by Hughes et al., 1990). For maximum boar stimulation, it is essential that gilts are reared out of sight and sound of boars until they are about 165 days of age. At this time, they are transported to a new location and are regularly exposed to a sexually active boar. This has the effect of bringing them into heat within 7 to 20 days (Hughes et al., 1990). For most effective boar exposure, gilts and boars should to be in physical contact for at least 30 min each day (Caton et al., 1986; Hughes et al., 1990). Introducing and remov-ing the boar is more effective than maintainremov-ing the boar and gilts in constant fence-line exposure (Caton et al., 1986). The pubertal response is further

en-Fig. 3. Effect of [a] boar libido on gilts reaching puberty, and of hanced if boar contact occurs more than once a day _{the presence of a boar on circulating concentrations of [b] LH and} (Hughes et al., 1997; Hughes and Thorogood, 1999). [c] cortisol. Gilts in [a] were exposed to boars with high or low libidos (based on mating tests) for 20 min per day, starting at 160 For best results, mature boars with high libido should

days of age (from Hughes, 1994). Mean LH concentrations and be used (Hughes, 1994; Fig. 3).

LH pulse frequencies in the gilts (n512) in [b] were for the While tactile, auditory and visual cues from the

periods of 6 h before (Before) and after (After) boar exposure at boar may be involved in the pubertal response, _{135 days of age (after Kingsbury and Rawlings, 1993). Cortisol} pheromonal stimulation has an important role in concentrations in [c] are mean values from 15-min periods after a back-pressure test for oestrus detection (no boar) or introduction to stimulating puberty in gilts (Signoret, 1970; Hughes

a boar (with boar) on each of 11 days prior to oestrus (after Turner et al., 1990; Pearce and Paterson, 1992). When the

et al., 1998). Bars within groups with no common superscript are olfactory bulbs were removed from gilts, they were

different (P,0.05). unresponsive to boar stimulation (Kirkwood et al.,

1981). In addition, transportation of gilts increases the response to boar stimulation, but transport alone

(not followed by boar stimulation) is insufficient to puberty (Pearce and Paterson, 1992), and treating stimulate early oestrous behaviour (Hughes et al., gilts with adrenal corticoids did not advance the age

1997). at puberty (Esbenshade and Day, 1980). In addition,

system(s) regulating the sensitivity of LH to oes- however, melatonin secretion in response to light-tradiol negative feedback. :dark cycles is less clear in pigs. Some studies have In summary, for optimal effect, gilts need to be shown a nocturnal rise in melatonin secretion exposed to a mature boar with high libido for one or (McConnell and Ellendorff, 1987; Paterson et al., more 30 min periods per day after 165 days of age. 1992a), whereas others have not (Minton et al., Boar exposure increases LH concentrations but the 1989; Diekman et al., 1992). More recently, it has role of cortisol and the mechanism by which this been concluded that pigs have no clear circadian occurs is unclear. rhythm of melatonin in peripheral blood (Bubenik et al., 2000) but that there is a weak nocturnal rise in serum melatonin concentrations (Green et al., 1996). 4.3. Confinement

In addition, differences in melatonin secretion be-tween light and dark periods may vary according to Overcrowding may decrease the percentage of

light intensity and age (Green et al., 1999). gilts showing oestrus (Cronin et al., 1983;

Christ-Lengthening the duration of the period of high enson, 1986). Gilts maintained with a space

allow-circulating melatonin concentrations by oral adminis-2

ance of 1 m per pig had significantly elevated free

tration of melatonin in the afternoon to gilts kept corticosteroid concentrations and a lower proportion

under long-days will overcome the seasonal inhibi-displayed oestrus and were successfully mated

com-tion of attainment of puberty (Paterson et al., 1992b). 2

pared with those pigs allowed 2 or 3 m of space

Seasonal depression of the attainment of puberty in (Hemsworth et al., 1986). This may be explained by

gilts can also be partially or wholly overcome by a delay in growth that has been observed in gilts

providing olfactory stimulation from boars (Hughes submitted to space restriction (Pearce and Paterson,

et al., 1990; Paterson et al., 1991). 1993). However, others have crowded gilts together

As in other species, links between long days, high to the extent that growth rate and feed efficiency

melatonin and increasing LH secretion are complex were reduced but without affecting the average age

in pigs (see Love et al., 1993). Since the inhibitory at first oestrus (Ford and Teague, 1978). While

influence of long-day regimes on gilt puberty attain-crowding may be a factor in controlling the age at

ment can be altered by the use of boar contact puberty, group size appears to be an additional

(Paterson and Pearce, 1990; Paterson et al., 1991), variable. Gilts housed in small groups (three or less)

we speculate that photoperiodic regulation of the reached puberty later than gilts housed in larger

attainment of puberty may be by a similar mecha-groups (nine or more) at the same density

(Christ-nism(s) as the boar effect (i.e., by altering the enson, 1986).

sensitivity to oestradiol negative feedback by as yet unidentified pathways).

4.4. Season

4.5. Manure gases The attainment of sexual maturation in gilts is

mech-luteinizing hormone secretion in the pig. Dom. Anim. Endo-anism whereby poor air quality delays the onset of

crinol. 9, 225–232. puberty in gilts is unknown, but it appears that

Barb, C.R., Rampacek, G.B., Kraeling, R.R., Estienne, M.J., odorous gases, such as ammonia, may diminish the _{Taras, E., Estienne, C.E., Whisnant, C.S., 1988. Absence of} ability of the gilts to perceive olfactory cues from _{brain opioid peptide modulation of luteinizing hormone} secre-boars (Curtis, 1972). tion in the prepubertal gilt. Biol. Reprod. 39, 603–609.

Beltranena, E., Aherne, F.X., Foxcroft, G.R., 1993. Innate vari-ability in sexual development irrespective of body fatness in gilts. J. Anim. Sci. 71, 471–480.

Beltranena, E., Aherne, F.X., Foxcroft, G.R., Kirkwood, R.N.,

5. Conclusion

1991. Effects of pre- and postpubertal feeding on production traits at first and second estrus in gilts. J. Anim. Sci. 69, Modern pig genotypes have been selected for

886–893.

rapid, efficient, lean-tissue growth, in combination _{Berardinelli, J.G., Ford, J.J., Christenson, R.K., Anderson, L.L.,} with low body-fat content. This has been associated 1984. Luteinizing hormone secretion in ovariectomized gilts: effects of age, reproductive state and estrogen replacement. J. with detrimental effects on pubertal development.

Anim. Sci. 58, 165–173. Using nutritional strategies, it is possible to alter

Bidanel, J.P., Gruand, J., Legault, C., 1996. Genetic variability of body composition and increase body-fat reserves to

age and weight at puberty, ovulation rate and embryo survival improve the rate of sexual maturation. To fully _{in gilts and relations with production traits. Genet. Sel. Evol.} understand the importance of nutritional programmes _{28, 103–115.}

on reproduction, such strategies need to consider that Booth, P.J., 1990. Metabolic influences on hypothalamic–pitui-tary–ovarian function in the pig. J. Reprod. Fertil., Suppl. 40, the onset of puberty in gilts is a function of

hypo-89–100. thalamo-pituitary maturation rather than attainment

Booth, P.J., Craigon, J., Foxcroft, G.R., 1994. Nutritional manipu-of specific body weight or composition parameters.

lation of growth and metabolic and reproductive status in We suggest that there may be an as yet undescribed _{prepubertal gilts. J. Anim. Sci. 72, 2415–2424.}

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Bryan, K.A., Hagen, D.R., 1991. Effects of nutrient intake and the peripubertal period, and management regimens

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Camous, S., Prunier, A., Pelletier, J., 1985. Plasma prolactin, LH, FSH and estrogen excretion patterns in gilts during sexual development. J. Anim. Sci. 60, 1308–1317.

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