Animal Science Publications Animal Science

1998 Biology and Genetics of Reproduction M. F. Rothschild Iowa State University, [email protected]

J. P. Bidanel Institut National de la Recherche Agronomique

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Abstract Reproduction, a process essential to maintenance of a species, must be under relatively strict genetic control. This genetic control must ensure that the steps in the reproductive process are repeated with great certainty and precision. Natural selection influenced these steps well before the pig was domesticated over 5000 years ago and humans applied artificial selection. However, nature did not remove genetic variation entirely and humankind has effectively altered the pig to fit ocs ial, food and environmental needs.

Disciplines Agriculture | Animal Sciences | Biology | Genetics

Comments This is a chapter from Rothschild, M. F. and J. P. Bidanel. 1998. Biology and genetics of reproduction. In:Genetics of the Pig, M. Rothschild and A. Ruvinksy (Eds.). CABI Press. pp. 313-343. Posted wtih permission.

This book chapter is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/ans_pubs/416 Biology and Genetics of Reproduction

M.F. Rothschild1 andJ.P. Bidanel2 1Iowa State University, Department ofAnimal Science, 225 Ki/dee Hall, Ames, IA 50011-3150 USA; 2Institut National de la Recherche Agronomique, Station de Genetique Quantitative et Appliquee 78352 jouy-en-josas Cedex, France

Introduction 313 Some Aspects of Pig Reproductive Biology 314 Male 314 Female 315 Traits of interest 316 Chromosomal Abnormalities 316 Between-breed Variation and Crossbreeding 318 Breed differences 318 Crossbreeding 320 Within-breed Genetic Variability 322 Components of genetic variation 322 Genetic correlations 324 Selection experiments 326 Inbreeding 328 Effects of Individual Genes 330 Conclusions and Implications 332 Acknowledgements 333 References 333

Introduction

Reproduction, a process essential to maintenance of a species, must be under relatively strict genetic control. This genetic control must ensure that the steps in the reproductive process are repeated with great certainty and precision. Natural selection influenced these steps well before the pig was domesticated over 5000 years ago and humans applied artificial selection. However, nature did not

©CAB INTERNATIONAL 1998. The Genetics of the Pig (eds M.F. Rothschild and A. Ruvinsky) 313 M.F. Rothschild and J.P. Bidanel I

remove genetic variation entirely and humankind has effectively altered the pig to fit social, food and environmental needs. A simple survey across breeds demonstrates that considerable genetic vari­ ability exists for several reproductive measures. Average litter size varies among breeds from 4 to 16 pigs per litter for mature sows. Mean age at puberty varies from 3 to 7 months of age. Clearly these breed differences, combined with evidence for genetic variability within breeds, suggest that substantial genetic improvement of reproductive performance in the pig is possible. Substantial gains in the efficiency of pig production systems can be ex­ pected from genetically improving reproductive traits (Tess et al., 1983; de Vries, 1989). Incremental costs related to the production of additional pigs are minimal so thac substantial gains can be achieved by improving the number of piglets weaned per breeding animal per unit of time. There is some evidence that genetic improvement of numerical productivity can be enhanced by genetically acting on its component traits, i.e. age at sexual maturity, fertility, prolificacy and piglet viability, or their underlying physiological processes. Genetic differences for reproductive traits have been observed both among and within breeds and lines. Differences among breeds and lines can be most effectively exploited through the use of crossbreeding. Within breed or line genetic variability is usually characterized by heritability and genetic correlation estimates which quantify the additive genetic variation that can be manipulated via selection of superior animals. The genes responsible for these genetic differ­ ences are usually not known. Yet recent advances in the pig genetic map (see Chapters 8 and 9) have made it possible to identify individual genes with large effects on reproductive traits. The purpose of this review is to provide and discuss recent evidence for the underlying genetic control of reproductive traits and methods of genetic improvement of these traits.

Some Aspects of Pig Reproductive Biology

Herd reproductive performance depends on complex physiological pathways which determine male and female reproductive performance such as age at sexual maturity, gamete production, libido, fertilization, embryo, fetal and piglet survival. This section only provides some basic features of sow and boar repro­ ductive biology which may be useful for understanding the rest of the chapter. More detailed elements on pig reproductive biology can be found in books such as Pond and Houpt 0978) and Cole and Foxcroft 0982).

Mak

Spermatogenesis in the boar starts at 4 to 6 months of age in most pig breeds, but may begin before 100 days of age in some early maturing breeds such as the Chinese Meishan breed. Sperm quality and quantity then steadily increase with testicular development, testosterone production and libido until sexual maturity IBiology and Genetics of Reproduction at 6 to 8 months of age and then at a much lower rate until boars reach their adult body size. A parallel rise in male accessory glands (seminal vesicle, prostate and bulbo-urethral glands), which produce 95% of the seminal plasma, results in a correlated increase in the volume of the ejaculate. Sexual activity is controlled by gonadotrophic hormones. Follicle stimulating hormone (FSH) stimulates sper­ matogenesis, whereas luteinizing hormone (LH) stimulates steroid hormones (testosterone, but also other steroids such as androstenone) synthesis and secre­ tion by the interstitial Leydig cells. The action of LH is dependent on the FSH induction of LH receptors on the Leydig cells. Boar ejaculate is characterized by its large volume (around 300 ml on average) and spermatozoa number (80 to 120 billion when semen is collected once a week), which corresponds to total sperm reserves and widely exceeds daily sperm production (10 to 20 billion 1 spermatozoa/ day- ). As a consequence, spermatozoa number per ejaculate steadily decreases when the boar is used or collected more than once a week, in spite of a slight increase in sperm production with ejaculation frequency. Large amounts of spermatozoa and semen are necessary to ensure normal conception rate and prolificacy (50 ml of semen and 3 billion sperm are usually considered as minimum requirements for artificial insemination). Frozen boar semen can successfully be employed, but leads to much lower conception rate and litter size than fresh semen, so that its commercial use is currently very limited. These peculiarities limit the use of either natural service (sow to boar ratio cannot exceed 12 to 15) or AI boars (which produce about 1000 semen doses per year) and consequently the dissemination capacity of favourable genes in breeding programmes.

Female

Puberty in gilts, which is usually defined as the moment of first ovulation, occurs at 3-4 months of age in the most early maturing breeds (Chinese) and at an average of 6-7 months of age in the most widely used Western pig breeds. It generally coincides with the first oestrus, though ovulation without external manifestation of oestrus (silent heat) occurs occasionally in pigs, and generates a steroid-secreting activity of corpora lutea. Ovulations then occur every 3 weeks during the second half of a 2-3 day oestrous period in the absence of gestation and have a mean duration of 2-3 hours. The oestrous cycle is control­ led by gonadotrophic hormones. FSH stimulates recruitment and development of ovarian follicles. Ovulation and corpora lutea formation are stimulated by LH. Ovulation rate increases with oestrus and parity number until the fourth or fifth parity. Conception rate in the pig is high (80-90%) and has increased with the generalization of double mating (two services 12 or 24 hours apart during oestrus). Ova fertilization begins a few hours after mating and lasts approxi­ mately 8 hours. Implantation occurs at about 18 days after fertilization, and gestation length averages about 114 days. The rate of prenatal mortality in pigs is 30 to 40% on average. The largest part of the loss (20 to 30%) occurs before or during the implantation period (Wrathall, 1971). As fertilization rate in pigs is 1316 M.F. Rothschild and J.P. Bidaned

generally close to 100% (Perry and Rowlands, 1962; Wrathall, 1971), most of the ova wastage is due to embryo mortality. An additional 10 to 15% loss occurs at pa1turition and during lactation, mainly during the first 3 or 4 days of life (Svendsen, 1992). With very few exceptions, the lactating sow has a very limited follicular development, does not ovulate nor show any oestrous symptom. The total removal of the sow from her litter at weaning normally results in an acceleration of follicular growth and in ovulation within 4-10 days.

Traits ofinterest

A list of reproductive traits of current or potential interest for pig breeding is given in Table 11.1. The reproductive efficiency of natural service boars may be characterized by their age at sexual maturity, their mating ability, the conception rate, the size of the litters resulting from their matings and their longevity. Important component traits are libido, aggressiveness, semen and sperm quan­ tity and quality. Traits of interest are rather similar for AI boars, but with a greater emphasis on semen and sperm quantity and quality and on the ease and frequency of semen collection. Components of litter size at weaning, i.e. ovulation rate, prenatal survival and piglet preweaning survival, are the most important contributors to sow numerical productivity (Tess et al., 1983 ; de Vries, 1989; Ducos, 1994). Other important component traits are uterine capacity (Bennett and Leymaster, 1989), maternal behaviour, teat number and milk production. Decreased age at puberty, which is expected to reduce generation inte1val and increase the sexual maturity of females at a given age, and reduced intervals from weaning to conception, which depend on both fecundity and sexual behaviour, are also associated with a better numerical productivity, but their economic value is lower than that of litter size.

Chromosomal Abnormalities

Though most genetic control occurs at the individual gene level, gross genetic abnormalities can also affect reproduction. The primary gross genetic abnormal­ ity affecting reproduction is when a chromosomal break happens and a recipro­ cal translocation occurs (see Chapter 8). Evidence of detrimental effects of reciprocal translocations on fertility and prolificacy have been reported (reviewed by Popescu, 1989). Reduction in litter size ranges from 5 to 100% and is primarily due to an increased embryo mortality (Popescu, 1989). A total of 68 reciprocal translocations involving all pig chromosomes except the Y chromo­ some have been reported so far (reviewed in Ducos et al. , 1997). Abnormalities of chromosome number have been found at relatively high frequencies (5-10%) in early pig embryos (Mcfeely, 1967; Fechheimer and Beatty, 1974; Long and Williams, 1982). These abnormalities generally lead to the death of embryos and may explain a significant part of prenatal mortality. As a consequence, such abnormalities have very rarely been found after birth. Exceptions include IBiology and Genetics of Reproduction

Kli nefelter (XXY) syndrome, Turner syndrome (XO) and occasionally trisomy. Other chromosomal abnormalities include intersexuality, which is one of the most frequent genetic defects in pig breeds (0. 1to0.4% according to Backstrom and Henricson, 1971). Such abnormalities are ra re and have generally a limited impact on overall reproductive effi ciency. A notable exception concerns boars carrying translocations, which reduce litter size of their matings and transmit

Table 11.1. Main reproductive traits of interest for animal breeding. Reproductive function Sex Main components or predictive traits Sexual maturity Male Age at first mating or sperm collection Testes size Size of Cowper's gland Female Age at first progesterone rise Age at first oestrus Sexual behaviour Male Ability to mount Female Visible symptoms of oestrus Mating stance Gonadocyte production Male Sperm quantity Semen volume (per ejaculate, per day) Sperm concentration Testes size (length, width, circumference, volume and weight) Sperm quality Sperm motility Proportion of: dead spermatozoa abnormal spermatozoa Female Ovulation rate Fertility Male Conception rate of mates Female Conception rate Weaning to oestrus interval Weaning to conception interval Number of service per conception Prolificacy Male Litter size of mates Female Fertilization rate Number of embryos or fetuses Embryo, fetus or prenatal survival rates Uterus size (length or weight of uterine horns) Uterine capacity Number of mummified piglets Number of piglets born or born alive Nursing abilities Female Number of piglets weaned Litter preweaning survival rate Teat number Milk production Hormone levels Male Testosterone level Female Progesterone level l318 M.F. Rothschild and J.P. Bidanel I

their abnormality to half of their progeny and may have important economic consequences at a herd or a breeding scheme level (Ducos et al., 1997).

Between-breed Variation and Crossbreeding

Breed di:fferences

Differences between pig breeds in reproductive traits have been reported by a number of authors, often in the context of crossbreeding studies. Though breed differences vary between experiments because of sampling, time-dependent or location-dependent variations, pig breeds can be classified into four main groups which differ in production and reproduction performance levels (Legault, 1985). Dual-purpose breeds, such as Large White, Yorkshire, Lanclrace and some original lines, exhibit a satisfactory level for both reproduction and production traits. Specialized 'paternal' breeds, such as Pietrain , Belgian Land­ race, Hampshire and Poland China and an increasing number of original strains, show medium reproduction and high production performance levels. Special­ ized 'maternal' breeds essentially include a limited number of native breeds from China, such as the group of the Taihu breeds (e.g. Meishan), which exhibit exceptional reproductive abilities, but poor production performance. Finally, there is a large group of 'native' breeds which generally have poor production and reproduction performance levels, but are well adapted to their particular environment. The reproductive performance of the first three groups of breeds only is considered here. Several surveys on the performance of prolific breeds of China have been published over the last 15 years (e.g. Zhang et al., 1983; Xu, 1985a,b) and have evidenced the early maturity, high prolificacy and good mothering abilities of the Meishan, Jiaxing, Fengjing, Erhualian and Minzhu breeds. The exceptional reproductive ability of th e Meishan breed has been confirmed under intensive management conditions of several European and American countries (see Table 11.2). Meishan gilts reach puberty about 100 days earlier than Large White gilts. Ovulation rate of Meishan gilts at first oestrus is rather low and inferior or similar to that of Large White pigs (Boler et al., 1986; Christenson, 1993). It then increases with oestrus number, so that Meishan gilts produce a larger number of ova than Large White gilts at the same chronological age. Meishan females also have a significantly higher conception rate than their Large White counterparts (Despres et al., 1992) and exhibit an average superiority for litter size at birth which ranges from 2.4 to 5.2 piglets. Larger litters of Meishan females come from a lower prenatal mortality (Bidanel et al., 1990a) or from the combination of a higher ovulation rate and a higher prenatal survival for a given ovulation rate (Haley et al., 1995). Meishan females have a similar or slightly lower proportion of stillbirths than Large White sows, but a higher preweaning mortality rate. However, as shown by Lee and Haley (1995) and Blasco et al. 0995), this larger mortality is essentially due to the higher litter size of Meishan sows at birth, as survival rate adjusted for the number of piglets born is clearly in favour of IBiology and Genetics of Reproduction

Table 11.2. Comparative reproductive performance of Chinese Meishan and European or American pig breeds . Western Western Trait Meishan1 breed1 breed used 2 Parity Reference Age at puberty (d) 92 (541) 197 (444) LW Despres et al. (1992) 96 201 y White et al. (1991) Ovulation rate 9.2 (13) 13.7 (15) LW 1 (1st oestrus) Bolet et al. (1986) 11.7(15) 14.4 (12) LW 1 (3rd oestrus) Bolet et al. (1986) 21.7 (30) 17.1 (32) c 1 Ashworth et al. (1990) 20.3 (38) 19.1 (19) LW 1-6 Bidanel et al. (1990a) 14.1 (18) 14.1 (19) LW 1 (4th oestrus) Hunter et al. (1991) 14.5 (20) 17.3 (17) c 1 Anderson et al. (1992) 24.9 (14) 15.2 (15) c 2-3 Anderson et al. (1992) 20.2 (19) 15.4 (14) c 1 Ashworth et al. (1992) 26 .2 (23) 18.3 (20) LW 3 Wilmut et al. (1992) 16.8(24) 14.7 (1 7) c 1 Christenson (1993) 27.8 (14) 20.7 (20) LW 3 Galvin et al. (1993) 22.7 (9) 16.3 (12) c 2 White et al. (1991) 19.2 (63) 15.1 (56) LW 1 Haley et al. (1995) 23.0 (33) 17.2 (28) LW 2 Haley et al. (1995) Conception rate (%) 93.0 (115) 85.2 (210) LW 1-4 Despres et al. (1992) Number born alive 14.0 (19) 10.7 (50) LW 1-3 Legault and Caritez (1983) 13.6 (93) 10.3 (44) LW 1-3 Bidanel et al. (1989) 11.9 (21) 9.5 (61) ws 1 Young (1990) 14.3(124) 10.3 (44) LW 1-4 Despres et al (1992) 11 .8 (21) 7.2 (20) y 1 White et al. (1991) 12.6 (148) 9.6 (84) LW 1-5 Bidanel (1993) 13.2 (63) 10.0 (56) LW 1 Haley et al. (1995) Prenatal survival 15.0 (33) 9.8 (28) LW 2 Haley et al. (1995) (%) 77.9 (38) 67.1 (19) LW Bidanel et al. (1990a) 65.0 68.8 LW 1 Haley et al. (1995) Perinatal survival 58.3 55.9 LW 2 Haley et al. (1995) (%) 96.0 (97) 90.8 (44) LW 1-3 Bidanel et al. (1989) 96.9 (148) 87.3 (84) LW 1-5 Bidanel (1993) Birth to weaning 91.6 94.1 LW 1-2 Haley et al. (1995) survival(%) 88.7 (93) 93 .9 (44) LW 1-3 Bidanel et al. (1989) 88.1 (148) 93.8 (84) LW 1-5 Bidanel (1993) Weaning to oestrus 81 .6 84.6 LW 1-2 Lee and Haley (1995) interval (days) 5.2 (87) 7.5(141) LW 2-4 Despres et al. (1992) 1Average performance (number of records). 2LW = Large White ; Y =Yorkshire; C = Crossbred ; WS =White synthetic. M. F. Rothschild and J.P. Bidanel I

Meishan sows. Finally, Meishan sows have shorter weaning to oestrus intervals than Large White sows (Despres et al., 1992). More detailed results on the reproductive characteristics of the Meishan breed can be found in several re­ views (e.g. Bidanel et al., l990b; Haley and Lee, 1993; Ashworth et al., 1996). Differences in reproductive performance between dual-purpose breeds are generally limited. However, Landrace gilts tend to reach puberty earlier (Christenson, 1981; Hutchens et al., 1982; Allrich et al., 1985; Bidanel et al., 1996a) while having a slighly lower ovulation rate and a higher prenatal survival rate than Large White gilts (e.g. Bidanel et al., I 996a). Paternal breeds generally have lower reproductive performance than dual-purpose breeds. Hampshire and Belgian Landrace sows show lower ovulations rates (-1.5 to -2 corpora lutea) and farrow about two piglets le_ss than Large White sows, Duroc and Pietrain sows being intermediate (see the review of Blasco et al., 1993). Paternal breeds also tend to have lower maternal abilities, as shown by higher prewean­ ing mortality rates as compared with Large White or Landrace breeds (reviewed by Blasco et al., 1995).

Crossbreeding

Pig producers have long known that crossbreeding is an effective means of improving reproductive performance. This improveme nt, called heterosis or hybrid vigour, comes from an increase in heterozygosity, which leads to better average genotypic values at dominant loci. As already mentioned, litter traits are controlled by the genes of both piglets and sows, and enhanced performance may come from crossed piglets (i.e. direct or individual heterosis effects) or crossed clams (i.e. sow or maternal heterosis effects). The plethora of cross­ breeding experiments makes it difficult to describe all of them but several reviews have been published (Sellier, 1976; Johnson, 1980, 1981; Gunsett and Robison, 1990). An attempt to summarize available data excluding crosses with prolific Chinese breeds is presented in Table 11.3. In terms of sow heterosis , there is an average reduction in age at puberty of 11.3 days for crossbred sows when compared with purebreds. In addition, crossbred females have 2-4% higher conception rates, slightly larger ovulation rates ( +0.5 ova) and 0.6 to 0.7 more piglets per litter at birth and 0.80 more piglets at weaning than purebreds. Postfarrowing survival of piglets is higher for crossbred sows (5%) and litter weights are greater ( + 1 kg at birth and +4.2 kg at 21 days). Litter heterosis effects lead to slightly larger litter size at birth ( +0.24 piglet per litter) and to higher piglet survival ( +5.8%) and litter weights. Crossbred sires have been compared with purebred boars in several experi­ ments (Wilson et al., 1977; Neely et al., 1980; reviewed in Buchanan, 1987). At a constant age, testis size and weight and total sperm are greater in crossbred than in purebred boars. Conception rates for first service or during extended breeding periods are higher (5-9%) for crossbred boars, and crossbred sires average 1.22 services per conception as compared with 1.41 services for purebreds (Johnson, 1981). Available results also suggest that crossbred boars have more libido and IBiology and Genetics of Reproduction

Table 11.3. Average heterosis effects for reproductive traits in crosses between Western pig breeds.1 Trait Heterosis value Number of estimates Dam heterosis Age at puberty (days) -11.3 13 Ovulation rate 0.52 7 Conception rate(%) 3.0 9 Litter size at 30 days of gestation 0.73 3 at birth 0.66 11 at 21 days 0.66 9 at weaning 0.84 9 Embryonic or prenatal survival rate(%) 6.7 3 Birth to weaning survival rate(%) 5.0 3 Litter weight (kg) at birth 0.93 9 at 21 days 5.04 7 at 42 days 15.0 3 Litter heterosis Litter size at 30 days of gestation 0.39 4 at birth 0.24 47 at 21 days 0.30 31 at weaning 0.49 16 Embryonic or prenatal survival rate(%) -1.1 5 Birth to weaning survival rate(%) 5.8 15 Litter weight (kg) at birth 0.59 33 at 21 days 2.47 29 at 42 days 13.35 12 1 Updated from Sellier (1976), Johnson (1981) and Gunsett and Robison (1990).

are more aggressive than purebred boars (Wilson et al., 1977; Neely and Robi­ son, 1983). Theoretically, crossbred boars should have more variable progeny than purebred boars but experimental results do not confirm this hypothesis. It should be noted that heterosis values may differ according to breed combinations. For instance, Large White x Landrace crosses generally exhibit lower heterosis values than other crosses between European or American breeds. Conversely, heterosis values in crosses between Large White and Mei­ shan breeds are two- or threefold higher than in Large White x Landrace crosses. Heterosis for age at puberty is around 40-50 days (Legault and Caritez, 1983). Sow heterosis effects on litter size at birth and at weaning exceed two piglets per litter, so that Meishan x Large White sows fa rrow larger litters than purebred Meishan (Bidanel et al., 1989; Bidanel, 1993; Haley et al., 1995; Lee and Haley, 1995). Similar results have been obtained with Chinese Fengjing and Minzhu breeds (Young, 1995). l322 M. F. Rothschild and J.P. Bidanel I

These crossbreeding results have been incorporated into crossbreeding programmes practised at the producer level. Comparisons of crossbreeding systems between European or American pig breeds have been conducted by several authors (e.g. Bennett et al. , 1983; McLaren et al., 1987). More recently, breeding organizations or companies have developed synthetic lines by cross­ ing breeds or lines known for high maternal performance such as the Meishan breed. These lines are then used as dam or more often grandam lines and crossed with dual-purpose breeds to produce F1 sows which are sold for cross­ ing with specific paternal genetic types (Bidanel, 1990; McLaren, 1990). Most individual pork producers practise crossbreeding through the use of specialized paternal and maternal genotypes. In some cases, they may also practise rotational or partial rotational crossbreeding programmes (reviewed in McLaren and Bovey, 1992).

Within-breed Genetic Variability

Components ofgenetic variation

Additive genetic variation is generally assessed by heritabilities. Estimates of heritability for several reproductive traits are summarized in Table 11.4. Regard­ ing male traits, testes and accesso1y gland measurements have moderate to high heritabilities and are expected to respond easily to selection, while sperm characteristics, testosterone level and libido traits are slightly less heritable. Female reproductive traits have low to moderate heritabilities. The most heritable traits are those depending solely on the genotype of the female, i.e. age at puberty, ovulation rate and weaning to oestrus interval. Conversely, litter size, conception and survival rates and, to a lesser extent, litter weight, which result from complex interactions between sow, boar and embryo or piglet genotypes, have low heritabilities and are therefore difficult to improve through selection. Several authors have quantified the relative importance of embryo and parental effects on genetic variation in litter traits. They have confirmed the prominent part of sow genotype, but have also shown that both progeny and boar geno­ types significantly influence litter traits. The service sire has a rather limited effect on litter size 0-5% of phenotypic variance) according to Ollivier and Legault 0967), See et al. 0993), Beauvois et al. 0997), but taking into account this effect has been shown to improve genetic evaluation models for litter size (Woodward et al. , 1993; Beauvois, 1996). Similarly, low but non-negligible additive direct genetic effects on embryonic survival ( 4% of phenotypic vari­ ance) and litter weight at 21 days (6% of phenotypic variance) were obtained by Gama et al. (1991) and Rodriguez et al. 0994), respectively. Some authors hypothesized that the preweaning environment provided by the female's dam, such as the size of the birth litter of the female, may have a significant effect on variation in litter traits and lead to underestimated herita­ bility values (e.g. Vangen, 1980) and lower than expected responses to selection (Van der Steen, 1985; Roehe and Kennedy, 1993). As reviewed by Haley et al. IBiology and Genetics of Reproduction

Table 11.4. Heritability estimates (ff) for male and female reproductive traits in the pig .1 Trait Number of estimates Mean ff Range Male traits Testis width 8 0.37 0.02-0.61 Testis length 6 0.33 0.30-0.39 Testis weight 5 0.44 0.24-0.73 Epididymis weight 4 0.33 0.15-0.55 Size of Cowper's gland 2 0.61 0.56-Q.66 Sperm quantity 3 0.37 0.31-0.42 Sperm motility 3 0.17 0.13-0.20 Basal testosterone level 2 0.25 0.14-0.37 Libido 13 0.15 0.03-0.47 Female traits Age at puberty 13 0.33 0-0.64 Standing reflex 1 0.29 Intensity of vulvar symptoms 1 0.24 Ovulation rate 15 0.32 0.10-0.59 Prenatal survival rate 9 0.15 0-0.23 Total number born 85 0.11 0-0.76 Number born alive 96 0.09 0-0.66 Number weaned 42 0.07 0-1.0 Piglet survival to weaning 16 0.05 0-0.97 Litter weight at birth 10 0.29 0-0.54 Litter weight at 21 days 15 0.17 0.07-0.38 Weaning to oestrus interval 4 0.25 0.17-0.36 Rebreeding interval 3 0.23 0.03-0.36 1Updated from Lamberson (1990), Mclaren and Bovey (1992) and Blasco et al. (1993, 1995).

(1 988), the impact of birth fraternity size on heritability estimates for litter traits is generally very small. Recent estimations of the heritability of this maternal effect have provided controversial results. Mercer and Crump (1 990), Haley and Lee 0 992) and Perez Enciso and Gianola 0992) found few or no maternal effects, while Southwood and Kennedy 0990), Ferraz and Johnson 0 993), See et al. 0993) and Irgang et al. (1 994) found significant estimates of maternal heritability ranging from 0.01 to Q.13. Differences between estimates may reflect sampling errors and genetic or management differences (e.g. crossfostering) between populations. However, as shown by Roehe and Kennedy 0993), ignoring maternal genetic effects which are negatively correlated with direct effects leads to reduced selection response as a result of negative maternal response and reduced direct response even when maternal heritability is low. Suggestions that the genetic correlations between successive litters might be substantially less than one have also been put forward to explain lower than expected response to selection for litter size. In their review of early work on this topic, Haley et al. 0988) showed that genetic correlations between adjacent parities are high and considered that the lower estimates obtained between 1324 M.F. Rothschild and J.P. Bidanetl

non-adjacent litters are likely to be biased downward due to culling. Recent studies using statistical methods accounting for selection bias have given contro­ versial results. In the Yorkshire breed Irgang et al. 0994) and Roehe and Kennedy 0995) obtained genetic correlations between first and second parities ranging from 0.17 to 0.59 and recommend the use of a multiple-trait model. Conversely, estimates of genetic correlations between parities reported by Al­ fonso 0995), Roehe and Kennedy (1995) and Beauvois 0996) in the Landrace breed were close to unity. Finally, crossbreeding studies indicate that non-additive genetic effects may be important for most reproductive traits. Though ignoring this variability may substantially bias estimates of additive genetic effects (Johansson et al., 1994), there is, to our knowledge, no estimate of non-additive genetic parameters of reproductive traits in pigs.

Genetic correlations

Phenotypic and genetic correlations between male genital tract measurements are generally large (Legault et al., 1979; Toelle et al., 1984; Bonneau and Sellier, 1986). Testes measurements are also favourably related to total sperm or per cent spermatogenesis (Wilson et al., 1977; Toelle et al., 1984; Young et al., 1986), as well as to basal or induced LH and testosterone levels (Bates et al., 1986; Lubritz et al., 1991). A number of researchers have examined the interest of male traits as indirect selection criteria to improve female reproductive per­ formance. Estimates of genetic correlations between testes measurements and age at first oestrus, ovulation rate or litter size are generally low and do not show any consistent trend (Schinckel et al., 1983; Toelle and Robison, 1985; Bates et al., 1986; Benoit, 1986; Young et al., 1986; Sellier and Bonneau, 1988; Johnson et al., 1994). Phenotypic and genetic correlations between several female traits are shown in Table 11.5. Age at puberty exhibits negative, i.e. favourable, genetic correlations with ovulation rate and number of embryos (Young et al., 1978; Bidanel et al., 1996a). Conversely, both negative and positive estimates of genetic correlations with litter size have been reported (Young et al., 1978; Rydhmer et al., 1992). Genetic parameters for litter size at birth and its com­ ponents, i.e. ovulation rate and embryo or fetal survival, have recently been reviewed by Blasco et al. 0993). Ovulation rate and prenatal survival show a moderate negative correlation. Litter size at birth appears to be more closely related to prenatal survival than to ovulation rate. Measurements of litter size at birth (total number and number born alive) and at weaning (number weaned) and litter weight exhibit large positive genetic correlations (reviewed by Blasco et al., 1995). However, they appear to be unfavourably correlated with stillbirth or preweaning mortality rates (Blasco et al., 1995). Numerous authors have estimated genetic correlations of male or female reproductive traits with growth and carcass traits. Testes measurements show favourable genetic relationships with growth traits when measured at a constant IBiology and Genetics of Reproduction 3251

Table 11.5. Means 1 of literature estimates of genetic and phenotypic correlations2 among reproductive traits. AP3 OR NB NBA s NW LBW L21W AP -0.08 0.04 0.04 0.08 0.10 -0.15 -0.11 OR 0.06 0.08 0.25 -0.38 0.10 0.17 0.09 NB -0.02 0.12 0.91 -0.1 1 0.73 0.62 0.45 NBA -0.03 0.13 0.92 0.16 0.81 0.65 0.61 s 0.11 -0.11 - 0.15 -0.05 0.53 0.13 0.80 NW 0.01 0.05 0.71 0.79 0.59 0.70 0.87 LBW -0.02 0.09 0.79 0.82 0.09 0.71 0.68 L21W -0.03 0.02 0.44 0.53 0.60 0.80 0.61 1Updated from Lamberson (1990) and Blasco et al. (1993, 1995). 2Genetic correlations above the diagonal , phenotypic correlation below. 3AP =age at puberty; OR= ovulation rate ; NB= number born; NBA= number born alive; S = preweaning survival rate ; NW= number weaned; LBW =litter weight at birth; L21 W = 21-day litter weight. age (Toelle et al., 1984; Young et al., 1986; Lubritz et al., 1991 ; Johnson et al., 1994), but relationships are less clear when measurements occur at a constant weight (Benoit, 1986; Young et al., 1986). Estimates of genetic correlations with backfat thickness are generally low and have a varying sign (Toelle et al., 1984; Young et al., 1986; Johnson et al., 1994). Growth traits also appear to be favourably associated with testosterone levels in the study of Lubritz et al. 0991). Similarly, age of gilts at puberty exhibits negative, i.e. favourable, genetic correlations with growth rate (Reutzel and Sumption, 1968; Young et al., 1978; Hutchens et al., 1981; Rydhmer et al., 1992; Bidanel et al., 1996a), while both negative (Rydhmer et al., 1992; Bidanel et al., 1996a) and null or positive (Young et al., 1978; Hutchens et al., 1981; Hixon et al., 1987) relationships with backfat thickness have been reported. Litter size or weights and growth or carcass traits are weakly correlated (reviewed by Brien, 1986 and Haley et al., 1988). Recent estimates of genetic correlations between growth/ carcass and litter traits (Short et al., 1994; Rydhmer et al., 1995; Ducos and Bidanel, 1996; Kerr and Cameron, 1996) generally agree with previous estimates, although some significant estimates were obtained by Ducos and Bidanel 0996) and Kerr and Cameron (1996). Growth rate and to some extent carcass lean content might also be unfavourably correlated with intensity of oestrous symptoms, as reported by Rypopulation was reported by Fouilloux et al. 0997). Results reported by Willeke et al (1987) and Sellier and M.F. Rothschild and J.P. Bidanel I

Bonneau (1988) suggest that low fat androstenone level in young boars and sexual precocity in gilts and young boars are genetically antagonistic. The few available estimates of the genetic relationships between reproduction and the meat technological quality are still inconclusive. Litter size at birth was found by Hermesch et al. 0995) to have insignificant relationships with pH or drip loss, but negative genetic correlations with meat colour (-0.50 ± 0.17 and -0.53 ± 0.24, respectively for second and third parity litter size). Similarly, Larzul 0997) reported non-significant genetic correlations between muscle glycolytic potential (GP) and litter size or weight, but a negative genetic relationship between GP and age at puberty.

Selection experiments

Several selection experiments dealing with various reproductive traits have been conducted over the last 30 years in pigs. Most experiments attempted, directly or indirectly, to improve litter size. There have been several selection experiments for directly increasing litter size (Ollivier and Bolet, 1981; Bolet et al., 1989; Lamberson et al., 1991). Most of these experiments produced little or no signifi­ cant response. Ollivier and Bolet (1981) conducted a selection experiment based on average litter size in the first two parities. After 11 generations of selection in a closed line, total response was only 0.26 piglets and not significant (Bolet et al., 1989). However, five subsequent generations of selection within the same line - with 12.5% immigration from the hyperprolific stock described below-yielded a significant genetic gain (Bolet et al. , 1987). Lamberson et al. 0991) conducted a selection for litter size for eight generations following previous selection for high ovulation rates. Realized heritability was 0.15 ± 0.05 and response after eight generations was estimated to be 0.48 to 1.06 pigs, depending on the method of analysis. Rutledge (1980) also attempted to improve litter size by correcting for fraternity size but response was not significant. McLaren and Bovey 0992), in reviewing these experiments, suggested that the failure or limitations of these experiments was due to several reasons including popula­ tion size, management problems, maternal effects, inbreeding depression and within-family selection. Hyperprolific selection is another way of increasing litter size. Such a scheme, which implies extremely intense selection of sows on several litters, combined with backcrossing of their sons to sows of similar high prolificacy, was initiated in France 20 years ago (Legault and Gruand, 1976). Results of the French hyperprolific Large White strain after 20 years showed a genetic super­ iority of 1.4 pigs/litter (born alive) compared with normal contemporary Large White sows (Bidanel et al., 1994). Hyperprolific sows also had larger ovulation rates, lower age at puberty and FSH concentration at 150 days of age and increased follicle oestradiol concentrations during the follicular phase of the oestrous cycle (Despres et al., 1992; Driancourt et al., 1992; Driancourt and Terqui, 1996). Other countries and pig breeding companies have practised hyperprolific selection with positive results (e.g. Sorensen and Vernesen, 1991). IBiology and Genetics of Reproduction 3271

Using total pigs born in five litters, the Pig Improvement Company selected the top 1.7% of their sows and responses to hyperprolific selection experiments have been nearly as high as in the French experience (D.G. McLaren, PIC USA, personal communication). While heritabilities for litter size are relatively low (around 0.10), heritabili­ ties for ovulation rate and embryo survival appear to be higher (Table 11 .4). Such estimates have encouraged researchers to consider selection based on components of litter size (ovulation rate, embryo survival and uterine capacity). Initiai experiments at the University of Nebraska dealing with ovulation rate gave a direct response of 3.7 ova (Cunningham et al., 1979) and an indirect response of 0.8 pigs per litter (Lamberson et al., 1991) after nine generations of selection. Following 11 generations of relaxed selection an advantage of 0.74 pigs per litter was maintained (Lamberson et al., 1991). Increased ovulation rate was associated with a faster increase in FSH concentration and a higher FSH peak (Kelly et al. , 1988). Bidanel et al. (1996b) selected two Large White lines for either increased ovulation rate or increased prenatal survival. After four generations of selection, ovulation rate had increased by 0.6 ova/ generation in the high ovulation rate line, but without any correlated response on litter size. Conversely, no significant genetic trends were obtained in the line selected for prenatal survival. Johnson et al. (1984) proposed that index selection for both ovulation rate and embryo survival would be more effective in increasing litter size. Early response over five generations of selection was 0.19 pigs/ litter/ generation (Neal et al., 1989) and more recent results at generation ten show a difference be­ tween the control and select lines of 6.6 ova, 3.3 fetuses at day 50 of gestation and 1.5 pigs born alive (Casey et al., 1994). Selection for ovulation rate and embryo survival resulted in differences in the pattern of oestradiol secretion in young males before puberty and in enhanced FSH secretion in mature boars (Mariscal et al. , 1996). A model in which litter size is the minimum number of viable embryos (a function of ovulation rate) or the minimum allowed by uterine space has been proposed tissue (Huang and Johnson, 1996). Daily sperm production and sperm epididymal storage also M. F. Rothschild and J.P. Bidane"

increased more rapidly at younger ages in the selected than in the control line (Rathje et al., 1995). Age at puberty decreased by 6 days, but not significantly, in the line selected for higher testicular development when compared with the control line. Ovulation rate also increased by 0.76 ± 0.43 ova in the females of the testicular selection line Qohnson et al., 1994). Johnson and co-workers concluded that testis weight might be used as a selection criterion for improving semen characteristics of Al boars, but should not be used as an indicator trait for genetically improving female reproductive performance. A significant direct response was obtained by Hixon et al. (1987) after one generation of divergent selection for age at puberty. Results from another selec­ tion experiment on age at puberty were reported by Lamberson et al. (1991). The line involved was selected for decreased age at puberty for eight genera­ tions following selection for increased ovulation rate. Age at puberty decreased by about 2 days/generation and realized heritability was 0.25 ± 0.05. Age at puberty was not associated with increased litter size in this selection line. More recently, selection on circulating levels of testosterone was con­ sidered. Robison et al. (1994) initiated a divergent selection experiment on gonadotrophin-releasing hormone challenge. Pre-challenge and post-challenge levels of testosterone in the high line were three times those of the low line after ten generations of selection. Heritabilities for pre- and post-challenge testost­ erone levels were moderate. Prolificacy of the high line females was significantly larger than that of the low line females. A selection experiment to reduce the inte1val from weaning to oestrus (IWE) has been practised for eight generations in The Netherlands. Realized heritability was estimated to be 0.17 (ten Nape! et al., 1995a). However, tl1e experiment also provided some indication of a genetic antagonism between IWE and litter traits (ten Nape!, The Netherlands, personal communication). Ten Nape! et al. Cl995b) divided IWE into the interval between weaning and the start of cyclic activity, the interval between the start of cyclic activity and oestrus, the incidence of silent oestrus and the cycle length. They concluded that genetic variation in IWE is mainly due to genetic variation in the interval of weaning to the start of cyclic activity.

Inbreeding

Inbreeding occurs when related animals are mated and is quantified by a coefficient which measures the probability that the two genes at any locus in an individual are identical by descent (i.e. descend from the same allele carried by a particular ancestor). The inbreeding coefficient F ranges from 0 (completely outbred) to 100% (completely inbred). Inbreeding was first used by breeders to help fix specific genetic characteristics in an effort to help develop breeds. In the United States, inbred lines of pigs were created in the early 1930s for further use in crossbreeding (Craft, 1958). These lines mirrored the extremely successful results obtained in the hybrid corn business. In pigs, inbred lines suffered from much lower fertility, lower piglet survival rates and some IBiology and Genetics of Reproduction reduction in general performance (Craft, 1958), so that this method of improve­ ment has been abandoned. The genetic effect of inbreeding is to increase homozygosity, which is undesirable for three reasons. First, it causes a loss in genetic variation and hence reduces the potential rate of genetic progress. Then it increases the frequency of genetic abnormalities by increasing the number of animals homozygous for recessive deleterious alleles which had been pre­ viously hidden in the population. Finally, the reduced proportion of hetero­ zygous individuals will result in lower average genotypic value at dominant loci and hence will cause a decrease of the performance levels. This decrease is called inbreeding depression and is generally larger for the least heritable traits and increases with additional amounts of inbreeding. Inbreeding occurs in any population of finite size and accumulates more rapidly in smaller and in selected populations. Rates of inbreeding depression for some reproductive traits are presented in Table 11.6. As litter traits depend on dam and offspring genotypes, the effects of inbreeding should be considered at both levels too. Though estimates are not numerous, dam inbreeding seems to strongly reduce ovulation rate and prenatal swv ival. Litter inbreeding causes an additional reduction of 0.60 embryos per 10% increase in Fat 25 days of gestation. Estimated decrease in total number of piglets born from a 10% increase in dam inbreeding coefficient is 0.40. The greatest effects of inbreeding are seen in reduced su1vivability of piglets. Estimates range from a decrease of 0.30 to 0. 50 piglets for each 10% increase in litter inbreeding with an additional decrease of 0.20 to 0.40 piglets for each 10% increase in dam inbreeding. In the male , the effects of inbreeding are reduction in sperm numbers and sexual aggressiveness or libido.

Table 11.6. Effect of 10% increase in inbreeding coefficient of litter and dam on reproductive performance. Litter Dam Trait N1 Mean Range N Mean Range Ovulation rate 2 -1.13 -1 .13 to-0.55 Embryo number at 25 days -0.60 2 -1.75 -2.7 to - 0.8 Embryo survival to 25 days(%) -3.30 2 -5.62 -10.9 to -0.33 Litter size Total number born 15 -0.29 -2.53 to 0.13 12 -0.40 -1.29 too Number of stillborn 2 -0.27 -0.37 to -0.16 2 -0.19 -0.28 to-0.10 Number born alive 6 0.01 -0.20 to 0.17 4 -0.30 -0.63 to 0 Number at 21 days 8 -0.53 -2.78 to 0.20 7 -0.22 -0.43 to 0.03 Litter weight (kg) at birth 10 -0.15 -0.64 to 0.20 7 -0.46 -1.12 to-0.07 at 21 days 6 -1.72 -3.35 to 0.10 5 -2.18 -4.33 to -0.91 Source: Johnson, 1990. 1N =number of estimates. M. F. Rothschild and J.P. Bidanel I

Effects of Individual Genes

The limited genetic improvement made by selection and crossbreeding for female and male reproductive traits has encouraged a search for single genes affecting reproduction. Recent developments in segregation analysis and in the area of gene mapping and molecular genetics have now made it possible to search for major genes and quantitative trait loci (QTL) and to study candidate genes which may control reproductive traits. Early research in this area centred on blood groups and protein polymor­ phisms and their association primarily with litter size and on the estimation of potential pleiotropic effects of known major genes. First evidence for such associations was provided by Jensen et al. (1968) and Rasmusen and Hagen 0973), who reported an association between the H locus, located on pig chromosome 6, and litter size, with an unfavourable apparent effect of the ff' allele and by Kristjansson (1964) and Imlah 0970) who reported an apparent effect of alleles at the transferrin locus, located on pig chromosome 13, on pig fertility and prolificacy. However, this transferrin locus effect was not confirmed by other authors (e.g. Jensen et al., 1968; Huang and Rasmusen, 1982). Several other associations between blood group and protein loci and reproductive traits have been investigated, but they have often led to contradictory results (reviewed by Ollivier and Sellier, 1982). During the 1980s, considerable efforts were made to investigate the role of the pig major histocompatibility complex (MHC), called the swine leucocyte antigen (SLA) complex on male and female reproductive traits (reviewed in Warner and Rothschild, 1991). The pig MHC is a large set of genes located on chromosome 7 (Warner and Rothschild, 1991). Certain MHC genotypes have been associated with increased or decreased testicular size and hormone differ­ ences and 1.5-5% of the phenotypic variation in these traits was explained by the pig MHC(Rothschild et al., 1986b). In the female , several traits appear to be associated with the SLA polymorphism. Several reports link the MHCto ovula­ tion rate (Rothschild et al., 1984; Conley et al. , 1988), litter size, number born alive and number weaned (reviewed in Vaiman et al., 1988; Warner and Rothschild, 1991). There is some evidence suggesting that MHChomozygosity of the embryo may be a disadvantage (reviewed in Vaiman et al., 1988). Researchers have also examined whether the pig has a MHC gene associated with embryo development and its relationship to litter size. Results from minia­ ture pigs (Ford et al., 1988) suggest that such a gene may exist within the pig MHC. Other reports (Rothschild et al., 1986a; Vaiman et al., 1988; Warner and Rothschild, 1991) indicate that the MHC is associated with birth and weaning weights. Whether these effects are direct effects of genes within the MHCsuch as 21-hydroxylase, or are due to linkages with other genes outside the complex is unknown. Further cloning and identification of individual genes on chromo­ some 7 should help to answer that question. Recent discoveries such as the FEC(fecundity) gene marker in sheep have encouraged the search of individual genes affecting pig reproductive traits. Of initial interest was the investigation of why some Chinese breeds of pigs, like the IBiology and Genetics of Reproduction

Meishan, are so prolific. In 1991, Rothschild and colleagues began a candidate gene investigation of the role of the oestrogen receptor (ESR) gene in controlling litter size. Initial results showed that one £SR polymorphism found initially in the Meishan and later in the Large White breed (Rothschild et al., 1994) was associated with improved litter size in a Meishan x Large White composite line. More recent results (Rothschild et al., 1995, 1996) demonstrate that ESRis either a major gene or very closely linked to a major gene for litter size. In the above mentioned line, the favourable B allele is associated with a first-parity additive effect of+ 1.15 pigs/ litter for each copy of the allele. In second and later parities, the effect of the Ballele is about +0.5 pigs/ litter and appears to act in a dominant manner. The B allele is also segregating in several Large White populations (Rothschild et al., 1995, 1996; Legault et al., 1996), and is approximately +0.4 pigs per litter in first parity and +0.3 pigs in later parities (Short et al., 1997) but the effect of the B allele seems to differ between populations. These differences may indicate either that the mutation used in the ESRtest is only a linked marker gene or that differences in the genetic background have an impact on the expression of the ESR locus. In any case, the underlying mechanisms of the favourable ESR allele are still unknown but it has been hypothesized that ESR may affect embryo survival. Progress achieved in the pig genetic map during the last 5 years (see Chapters 8 and 9) now gives the opportunity to begin the systematic search for loci affecting quantitative traits of economic importance. First results dealing with marker gene effects on reproductive traits using this systematic approach indicate associations between the microsatellite marker Sw444 region on chromosome 8 and ovulation rate or uterine length in a cross between Meishan and Large White breeds (Wilkie et al., 1996). Other associations involving one chromosome 6 region, which seems to differ from the H blood group locus region, and number born per litter, as well as regions of chromosomes 4 and 7 and number of stillborns, were suggested by Wilkie et al. 0996). A QTL for ovulation rate was also found on chromosome 8 in a cross between a line selected for ovulation rate and a control line (Rathje et al., 1996). Several genes with major effects on economically important traits have been evidenced in pigs. The most widely studied gene is the skeletal muscle ryanodine receptor or halothane sensitivity (HAL) locus, which has major effects on several carcass and meat quality traits in pigs (see Chapter 14). Various but fairly inconsistent effects of the HAL locus on male and female reproductive performance have been reported. Schlenker et al. (1984) found a smaller ejacu­ late volume and a lower number of sperm for halothane-negative (HN) as compared with halothane-positive (HP) boars while an opposite conclusion was reached by Hillbrand and Glodek 0984). Pfeiffer et al. 0986) reported a better semen quality in HN than in HP boars. Schneider et al. 0980) in the Swiss Landrace, Baulain and Glodek (1987) in the German Landrace and Sellier et al.(1987) in the Pietrain found a favourable sire effect of HP boars on litter size at birth, while Lampo et al. 0985) in the Belgian Landrace breed and Sellier et al. (1987) in the Pietrain x Large White cross did not find any noticeable difference. With regard to fertility traits, HP sows appear to be similar or even 1332 MF. Rothschild and J.P. Bidanetl

slightly superior to HN sows in the ability to become pregnant (Van der Steen, 1983; Simpson et al., 1986; Baulain and Glodek, 1987; Sellier et al., 1987). A significant advantage of HN over HP sows for number born per litter was reported by Schneider et al. (1980) in the Swiss Landrace ( +0.55 piglet born alive), by Van der Steen (1983) in the Dutch Landrace ( + 1.3 piglet born/ litter) and by Carden et al. (1985) in Pietrain-Hampshire composite lines ( + 1. 20 ± 0 .4 piglet born/ litter). Several studies on the German Landrace breed (e.g. Willeke et al., 1984; Grosse-Lembeck and Kalm, 1985; Haulain and Glodek, 1987) also showed a slightly, but non-significantly better prolificacy of HN sows as com­ pared with HP sows. Conversely, Simpson et al. (1986) and Sellier et al. (1987) did not find any difference in litter size between halothane phenotypes. As suggested by Sellier et al. 0987), the differences observed between studies tend to indicate that the halothane locus has no direct effect on reproductive perform­ ance, but may be in linkage desequilibrium with the H blood group chromo­ somal region in some populations. Other major genes such as the RN gene (Le Roy et al. , 1990a), the MU gene (Le Roy et al., 1990b), the IMF gene Qanss et al., 1997) or a gene with a major effect on the size of bulbo-urethral glands (Fouil­ loux et al., 1997) have recently been evidenced in pigs, but their effect on reproductive traits has not been investigated so far.

Conclusions and Implications

Large genetic differences for reproductive traits exist both among and within pig breeds. Between-breed variations have been widely exploited over the last decades through breed specialization and the generalization of crossbreeding. Conversely, little had been done until recently to profit from the within-breed variability. Selection plans have mainly been aimed at improving production traits and generally have neglected the least heritable reproductive traits. Things have begun to change over the last 10 years due to the combination of several factors. The economic interest in reducing backfat thickness is now limited in many countries, whereas much can be gained from improved sow and boar reproductive performance. Experimental results have shown that the least heri­ table traits such as litter size could be successfully selected for in certain circum­ stances. The use of powerful across-herd genetic evaluation techniques based on Best Linear Unbiased Prediction methodology (e.g. Henderson, 1984) have given geneticists the opportunity to substantially increase the efficiency of selection of these least heritable traits. As a consequence, litter size has become a major component of selection goals in maternal lines of pigs and annual genetic trends of +0.1--0.3 piglet/ litter have been obtained in some pig popula­ tions over the last few years. Further gains in prolificacy, but also in sexual maturity and mothering abilities, can be expected in the near future from the increasing use of prolific Chinese breeds or of synthetic lines developed using these prolific breeds in crossbreeding plans. The use of genetic markers should also contribute to more efficient genetic improvement of reproductive traits, which are sex limited and IBiology and Genetics of Reproduction

often have a late expression in life. Genes like ESR and genetic markers can be used for marker-assisted introgresssion of favourable genes affecting reproduc­ ti on from Chinese prolific breeds into commonly used maternal geneoypes, for removing unfavourable alleles for fa tness in Chinese x Western synthetic lines or for marker assisted selection within populations. However, as discussed by Visscher and Haley (1 995), the use of geneti c markers is associated with poten­ tial extra gains, but also with extra costs and risks due to poor estimates of QTL position and effects or detection of spurious QTLs. Further research to develop high density maps, to identify the genes responsible for the observed variations and to study gene effects on economically important traits and their underlying physiological processes will be very useful to solve these problems. Other reproductive traits are likely to have an increasing impo1tance in fu ture genetic improvement programmes. The increasing number of piglets per litter and the regulations against early weaning of piglets should enhance the importance of mothering abilities. They can be measured through number of piglets weaned or preweaning survival rate, although some bias may arise from piglet exchange across litters. They can also be characterized through component traits such as behavioural traits, milk production and associated traits such as sow feed consumption during lactation. Other reproductive traits, such as boar semen quality and quantity, boar and sow longevity, might also be worth considering.

Acknowledgements

The authors would like to thank Louis Ollivier, Pierre Sellier and the anonymous referees for their useful comments and suggestions.

References

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