(Mini review)

Use of the Syrian hamster, Mesocricetus auratus, in selection for fertility in animal breeding 1. Physiology of reproduction for selection experiments

Masahiro SATOH

Genetic Diversity Department, National Institute of Agrobiological Sciences

1. Introduction reproductive performance of cattle, sheep, and pig The Syrian hamster, Mesocricetus auratus, has been populations with particular attention to variations in used as a laboratory animal for three-quarters of a century. ovulation rate, litter size, and embryo survival. Rydhmer It is the most commonly used of several related species that (2000) discussed the possibility of improving different sow include the Chinese hamster (Cricetulus griseus) and, more reproduction traits, such as age at puberty, estrous recently, the grey hamster (Cricetulus migratorius), which symptoms, and ability to become pregnant. At the are bred in captivity and used in biological and medical University of Nebraska in the U.S.A., litter size at birth in research laboratories (Fulton 1968). Recently, the Syrian pigs and its components have been selected, and direct and hamster has been used as a pilot animal for improving correlated responses such as ovulation rate, uterine fertility in domestic livestock (Furukawa et al. 1988; Satoh dimensions, and uterine capacity have been investigated et al. 1997, 1998c; Ishii et at. 2003). (Gama & Johnson 1993; Ruiz-Flores & Johnson 2001; So far animal breeders have selected mainly for Mesa et al. 2003; Petry & Johnson 2004; Petry et at. 2004). litter size at birth in pigs and sheep, litter weight at weaning Testicular characteristics have been studied for their genetic and number of teats in pigs, multiple births in sheep, and relationship with female reproductive traits in pigs weaning weight in beef cattle in studies of reproductive (Schinckel et al. 1983; Toelle & Robison 1985; Young et performance of livestock. They have also studied age at at. 1986; Johnson et al. 1994) and in sheep (Land & Can puberty, age at first service, and age at first calving in 1975; Hanrahan & Quirke 1977). studies of sexual maturity (Holm et at. 2004b; Serenius et Traits for selection in livestock should be not only at. 2004b); percentage of live births and prenatal and pre- economically important, but also easy to measure. In pilot weaning survival in studies of productivity of the dam tests of selection methods, laboratory animals offer (Lund et at. 2002; Leenhouwers et at. 2003); return rate advantages over livestock in having a much shorter lifespan after parturition, duration of parturition, the need for birth and traits that are easy to measure. Kent (1968) reviewed assistance, and lactation length in studies of fertility for the existing knowledge of reproductive physiology of the management of the dam (Holm et at. 2004a, 2005); Syrian hamster. My group has explored the reproductive gestation length, interval from weaning to first service, and physiology of the Syrian hamster for selection experiments number of parturitions in a lifetime in studies of long-term since the 1980s. The objectives of this paper are to reproduction (Moeller et at. 2004; Serenius et at. 2004a; summarize current knowledge and to introduce our results Holm et at. 2005); and testicular growth in studies of male of recent experiments in fertility of Syrian hamsters. reproductive efficiency (Wilson et at. 1977; Neely & Robison 1983). Response to selection could be improved if some characteristics could be used as a predictors of the Correspondence: Masahiro Satoh, Genetic Diversity Department, reproductive efficiency of genetically related selected traits. National Institute of Agrobiological Sciences, Tsukuba 305-8602, Hanrahan (1982) reviewed evidence for genetic variation in Japan (e-mail: hereford@ affrc.go.jp)

Journal of Animal Genetics (2005) 32(2), 55-64 55 M. Satoh

2. General reproductive capacity (Satoh et al. 1999a). These differences indicate that the Reproductive features generation interval is affected by genetics. It also depends The lifespan of the Syrian hamster varies between 1 on environmental factors such as nutrition and housing. In and 3 years, though over 2 years is uncommon. Females long-term selection experiments, 4 generations per year are tend to mature about 2 weeks earlier than males, which desirable. apparently reach maturity at between 40 and 60 days of age (Magalhaes 1968a). Females can breed at about 6 weeks of Diet for optimum reproduction age, but they should be bred first when they are between 8 Commercial pelleted diets for hamsters are and 14 weeks of age because of small litter size at birth and available, similar to those used for other laboratory animals weaning before 8 weeks and low conception rate after 14 such as mice and rats, catering to the Syrian hamster's weeks. Sexually active females have a 4-day estrous cycle specific digestive system (e.g., Matsumoto 1955; Hoover et (Table 1). al. 1969), especially forage digestive ability (Manila & The breeding span of females is about 10 to 13 Takano 1976; Manila & Gotoh 1976; Shinohara et al. months, and pregnancy rate decreases after 9 months 1989). However, few reliable investigations of the (Okuki 1972). The use of over-age females is sometimes the hamster's feed requirements for reproduction have been cause of breeding failures. Pregnancy rate may decrease made. Our group reported that Syrian hamsters raised on after the third parity. However, males have sired litters at fibrous feed before mating age gave optimal reproductive about 2 years of age. Females of inbred strains over 12 performance (Satoh & Obata 1995). In general, diets must months of age rarely breed, but we have found difference supply sufficient vitamins B1, C, and D, and fat females among lines. In general, synthetic strains have a longer should be avoided for optimal reproduction. breeding span than inbred strains. The generation interval depends on the age of sexual 3. Estrous cycle and mating maturity, pregnancy rate, and parturition interval. Under a Estrus cycle harem-mating system, the average generation intervals from Nakano (1960) observed the first corpora luteal at weaning of 3 inbred lines were 65.5, 78.4, and 85.3 days 30 days. But Kupperman et al. (1944) reported that luteal

Table 1. Breeding data for Syrian hamsters

1) Festing (1972) . 2) Author.

Journal of Animal Genetics (2005) 32(2), 55-64 56 Use of Syrian hamster in animal breeding 1. Physiology of reproduction

formation and cyclic changes in the vagina were not On the morning following ovulation, a creamy white, thick, initiated until the 33rd to the 38th day. The first opaque, stringy, viscous, mucous discharge with a lingering spontaneous estrus is about 5 weeks, but it depends on pungent odor fills the vagina. This avoids the need for tools genetics and nutrition. such as a microscope. If this characteristic postovulatory The Syrian hamster exhibits regular ovarian cycles discharge does not ooze out of the vaginal orifice while the with ovulation every 4 days. The cycle is classified into 4 animal is being handled, gentle pressure at the sides of the stages: proestrus, estrus, metestrus, and diestrus (Figure 1). orifice will cause it to exude. The discharge occurs from the Typical durations of proestrus, estrus, and metestrus are end of estrus through metestrus. The external signs continue approximately 3, 12, and 4 hours, respectively. The onset of in the morning. psychic estrus occurs approximately 8 hours before At this stage, the number of ova can be determined ovulation in any single animal, and the time of onset is by flushing out the ampulla of the oviduct with saline therefore a guide to the approximate time of ovulation. containing 0.5 % hyaluronidase and counting under a Most Syrian hamsters ovulate 8 to 9 hours after the onset of stereomicroscope. On the next day following the sign, the psychic estrus. Orsini (1961) reported that ovulation was number of fertilized (2 cells or more) and unfertilized ova under way approximately 7 hours after the onset of can be counted by this method if the female was mated at darkness. It is a common observation that psychic estrus the previous estrus. The number of ova can be also counted commences at dusk or within an hour or 2 thereafter. by observing the corpus luteum. About 3 hours after ovulation, the liberated ova have Our group reported means of 10.4 total and 9.7 reached the ampulla of the oviduct. The diameter of the normal ova in 247 females of the CBN inbred strain (Satoh vitellus of the unfertilized ovum is about 60,um. The et al. 1998a). We found evidence of strain differences in the dimensions of the unfertilized ovum change slowly but numbers of total and normal ova, averaging 8.4 and 7.7 per steadily after ovulation. The maximum fertilizable life of litter in line AC and 9.9 and 9.1 in line CBN (Satoh et al. ova is about 13 hours. At 6 hours after ovulation, only about 1999a). Numbers of total and normal ova from the right half of the ova remain fertilizable, and coatings after ovary were 0.6 and 0.5 greater than those from left ovary. daybreak are less likely to produce young (Kent 1968). They also found that the number of ova was affected by age Fertilization rate is higher in morning matings than in and feed condition. We reported a mean of 12.6 normal ova evening matings. The ova reach the uterus during the third from 915 females of a closed herd of a synthetic strain day after ovulation. It remains free in the uterus for (Satoh et al. 2001a). The number of ova from the right approximately 24 hours. ovary was 0.6 greater than that from the left ovary. These External signs indicate certain stages of the cycle. lifferences between right and left ovaries agree with those

Fig. 1. Chronology of reproductive cycle of female Syrian hamsters.

Journal of Animal Genetics (2005) 32(2), 55-64 57 M. Satoh

in mice reported by Clutter et al. (1990, 1994). The 4. Pregnancy heritability estimates for total number of ova was 0.37. Fertility However, heritability estimates for number of ova from Selle (1945) was able to breed 1 female at 27 days right and left ovaries were 0.14 and 0.17, respectively. The of age, and the last of 10 on the 42nd day. An animal that genetic correlation between them was high and positive, but mated on the 28th day gave birth to 5 young on the 44th environmental correlation was negative (Satoh et al. 1998a, day, and one that mated on the 31 st day had 9 young on the 2001a). Furukawa et al. (1992) reported heritability 47th day; each raised all pups. However, for obtaining high estimates for number of embryos of 0.29 from inbred strains pregnancy rate and normal parturition, the animals should and 0.65 from 4-way crossed animals. Thus, ovum number be mated at 7 or more weeks of age. is affected by at least strain, age, and feed. Our group reported a conception rate of 84.5 % in a 16-day mating period in 240 females of an inbred strain

Mating (Satoh & Obata 1995). The conception rate is strongly The Syrian hamster is most active during the dark affected by age of females. The conception rate of animals period, and hand-mating is usually most successful within mated at 12 weeks of age (89.2 %) was higher than that of about an hour of nightfall in laboratory conditions. When animals mated at 8 weeks of age (80.0 %), and the the female is in strong heat near the hour of ovulation, difference was statistically significant (Satoh & Obata pacing a male in her cage may elicit lordosis within 5 1995). However, the conception rate of a nulliparous animal seconds. At the onset of heat, the female may at first appear past 20 weeks decreases greatly. Even a multiparous animal unreceptive but not belligerent. When the female is in heat, may be difficult to become pregnant beyond 3 months since she stiffens her legs, flattens her back, and points her tail the last conception. Fat females also have a low conception straight up. She assumes this posture after the male has rate, even if they are young. Females raised on fibrous feed rubbed her back with his nose. Murphy & Schneider (1970) from weaning till mating age had a higher conception rate have shown that the mating behavior of the male hamster than those raised on high-energy commercial pellets (Satoh depends entirely on the sense of smell. If the female is in & Obata 1995). heat, she generally permits the male to mount and remains Our group investigated sex differences in the quiet for 30 to 60 minutes. Females that are not in heat may infertility rate from the parturition records of 6403 females attack the male within 2 or 3 minutes. Females have been (Satoh & Ishii 2005). The ratio of pregnant to mated known to attack a male with sufficient strength to break a leg (Magalhaes 1968a). If a series of coatings is being made, it is advisable to continue for at least 8 days. Our group reported conception rates of 69.6 % over 4 days, 82.7 % over 8 days, and 89.8 % over 12 days in a synthetic strain (Satoh & Ishii 2002). Harem-mating is used as a breeding method, the usual procedure being to group 1 to 4 males with several females and to separate the females before parturition. The main problem with harem-mating systems is that there may be a certain amount of fighting when the females are returned to the mating cage. If information on pedigree is important, only 1 male must be mated to 1 or several females. Fighting does not occur if animals are paired at Fig. 2. Numbers of total and normal ova and young born weaning and left together for their whole breeding life. alive with different feed condition (low and high Monogamous pair mating may be a good system when an nutritious feeds) and mating age (Satoh et al. 1998a). inbred strain is maintained.

Journal of Animal Genetics (2005) 32(2), 55-64 58 Use of Syrian hamster in animal breeding 1. Physiology of reproduction

females was 80.4 %. But at least 93.3 % of males were expulsion of the placentas, which she stores in the cheek

fertile. Estimated infertility rates were 4.2 % in males and pouch and eats after the last delivery. We have observed the 16.0 % in females. Thus, approximately 80 % of infertility death of 1 % or 2 % of females on the day of delivery at first

originated in females. The difference between number of parity. The cause may be inhibition of the uterine normal ova and litter size at birth ranged from 0.95 to 1.70 contractions by overcrowding. between feed conditions and mating ages of the dam (Figure 2) (Satoh et al. 1998a). Litter size Litters of 3 to 14 are not uncommon, and litters as Delivery high as 17 have been reported (Kent 1968). Cannibalism The Syrian hamster usually delivers at about 16 days tends to reduce the size of litters. If a dam kills all her after ovulation. Thus, birth occurs on the 16th day after a young, she tends to kill all her young again at the next mating on the evening of estrus, and therefore on the 15th parturition. Not all cannibalism is the result of litter size, day after the last postovulatory discharge. Kupperman et al. but when the number per litter exceeds 10, cannibalism is (1944) reported the interval between the observation of more likely to occur. The first 3 days after birth are the most sperm and parturition to have been 14 days (4 %), 15 days critical. The number of young per litter at birth varies (85 %), and 16 days (11 %) in 71 pregnancies. Okuki (1972) depending on several factors, some of which are unknown. reported gestation intervals of 16 days (26 %), 17 days The average number of young born in 4 inbred strains (57 %), and 18 days (17 %). We found that in an inbred ranged from 8.2 to 10.7 (Satoh et al. 1999a). Similarly, the strain birth occurred on the 16th day after the last average number of young born alive of 5 inbred strains postovulatory discharge in all 43 pregnancies mated at 10 ranged from 8.3 to 10.6, a result of direct genetic effects weeks of age (Satoh et al. 1999b). However, using the same (Satoh et al. 2000). In 1,070 litters of a synthetic strain by strain, we recorded gestation intervals under different feed random mating, my group recorded 2 to 17 young (average, conditions and mating ages of 15 days (4 %), 16 days 10.7) and a stillborn rate of about 0.3 % (pers. obs.). (71 %), and 17 days (25 %) (Satoh & Obata 1995). Similarly, in 3,360 litters of 4 lines selected by reproductive Therefore, it seems that the length of pregnancy is affected performance, the litter size at birth was 1 to 20 (average, by both genetics and environment. 11.6) (Satoh et al. (2001a). Approximately 8 % of ova seem to fail in insemination or implantation, because the number 5. Parturition of normal ova of 915 relatives was 12.6. Process of parturition Litter size at birth is affected not only by maternal Kuramasu (1979) suggested that parturition genetic effects on the uterine environment, but also by fetal generally commences at darkness, and parturition in genetic effects (Satoh et al. 2000, 2001b). Estimates of daylight is abnormal. However, my group has observed direct and maternal heritabilities for litter size at birth were twice as many parturient animals in daylight as in darkness, 0.07 and 0.03, respectively (Satoh et al. 1998b). The genetic and no difference in the number of abnormal parturitions correlation between litter size at birth and ovulation rate between daylight and darkness in over 3,000 pregnancies. was 0.45 (Satoh et al. 2001a). Litter size at birth has a Kent (1968) described the process of parturition in positive genetic correlation with adult body weight (Satoh the Syrian hamster in detail. Before appearance of the first et al. 1997). This is why the correlation between direct and fetus, a bloody flow is usually evident for a short time. maternal genetic effects in litter size is negative (Satoh et al. During early labor the female walks around the cage, and 1998b), because body weight of the dam tends to decrease with the approach of parturition she settles into her nest. with increasing litter size. The time between delivery of the first and second siblings is The number of young per litter at birth varies about 7 to 8 minutes. A litter of 8 animals may be delivered depending on age of dam, parity, nutrition of dam, and in 30 minutes, or it may take nearly 3 hours. The elapsed season. The age of the female is an important factor in time between deliveries of littermates may be as short as 30 successful mating. Litter size at birth was 0.9 pups larger at seconds or as long as 20 minutes. The female helps with the a 12-week mating than at an 8-week mating (Satoh & Obata

Journal of Animal Genetics (2005) 32(2), 55-64 59 M. Satoh

1995). The average litter size from 186 mothers aged 1 inbred female litters (Satoh et al. 2000). Individual body through 13 months was not significantly different, but that weight at birth tends to decrease with increasing litter size at after the 13th month was greatly reduced. The average birth, but individual variation in a litter is large. Body number per litter may be a function of the number of weight at birth differs between lines. There is a negative previous pregnancies. It rose steadily from 5.7 in the first correlation between body weight and litter size at birth parity to 7.2 in the fourth parity (Kent 1968). Females within a line. raised on fibrous feed from weaning till mating age had a Individual birth weight and litter size at birth are smaller litter size at birth than those raised on high-energy affected not only by line effects of the dam, but also by commercial pellets (Satoh & Obata 1995). Litter size is growth of fetus as direct genetic effects (Satoh et al. 2000, affected by the hour of the night when mating occurs, and 2001b). Body weight at birth varies depending on sex of the optimal time varies with the strain (Magalhaes 1968a). fetus, the number of sibs in a litter, and nutrition for dam as Many breeders see a decrease in the number of young born environmental factors (Satoh & Obata 1995; Table 2). during winter, often from October through March or April, but mainly in December, January, and February. However, 6. Nursing there is no difference between seasons if the animals are The Syrian hamster is born hairless and blind, with raised in a windowless room with controlled lighting, closed ears and underdeveloped limbs. Teeth are evident. temperature, and humidity. The young show pigmentation on the dorsum at 5 days and gets darker at 3 days. The young eat hard food on day 10, Sex ratio and milk production begins to decrease at this time. The sex ratio of 90 blastocysts recovered 80 to 90 However, digestibility seems to be low at first, because hours after mating was 180 males : 100 females. The sex daily weight gain of young decreased from days 10 to 14 ratio of 167 young from 39 litters with no postnatal loss (Ishii et al. 1998). The eyes open on day 14 or 15. before weaning was 106:100 (Kent 1968). In contrast, In the laboratory, young are usually weaned at 21 Kupperman et al. (1944) reported a ratio of 369 males : 401 days, but it is possible to wean at about day 16 if the young females. We found a similar sex ratio in about 40,000 pups are well developed. The body weight of the dam decreases from 3,360 litters in the first parity (pers.obs.). after parturition and increases again from about the 12th day. Average weights of young were 2.8 g at 0 days, 5.6 g at Birth weight 4 days, 9.6 g at 8 days, 14.8 g at 12 days, and 16.9 g at 16 At parturition, fetus weight ranges from 1.3 to 3.2 g, days when the number of young was standardized to 6 at and body length ranges from 19 to 30 mm (Okuki 1972). birth (Satoh et al. 1999b). Average weight gains of young The average weight at birth for males is 2.49 g and for were 5.4 g from week 0 to 1, 9.6 g from week 1 to 2, and females is 2.32 g (Kent 1968). The average weight at birth 18.4 g from week 2 to 3 in 1,435 animals from 5 inbred of males (2.73 g) was significantly larger (P < 0.001) than strains (Satoh et al. 2001b). There was a consistent increase that of females (2.65 g) in 3,076 pure and FI pups from 350 in average body weight gain until the 9th day from birth,

Table 2. Environmental factors that affect individual birth weight (g) (Satoh et al. 2000)

Journal of Animal Genetics (2005) 32(2), 55-64 60 Use of Syrian hamster in animal breeding 1. Physiology of reproduction

and a steep rise in the next 2 days (Ishii et al. 1998). The 7. Genital organs average body weight gain decreased from the 12th to the In the female hamster, as in the rat, there are 2 uteri, 14th day and increased again from the 15th day. When the each with its own cervix opening separately into the vagina. litter size was standardized to 6 at birth, the survival rate of The ovaries are contained within periovarial sacs embedded young decreased from birth until the 4th day then was in large masses of fat. Connections with the uteri are made constant. When the litter was standardized to 8 at birth, the by rather long, closely coiled oviducts. Average uterine survival rate of young consistently decreased during 21 days weight was 311 mg in 773 females (Satoh et al. 2001). The of nursing. When the litter was standardized to 6 and 8 at right uterus was significantly heavier than the left. birth, the survival rates at day 21 were 90 % and 91 %, Mammary glands are used as a generic characteristic of giving a litter size at weaning of >5. However, it was hamsters. The Syrian hamster usually has 12 to 14 glands, approximately 4.5 without a standardized litter (M. Satoh although as many as 22 have reported (Magalhaes 1968b). unpublished). In the male, the genital system resembles that of the Individual body weight at weaning is also affected rat more closely than that of the mouse. Few studies have by both line of dam as maternal genetic effects and growth reported the physiology of reproduction in the male. Real of young as direct genetic effects (Ishii et al. 1998; Satoh et testis weight in Syrian hamsters is heavier than that in rats al. 1992, 1999a, 2000, 2001b; Table 3). Heritability and is about 10 times heavier than that in mice. Okuki estimates were 0.17 and 0.29 for litter weight at 2 and 3 (1972) reported that right and left testis weights were 0.67 weeks of age, and estimates of direct and maternal and 0.66 g, respectively, and right and left epididymis heritabilities were 0.12 and 0.13 (Satoh et al. 1998b) and weights were 82 and 84 mg, respectively, at 5 weeks of age 0.15 and 0.18 (Ishii et al. 2003). Body weight at weaning in 56 males. Furukawa et al. (1992) reported that the depended on feed as environmental factors, but there was average testis size and weight at 19 weeks of age were little effect of age of dam (Satoh & Obata 1995). 5.7 cm 3 and 1.60 g in 120 males from 3 inbred strains. Tanaka (1986) found a statistically significant difference between inbred strains. My group investigated testis weight of males selected by estimated breeding values for Table 3. Least-squares constant estimates for direct and reproductive traits at 15 weeks of age in each generation in maternal genetic effects on individual weight at weaning (g)1) (Satoh et al. 1992) a selection experiment (Satoh et al. 2001a). The average testis weight was 3.15 g (Table 4), and weight of left testis was 0.01 g heavier than that of right testis. We reported heritability estimates for uterine and testis weights of 0.62 and 0.37, respectively, and a high positive genetic correlation between uterine weight and ovulation rate (Satoh et al. (2001a). Furukawa et al. (1992) reported that heritability estimates for testis weight ranged 1) Overall mean is 32 .6g. Different letters are significantly different at P < 0.05. from 0.61 to 0.69 from a 4-way cross. Furukawa et al.

Table 4. Basic statistics for uterine and testis weights (Satoh et al. 2001a)

1) Males which were either not selected or selected by estimated breeding values for reproductive traits in a

selection experiment.

Journal of Animal Genetics (2005) 32(2), 55-64 61 M. Satoh

(1988) estimated a realized heritability of 0.40 for testis size Proceedings of the 3rd World Congress on Genetics from a selection experiment. Applied to Livestock Production, 11:203-208.

Kupperman et al. (1944) and others have studied Gama LLT, Johnson RK. 1993. Changes in ovulation rate, senility changes in the female reproductive organs. Sterility uterine capacity, uterine dimensions, and parity effects in females may begin as early as 12 months of age. It is with selection for litter size in swine. Journal of typically observed at 400 to 500 days of age in males and Animal Science, 71:608-617. females, but may commence as late as 19 months. There are Hanrahan JP. 1982. Selection for increased ovulation rate, definite seasonal variations in the weight of the testes. Kent litter size and embryo survival. Proceedings of the 2nd

(1968) designated average weight of testes as •gsexually World Congress on Genetics Applied to Livestock mature•h. Testis weight is lower in winter than in other Production, 5:294-309. seasons. Testis size decreased owing to low temperature Hanrahan JP, Quirke JF. 1977. Testis size and plasma

(Hoffman 1968). Hoffman et al. (1965) showed that short luteinizing hormone as aids to selection for fecundity in photoperiods and low ambient temperatures acting over a sheep. Animal Production, 24:148. period of weeks had potentiating or additive effects which Hoffman RA. 1968. Hibernation and effects of low resulted in a significant decline in testis weight and in temperature. In the golden hamster. Its biology and use damage to seminiferous tubules. Thus, the reduced in medical research (Hoffman RA, Robinson PF, reproductive activity often noted in winter months is Magalhaes H eds.) 25-39. Iowa State Univ. Press. attributable, at least in part, to decreased testicular function. Ames. Hoffman RA, Hester RJ, Towns C. 1965. Effect of light References and temperature on the endocrine system of the golden Clutter AC, KocheraKirby YL, Nielsen MK. 1994. Uterine hamster (Mesocricetus auratus, Waterhouse). capacity and ovulation rate in mice selected 21 Comparative Biochemistry and Physiology, 15: generations on alternative criteria to increase litter size. 525-533. Journal of Animal Science, 72:577-583. Holm B, Bakken M, Vangen O, Rekaya R. 2004a. Genetic Clutter AC, Nielsen MK, Johnson RK. 1990. Alternative analysis of litter size, parturition length, and birth methods of selection for litter size in mice: 1. assistance requirements in primiparous sows using a Characterization of base population and development joint linear-threshold animal model. Journal of Animal of methods. Journal of Animal Science, 68: Science, 82:2528-2533. 3536-3542. Holm B, Bakken M, Klemetsdal G, Vangen O. 2004b. Festing MFW. 1972. Hamsters. In The UFAW Handbook Genetic correlations between reproduction and on the Care and Management of Laboratory Animals. production traits in swine. Journal of Animal Science, (UFAW eds.) 242-256.Longman Press. Edinburgh & 82:3458-3464. London. Holm B, Bakken M, Vangen O, Rekaya R. 2005. Genetic Fulton GP. 1968. The golden hamster in biomedical analysis of age at first service, return rate, litter size, research. In the golden hamster. Its biology and use in and weaning-to-first service interval of gilts and sows. medical research (Hoffman RA, Robinson PF, Journal of Animal Science, 82:2528-2533. Magalhaes H eds.) 3-13. Iowa State Univ. Press. Hoover WH, Mannings CL, Sheerin HE. 1969. Observation Ames. on digestion in the golden hamster. Journal of Animal Furukawa T, Awata T, Shioya Y, Tanaka H. 1992. The Science, 28:349-352. possibility of the indirect selection for ovulation rate Ishii K, Satoh M, Furukawa T. 1998. Effect of number of based on testis size in golden hamsters. Animal pups before weaning and estimation of variance Science and Technology, 63:495-502. components with restricted maximum likelihood for Furukawa T, Tanaka H, Awata T. 1988. Selection weight at 3, 4, and 5 weeks of age in golden hamsters. experiment in the golden hamster for testis size and Experimental Herbivora, 22:39-45. correlated responses in female reproductive traits. Ishii K, Satoh M, Sasaki O, Takeda H, Furukawa T. 2003.

Journal of Animal Genetics (2005) 32(2), 55-64 62 Use of Syrian hamster in animal breeding 1. Physiology of reproduction

Selection experiment using maternal effect in Syrian for feed protein. I. Utilization of urea by the golden

hamster 7. Genetic parameter re-estimation. hamster. Tohoku Journal of Agricultural Research, 6:

Experimental Herbivora, 27:23-28. 127-131.

Johnson RK, Eckardt GR, Rathje TA, Drudik DK. 1994. Mesa H, Safranski TJ, Johnson RK, Lamberson WR. 2003.

Ten generations of selection for predicted weight of Correlated response in placental efficiency in swine

testes in swine: Direct response and correlated response selected for an index of components of litter size.

in body weight, backfat, age at puberty, and ovulation Journal of Animal Science, 81:74-79.

rate. Journal of Animal Science, 72:1978-1988. Moeller SJ, Goodwin RN, Johnson RK, Mabry JW, Baas

Kent GC. 1968. Physiology of reproduction. In the golden TJ, Robison OW. 2004. The national pork producers

hamster. Its biology and use in medical research council maternal line national genetic evaluation

(Hoffman RA, Robinson PF, Magalhaes H eds.) program: A comparison of six maternal genetic lines

119-138. Iowa State Univ. Press. Ames. for female productivity measures over four parities.

Kupperman HS, Greenblatt RN, Hair LQ. 1944. The Journal of Animal Science, 82:41-53.

sexual cycle and reproduction in the golden hamster Murphy M, Schneider GE. 1970. Olfactory bulb removed

(Cricetus auratus). Anatomical Record, 88:441-442. eliminates mating behaviour in the male golden

Kuramasu S. 1979. Hamsters. In the techniques for hamster. Science, 167:302-303.

experimental animals. (Tajima Y eds.) 204-210. Nakano A. 1960. Histological studies of the prenatal and

Asakura Publishing Company Press. Tokyo. postnatal development of the ovary of the golden

Land RB, Can WR. 1975. Testis growth and plasma LH hamster (Cricetus auratus). Okajima's Folia Anatomica

concentration following hemicastration and its relation Japonica, 35:183-217.

with female prolificacy in sheep. Journal of Neely JD, Robison OW. 1983. Estimates of heterosis for

Reproduction fertility, 45:495-501. sexual activity in boars. Journal of Animal Science,

Leenhouwers JI, Wissink P, van der Lende T, Paridaans H, 56:1033-1038.

Knol EF. 2003. Stillbirth in the pig in relation to Okuki M. 1972. The hamsters. In the experimental

genetic merit for farrowing survival. Journal of Animal animals. (Tajima Y eds.) 92-113. Asakura Publishing

Science, 81:2419-2424. Company Press. Tokyo.

Lund MS, Puonti M, Rydhmer L, Jensen J. 2002. Orsini MW. 1961. The external vaginal phenomena

Relationship between litter size and pernnatal and pre- characterizing the stages of the estrous cycle

weaning survival in pigs. Animal Science, 74: pregnancy, pseudopregnancy, lactation, and the

217-222. anestrous hamster, Mesocricetus auratus Waterhous.

Manda T, Takano N. 1976. Growth response of golden Proceedings of Animal Care Panelist, 11:193-206.

hamster to diets having different levels of forages. Petry DB, Johnson RK. 2004. Responses to 19 generations

Journal of Japanese Grassland Science, 22:46-51. of litter size selection in the Nebraska Index line. I.

Manda T, Gotoh N. 1976. Comparative study on forage Reproductive responses estimated in pure line and

digestive ability of meadow voles and golden hamsters. crossbred litters. Journal of Animal Science, 82:

Journal of Japanese Grassland Science, 22:52-56. 1000-1006.

Magalhaes H. 1968a. Housing, care, and breeding. In the Petry DB, Holl JW, Johnson RK. 2004. Responses to 19

golden hamster. Its biology and use in medical research generations of litter size selection in the Nebraska (Hoffman RA, Robinson PF, Magalhaes H eds.) Index line. II. Growth and carcass responses estimated

15-23. Iowa State Univ. Press. Ames. in pure line and crossbred litters. Journal of Animal

Magalhaes H. 1968b. Gross anatomy. In the golden Science, 82:1895-1902.

hamster. Its biology and use in medical research Ruð©z-Flores A, Johnson RK. 2001. Direct and correlated

(Hoffman RA, Robinson PF, Magalhaes H eds.) responses to two-stage selection for ovulation rate and

91-109. Iowa State Univ. Press. Ames. number of fully formed pigs at birth in swine. Journal

Matsumoto T. 1955. Nutritive value of urea as a substitute of Animal Science, 79:2286-2297.

Journal of Animal Genetics (2005) 32(2), 55-64 63 M. Satoh

Rydhmer L. 2000. Genetics of sow reproduction, including Satoh M, Obata T. 1995. Effects of feed and mating age on

puberty, oestrus, pregnancy, farrowing and lactation. reproductive performance in Syrian hamsters.

Livestock Production Science, 66:1-12. Experimental Animals, 43:731-735.

Satoh M, Furukawa T, Nishida A. 1992. The genetical Satoh M, Nishida A, Arendonk JAM, Lende T. 1997.

analysis of growth in body weight with diallel crosses Benefit of multiple trait selection to increase

among inbred lines of golden hamsters. Animal reproductive trait: Experimental evidence from golden

Science and Technology, 63:1160-1167. hamsters. Journal of Animal Science, 75:3103-3113.

Satoh M, Furukawa T, Takahashi H, Minezawa M. 2001a. Schinckel A, Johnson RK, Pumfrey RA, Zimmerman DR.

Estimation of genetic parameters for reproductive traits 1983. Testicular growth in boars of different genetic

in Syrian hamsters. Experimental Herbivora, 25: lines and its relationship to reproductive performance.

5-12. Journal of Animal Science, 56:1065-1076.

Satoh M, Ishii K. 2002. Reproduction ant its selection in Selle RM. 1945. Hamster sexually mature at twenty-eight

Syrian hamsters. Experimental Herbivora, 26:11-22. days of age. Science, 102:485-486.

Satoh M, Ishii K. 2005. Sex differences in the infertility Serenius T, Sevð®n-Aimonen M-L, Kause EA, Mantysaari

rate of the Syrian hamster. Experimental Herbivora, 29 EA, Mð ki-Tanila A. 2004a. Selection potensial of

in press. different prolificacy traits in the Finnish Landrace and

Satoh M, Ishii K, Furukawa T. 1998a. Effects of feed and Large White populations. Acta Agricultural

age for ovulation rate in Syrian hamsters. Experimental Scandinavia, Section A, Animal Science, 54:36-43.

Herbivora, 22:27-32. Serenius T, Sevð®n-Aimonen M-L, Kause EA, Mð ntysaari

Satoh M, Ishii K, Furukawa T. 1998b. Animal model EA, Mð ki-Tanila A. 2004b. Genetic associations of

estimation of maternal genetic variance for prolificacy with performance, carcass, meat quality,

reproductive traits and weaning weight in Golden and leg conformation traits in the Finnish Landrace and

hamsters. Experimental Herbivora, 22:33-38. Large White pig populations. Journal of Animal

Satoh M, Ishii K, Furukawa T. 1999a. Characteristics of Science, 82:2301-2306.

reproduction and growth in AC line of Syrian hamsters. Shinohara H, Kayaba T, Mizuma Y. 1989. Comparative

Experimental Herbivora, 23:7-14. studies on the forage utilization of hamsters and other

Satoh M, Ishii K, Furukawa T. 1999b. Effects of feed for rodents. Journal of Japanese Grassland Science, 35:

reproductive performance in Syrian hamsters. 247-253.

Experimental Herbivora, 23:37-42. Tanaka H. 1986. Selection experiments for prolificacy of

Satoh M, Ishii K, Furukawa T. 2000. Genetic analysis of the golden hamster as a pilot animal. Experimental

reproduction and growth from diallel crossing in inbred Herbivora, 11:107-116.

strains of Syrian hamster 1. Estimation of direct and Toelle VD, Robison OW. 1985. Estimates of genetic

maternal genetic effects. Experimental Herbivora, 24: relationship between testes measurements and female

39-44. reproductive traits in swine. Zeitschrift fur

Satoh M, Furukawa T, Hicks C. 1998c. A simple method Tierzð¹chtung and Zð¹chtungsbiologie, 102:125-132.

of computing restricted best linear unbiased prediction Wilson ER, Johnson RK, Wettemann RP. 1977.

of breeding values and application to improvement of Reproductive and testicular characteristics of purebred

reproductive traits in golden hamsters. Proceedings of and crossbred boars. Journal of Animal Science, 44:

the 6th World Congress on Genetics Applied to 939-947.

Livestock Production, 25:649-652. Young LD, Leymaster KA, Lundstra DD. 1986. Genetic

Satoh M, Ishii K, Furukawa T, Takahashi H, Minezawa M. regulation of testicular growth and its relationship to

2001b. Genetic analysis of reproduction and growth female reproductive traits in swine. Journal of Animal

from diallel crossing in inbred strains of Syrian hamster Science, 63:17-26.

2. Estimation of combining ability effects.

Experimental Herbivora, 25:13-19.

Journal of Animal Genetics (2005) 32(2), 55-64 64