meiotic chromosome asynapsis in a boar with a reciprocal translocation and acquired testicular...

Hereditas 118: 101-111 (1993)

Meiotic chromosome asynapsis in a boar with a reciprocal translocation and acquired testicular degeneration D. A. F. VILLAmMEZ', I. GUSTAVSSON', B. ALABAY'* and L. PL6ENZ

Departments of ' Animal Breeding and Genetics, and 2Anatomy and Histology, Swedish University of Agricultural Sciences, Uppsala, Sweden

VILLAG~MEZ, D. A. F., GUSTAVSSON, I., ALABAY, B. and PLOEN, L.1993. Meiotic chromosome asynapsis in a boar with a reciprocal translocation and acquired testicular degeneration. - Hereditas 118: 101 -1 11. Lund, Sweden. ISSN 0018-0661. Received June 30, 1992. Accepted September 14, 1992

During a period of performance testing, a boar used for artificial insemination purposes was found responsible for reduced litter size and slightly increased incidence of repeat breeding. The qualitative and quantitative semen characteristics, however, were within normal limits. Later, evaluation of the semen during a period of 3 months revealed a decreased sperm concentration, but sperm cell morphology and mobility were normal. At castration, the boar, which had suffered from scrotal inflammation, was found to have hypoplastic gonads, the right testis being smaller than the left one. Histologically there was spermatogenic arrest at the primary spermatocyte level in almost all tubules of the right testis. In the left testis, histology was more heterogeneous, with some tubules containing all developmental stages, while others had an almost complete spermatogenic arrest. Cytogenetically the boar was carrying a translocation, rcp(2; 14)(p14;q23). Synaptonemal complex analysis revealed complete quadrivalent pairing in 21 out of 43 cells analysed. The remaining cells demonstrated quadrivalents with axes moderately or extensively unpaired. There was a distinct difference between cells from the right vs. the left testis. The latter cells showed more completely paired translocation configurations. Moreover, in 14 and 7 cells analysed from the right and left testis, respectively, the translocation configuration could not be identified. This was due to chromosome asynapsis and frequent Occurrence of gaps in the chromosomes, including others than those of the translocation, plus an abundant cellular deposit which formed a dense cell background. Association or pairing of the quadrivalent with the sex bivalent was seen in one cell only. At diakinesis-MI, most cells had a ring-shaped quadrivalent. It is believed that the asynapsis of chromosomes during the prophase of meiosis was to a large extent due to the degeneration caused by the inflammation processes.

lngemar Gustavsson, Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Box 7023, S-750 07 Uppsala 7, Sweden

Evidence is accumulating that chromosome translocations are more common in the domestic pig than previously believed and are observed particularly in boars producing smaller litters (Gus- TAVSSON 1992). The overwhelming majority of cases have, however, demonstrated a normal semen picture, and the reduced litter size is ascribable to non-disjunctional events of translocation chromosomes in meiosis, with the production of gametes partly resulting in zygotes with unbalanced kary- otypes (e.g., KING et al. 1981; POPESCU and BOSCHER 1982). In only one boar with a rcp(2;4)( pl7;qll) translocation could meiotic arrest be observed in some parts of the testes, although testis size was normal, as was the semen picture ( GUSTAVSSON et al. 1992). Synaptonemal complex (SC) analysis demonstrated a high inci-

* Present addrers: A. U. Veterinar Fakiiltesi. Histoloji-Embriy- ploji Bilim Dali, Diskapi-Ankara, Turkey

dence of pairing between the quadrivaknt and the sex bivalent. Association between chromosome pairing failure and gametogenic impairment has been observed in humans and mice (BURGOYNE and BAKER 1984; CHANDLEY 1984; SETTERFIELD et al. 1988). It is still not known, however, if the chromosome pairing failure is a cause of such germ-cell death, or vice versa (SPEED and CHAND- LEY 1990; MIJTWOCH and MAHADEVAIAH 1992).

In the present work, a boar, detected because it was found responsible for siring small litters, has been studied cytogenetically in mitosis and meiosis after acquiring a scrotal inflammation.

Material and methods Case report

The boar, which was 2.5 years old and of the Hampshire breed, had been used for A.I. (artificial

Hereditas 118 (1993) 102 D. A. F. VILLAGOMEZ ET AL.

Table 1. Semen analysis (results from the A.I. station)

Observed values Expected for boar with values translocation

Volume per 175.11 5 8.44 > 100 ejaculate (ml)

No. of spermatozoa 55.20 If- 3.01 > 10 per ejaculate ( lo9 unit)

Total no. of 323.02 rt 12.87 > 200 spermatoza per mi (,lo6 unit)

insemination) work. Both parents of the boar were found to be chromosomally normal. Thirty-three females had been inseminated, but 8 (24 YO) of them required repeat mating. From the remaining inseminations the boar produced 5.4 piglets per litter as the average litter size. This value was 41.3 YO lower than predicted according to the average of the Hampshire boars on the A.I. station concerned. The testicular size of the proband boar was regarded as normal. Forty-three semen sam- ples, regularly taken at the A.I. station over a period of 10 months, showed that the boar had not only a qualitatively but also a quantitatively normal semen picture (Table 1). After the boar was moved to the Clinic of Obstetrics and Gynaecology it developed a scrotal inflammation, which was not therapeutically treated.

Mitotic chromosome analysis

Blood was drawn repeatedly from the boar, and lymphocyte cultures were set up with RPMI 1640 plus 30 % fetal calf serum as medium with poke- weed (Grand Island) mitogen. After 3 days, col- cemid (100 ,ug/ml) was added to the cultures half an hour before harvest. Cultures with cells to be used for R-banding of the chromosomes (see below) were treated with 5-bromodeoxyuridine (BrdU) at a concentration of 200 pg/ml 7 h before harvest. At harvest the cells were treated with 0.075 M KCI, repeatedly fixed with absolute methanol-glacial acetic acid (3:1), and spread on slides. The following banding techniques were applied: GTG (SEABRIGHT 1971), QFQ (CASPERS- SON et al. 1971), RBA (DUTRILLAUX et al. 1973) and THA (DUTRILLAUX 1973).

Seminal, meiotic and histological analyses

Twelve semen ejaculates were collected from the proband boar during a three months’ period at the

Obstetrics and Gynaecology Clinic. Standard pro- cedures for semen evaluation were conducted.

Testicular material was taken at slaughter from both testes for SC studies by applying the surface spreading technique (COUNCE and MEVER 1973), as described by VILLAG~MEZ ( 1993). Finely minced pieces of testicular material were placed in drops of 0.2 M sucrose on slides which had earlier been coated with a Necoloidine (BDH Chemicals Ltd, Poole, Dorset, England) film dissolved in amylac- etate. After drying, the preparations were fixed with 4 YO paraformaldehyde in 0.1 M sucrose and stained with an ethanolic phosphotungstic acid (PTA) solution. The Necoloidine film was floated off on a water surface and 100-square mesh copper grids were applied. The cells were then investigated with a Philips EM 210.

Conventional meiotic preparations were made according to the technique described by PATHAK et al. (1976) as applied by KING (1981). Testicular material was also fixed with 3 % glutaraldehyde in 0.067 M cacodylate buffer (pH 7.2). The tissue was postfixed in osmium tetroxide, dehydrated, and embedded in Epon. Semithin sections ( x 1 pm) were stained with buffered toluidine blue.

Results Veterinary data

Semen picture

Semen morphology and motility were normal. Nevertheless, a reduced sperm concentration - 51 % less than when sampled at the A.I. station- was observed.

Anatomy and histology

The gross anatomy of the reproductive organs showed at slaughter that the boar had suffered from a scrotal inflammation. Its gonads were hypoplastic; the right testis was smaller than the left one (weight 193 g and 318 g, respectively). The normal testicular weight of Hampshire pigs at an age of 7.5 months is approximately 320 g per testis (HOLZLER et al. 1975).

Spermatogenic arrest was obvious in practically all tubules of the right testis. In some of them the number of spermatocytes was also reduced. Only occasionally were a few spermatids developing up to the maturation phase encountered (Fig. 1). There was a heterogeneous histological picture of

Heredifus 118 (1993) MEIOTIC CHROMOSOME ASYNAPSIS IN PIG 103

Fig. 1. Histology of a semithin section of the right testis. Note that only a few primary spermatocytes are present. There is also a loss of mature cells.

the left testis, with some tubules containing all developmental stages, and some with a near total spermatogenic arrest at the primary spermatocyte level. Tubules almost devoid of epithelium were also found. In these, the lamina propria was thick. In the tubules with spermatogenesis there were few spermatids and the ratio of spermatids/primary spermatocytes was greatly reduced. Moreover, the epithelium seemed less well organized than in normal animals and degenerating primary spermatocytes were common. No obvious changes were seen in the interstitial tissue.

Cytogenetic data

Somatic chromosomes

One biarmed and one one-armed chromosome were involved in the translocation (Fig. 2 and 3). The breakage/rejoining points were located in a strong proximal GTG-positive ( RBA-negative) band of chromosome arm 2p, and in a subterminal GTG- negative (RBA-positive) band of chromosome 14. According to the Committee for the Standardized

Karotype of the Domestic Pig (1988) the translocation could be designated rcp(2; 14) (p14;q23).

Synaptonemal Complex (SC) chromosomes

A total of 64 cells were investigated, 26 cells from the right and 38 cells from the left testis. However, analysis of the translocation pairing behaviour was possible in only 12 and 31 cells of right and left testis, respectively (Table 2). Thirteen of these cells (30.2 YO of 43 cells) were partly concealed by the mesh of the grids. These 13 incomplete cells, con- sisting of 10- 16 bivalents, had a quadrivalent SC configuration and in 12 of them the sex bivalent could be observed. The remaining 30 cells (69.8 YO of 43 cells) demonstrated 17 bivalents and a quadrivalent. Although there were 4 cells showing single incompletely paired bivalents, the sex bivalent morphology made classification possible according to pachytene stage.

According to the spermatocyte substaging sys- tem (VILLAG~MEZ 1993), the cells were distributed in early (PI-P2), mid- (P,-P,) and late (P,-P6) pachytene cells (Table 2). Bivalent appearance was

104 D. A. F. VILLAG~MEZ ET AL Hereditas 118 (1993)

Fig. 2. GTG-banded karyotype of the boar showing the rcp(2p+;14q-). Bar indicates 10 pm.

Tuble 2. Distribution of spermatocytes investigated in the right and left testis according to cell stage/quadrivalent configuration, and percentage of pairing

~~ ~~

cell stage No. of cells right testis/ left testis Complete homologous Centrally unpaired Homologous and Open configuration

Quadrivalent morphology (range of % axis pairing)

pairing configuration heterologous pairing

Early pachytene p, 512 010 p2 314 01 I

p4 013 010

p5 112 010 ' 6 010 010

Mid-pachytene p3 3/20 013

Late pachytene

Subtotal 12/31 014

2 (62-85)/1 (93) 010 1 (77) 10 013

1 (94) /5 (94-97) 018 0 I0 013

0 I0 112 0 I0 010 4 (62-94)/6 (93-97) 1/16

3 (60-70)/1 (60) 2 (35-81)/0

2 (81-92)/4 (77-88) 0 I0

0 /O 0 10 7 (35-92)/5 (60-88)

Total 43 4 10 17 12

Hereditas 118 (1993) MEIOTIC CHROMOSOME ASYNAPSIS IN PIC 105

Fig. 3a-c. RBA- (a), QFQ- (b), and THA-banded (c) chromosomes of pairs 2 and 14 demonstrating the segments translocated. Bar indicates 10 fim.

similar to that in earlier investigations; the bivalent was formed by the paired axes having a central element which frequently was clearly visible. The kinetochores formed dense identifiable struc- tures ~ though not visible in the XY-bivalent - and the attachment plaques were strongly stained.

When completely paired, the quadrivalent also demonstrated the typical appearance of axes, central element and attachment plaques, but the kinetochores of chromosome 2 were, for unknown reasons, only rarely visible. Four main types of quadrivalent configuration were observed. A cross quadrivalent configuration with completely paired

axes (100 % presumptive homologous pairing), was found in only four spermatocytes of the left testis (Fig. 4a). Cells of both testes (10 cells) demonstrated a quadrivalent (Fig. 4b) with centrally unpaired chromosome segments. The centrally unpaired quadrivalents of cells of the right testis had larger unpaired segments than cells of the left testis. In altogether 17 spermatocytes the translocation chromosomes were completely paired, including heterologous pairing between the nonderivative chromosomes extending from 3-17% of the axes’ length. The translocation chromosomes formed an asymmetrically paired quadrivalent in 1 cell and 16 cells of the right and left testis, respectively. In one of the latter cells the quadrivalent was associated end-to-end with the sex bivalent. In the P, late pachytene cells of both testes the asymmetrically paired quadrivalent showed an interstitial unpaired segment which involved the proximal segments of chromosomes 14. Seven and 5 cells of the right and left testis, respectively, demonstrated an open quadrivalent configuration with the presumptive homologous segments of chromosomes 14 and 14q- unpaired (Fig. 5a). The terminally located kinetochores of the latter chromosomes were associated with a chromocentre. This occurred singly in most cells. The normal telocentric bivalents were also associated with the chromocentre and end-to-end associations with the quadrivalent were often seen (18 cells), particularly with the unpaired chromosomes 14 and 14q- (Fig. 5a). In 4 of those cells (3 and I of right and left testis, respectively) showing an open quadrivalent, some normal telocentric bivalents demonstrated unpaired segments.

Fourteen and 7 cells from the right and left testis, respectively, gave little information concerning the type of translocation configuration (Table 3). In general, this was due to the fact that the cells demonstrated 2-3 chromosomes with unpaired segments and/or 2-5 chromosome gaps which im- peded the accurate identification of SC configurations (Fig. Sb). These cells also showed more cellular deposit which gave a dense background interfering with the SCs visibility.

Thus, there was a distinct difference between the right and the left testis cells regarding the relative frequency of quadrivalents with differing configurations. The quadrivalent configurations of the left testis appeared to show a larger degree of pairing, particularly in the form of heterologous pairing, and fewer translocations with unpaired segments. How- ever, both testes had cells demonstrating open quad-

106 D. A. F. VILLAG~MEZ ET AL. Hereditas 118 (1993)

Fig. 4a and b. Electron micrographs of pachytene synaptonemal complexes of spermatocytes with a quadrivalent configuration. a Completely paired quadrivalent presumptively without non-homologous pairing at P, mid-pachytene substage. The sex bivalent is indicated (XU). b Quadrivalent configuration showing a small buckle in central region at P, mid-pachytene substage. The arm containing the homologous segments of chromosomes 14 is associated with a chromocentre as well as the normal telocentric bivalents. Bar indicates 4 pm in (a) and 6 pm in (b). k = kinetochores.

rivalent configurations, with unpaired segments which were invariably thicker than paired ones.

Conventional meiotic analysis

Altogether 52 spermatocytes at diakinesis-metaphase I were analysed; 17 and 35 originating from

Table 3. Distribution of cells from the right and left testis in which the translocation product could not be identified

Cell stage Specimen

Right testis Left testis

Early pachytene PI

p;

p3 p4

p5 P6

Mid-pachytene

Late pachytene

Total

Table 4. Quadrivalent morphology (diakinesis-MI)

Specimen Quadrivalent morphology

Ring Chain No of cells investigated

Right testis 16 1 17 Left testis 25 10 35 Both testes 41 1 1 52

the right and left testis, respectively (Table 4). In 41 cells the quadrivalent was ring-shaped (Fig. 6a). The remaining 11 spermatocytes showed a rod- shaped quadrivalent (Fig. 6b).

Discussion Somatic chromosome analysis using different banding techniques could accurately demonstrate which chromosome segments had been exchanged.

Hereditas 1% (1993) MEIOTIC CHROMOSOME ASYNAPSIS IN PIG 107

Fig. 5a and b. Electron micrographs of synaptonemal complexes of partial spermatocytes at P, early pachytene substage, showing an open quadrivalent with end-to-end pairings (a), and multiple associated configurations with extensively unpaired segments (b). The translocation configuration is not identifiable in (b). Note the thickening of unpaired segments in (a) and (b). Schematic drawings to the side of each figure. Bar indicates 4 pm.

108 D. A. F. VILLAGOMEZ ET AL Hereditas 118 (1993)

Fig. 6a and b. Diakinesis-metaphase I configurations of spermatocytes demonstrating a ring-shaped quadrivalent (a), and a rod-shaped quadrivalent (b), the preparations being banded according to the CBG technique and the THA technique, respectively. Bar indicates 10 pm. Q = quadrivalent.

Chromosome 14 is one of the chromosomes most mal, it is assumed that the translocation had a de often involved in reciprocal translocations ( G u s - novo origin. TAVSSON 1990) while chromosome 2 has only once It was quite evident that the proband, when previously been reported to be involved in a serving as an A.I. boar, had a normal semen translocation (GUSTAVSSON et al. 1992). Since the picture, which evidently deteriorated later, proba- parents of the proband were chromosomally nor- bly due to degeneration caused by the inflamma-

Herediras 118 (1993) MEIOTIC CHROMOSOME ASYNAPSIS IN PIG 109

tory processes observed. A normal semen picture, but a reduced litter size, seem to be common features of reciprocal translocations in heterozygous boars (for a review, see GUSTAVSSON 1990). Therefore, the reduced litter size of the present heterozygous boar could by analogy with earlier described cases be ascribed to meiotic chromosome malsegregation, with the partial production of chromosomally unbalanced gametes. After fertilization, these unbalanced gametes would pro- duce chromosomally unbalanced zygotes which subsequently would be eliminated early during embryonic life (e.g., KING et al. 1981; POPESCU and BOSCHER 1982).

The SC analysis demonstrated differences between right and left testis concerning the types and frequencies of multivalent configurations. There were few completely homologously paired quadrivalent configurations. They occurred only in the left testis (4 out of 31 cells). The lengths of arms and localization of the kinetochores in the cross- shaped quadrivalents appeared to agree with the size of segments translocated according to the somatic chromosome analysis. Completely paired quadrivalents-including a heterologously paired segment-occurred more frequently in the left testis (16 out of 3 1 cells) than in the right ( 1 out of 12 cells). Moreover, open quadrivalent configurations were less frequent in the left testis (5 out of 31 cells) than in cells of the right testis (7 out of 12 cells). The extension of the unpaired chromosome segments was also greater in quadrivalents of the latter cells. The irregular synaptic pattern of the present reciprocal translocation is not comparable with most of those previously reported in the liter- ature. Open quadrivalent configurations were not formed by several reciprocal translocations described earlier in the pig (GUSTAVSSON et al. 1988; GABRIEL-ROBEZ et al. 1988; JAAFAR et al. 1989). However, a rcp( 7; 17)( q26;qll) translocation in a boar was also found to give an irregular pairing pattern, which included formation not only of open quadrivalent configurations but also of triva- lent plus univalent configurations ( VILLAGOMEZ et al. 1993). Nevertheless, that boar had normal testicular histology and a normal semen picture. Fur- ther meiotic pairing analyses in our laboratory of several reciprocal chromosome translocations in boars have demonstrated a regular quadrivalent pairing behaviour (unpublished).

It is well known in man and mice that certain autosomal reciprocal translocations cause congeni- tal subfertility or even sterility as a result of sper-

matogenic impairment ( CHANDLEY 1982; SEARLE 1982). Some general facts emerged from those observations: (1) there is a greater risk of spermatogenic breakdown when the point of breakage preceding the translocation is close to or within the centromeric heterochromatin in one chromosome and in the telomeric region of the other chromosome; (2) there is a tendency for male-sterile reciprocal translocations to give higher frequencies of chain configurations than ring-shaped configurations at diakinesis-metaphase I. These two facts were relevant to the rcp(2;4)(pl7;qI 1) translocation, which is the only indication in pig that an autosomal translocation may interfere with normal spermatogenesis (GUSTAVSSON et al. 1993). Be- sides producing reduced litter size, the boar also demonstrated testicular degeneration in the form of meiotic arrest in some tubules.

The reasons for cell degeneration in the male- sterile autosomal translocation carriers is not known. According to one hypothesis ( LIFSCHYTZ and LINDSLEY 1972), occurrence of pairings between the sex bivalent and unpaired autosomal segments may interfere with the inactivation of the X chromosome. According to this hypothesis such X-inactivation is necessary for the normal metabolism of a cell in meiotic division. There are several examples of frequent associations between the sex bivalent and unpaired translocation segments (for a review, see SPEED 1989; DE BOER and DE JONG 1989) in man and mouse autosomal translocations causing sterility or subfertility. In pigs, the rcp( 2;4)( pl7;qll) translocation seemed to be such a case. About half of the prophase cells analysed demonstrated associations between the sex chromosomes and the unpaired segments of the quadrivalent ( GUSTAVSSON 1993). In the present study only one cell demonstrated an association between the sex chromosomes and the translocation configuration. However, a high percentage (41.8 %) of end-to-end association was seen between some autosomes and the quadrivalent, particularly between chromosomes having terminally located kinetochores forming a chromocentre (SCHWARZACHER et al. 1984).

According to another hypothesis ( MIKLOS 1974) it is a prerequisite for normal spermatogenesis that all pairing sites between homologues and the pairing segment of the sex chromosomes have to be saturated by homologous pairing. It is believed that unpaired (‘unsaturated’) chromosome segments, as in the present reciprocal translocation, can prevent spermatogenesis, as a result of failure

110 D. A. F. VILLAG~MEZ ET AL. Hereditm 118 (1993)

of homologous pairing. In both man and mouse, a positive correlation between chromosome pairing failure and germ-cell death has been found in several studies, including male and female gametogenesis. However, it is not known whether the chromosome pairing is the cause or the effect of the degeneration observed (e.g., SETTERFIELD et al. 1988; SPEED and CHANDLEY 1990).

The segments exchanged in the present translocation involved almost the whole short arm of chromosome 2 but only approximately the distal third of chromosome 14. Ring-shaped quadrivalents were seen at diakinesis-metaphase I in most cells of both testes. This means that there should not have been any intrinsic chromosome pairing problems with absence of chiasmata for these cells in the prophase stage.

Although no proper control material was avail- able, our observations indicate that gonadal degeneration can interfere with chromosome pairing in the prophase stage of meiosis. This would explain the fact that more extensive chromosome pairing irregularities were observed in cells of the right testis, which also demonstrated a greater tubular degeneration. It should be remembered that spread spermatocytes showing clear signs of degeneration - chromosome pairing failure and chromosome gaps including SCs other than those of the translocation - were most frequent in the right testis cells (14 versus 7 cells). These cells most often occurred in early pachytene ( 1 1 out of 21 cells), suggesting early germ-cell death during meiosis. Recently, meiotic studies on chromosome translocations in female and male mice have demonstrated a correlation between asynapsed translocation configurations and chromosome pairing anomalies of non-translocation chromosomes. According to MITTWOCH and MAHADEVA- IAH (1992) such chromosome pairing failure may be a symptom rather than a cause of the germ-cell death observed in the translocation carriers.

It was interesting that asymmetrically paired quadrivalents at P, late pachytene demonstrated an interstitial unpaired segment of the arm containing the proximal segments of chromosomes 14. Meiotic investigations of normal boars as well as carriers of various reciprocal translocations have in some cases demonstrated an interstitial unpaired segment of bivalent 14 at late pachytene. Thus, premature desynapsis seemed to occur. Pre- liminary somatic chromosome analyses of such individuals suggest the presence of a duplication (unpublished).

Acknowledgements. -The authors are grateful to Ms Kerstin Lindblad for technical assistance and to Ms Gudrun Wieslander for secretarial assistance. The project was financed by the Swedish Council for Forestry and Agricultural Research.AAk

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