Nine New Cases of Reciprocal Translocation
in the Domestic Pig (Sus scrofa domestica L.)
A. Ducos, H. M. Berland, A. Pinton, E. Guillemot, A. Seguela, M. F. Blanc,
A. Darre, and R. Darre
Nine pigs with decreased litter size or sired by boars with decreased litter size were
found to be reciprocal translocation carriers. Four Large White animals (two females and two males) demonstrated translocations involving chromosomes 1 and
9 (1p2;9p1), 11 and 13 (11q1;13q2), 3 and 13 (3;13)(p1.5;q3.1), and 15 and 17
(15;17)(q1.3;q2.1). Two Large White 3 Pietrain terminal boars demonstrated translocations involving chromosomes 11 and 16 (11;16)(p1.4;q1.4), and 6 and 14
(6;14)(q2.7;q2.1). The (9;15)(p2.4;q1.3) and (6;16)(q1.1;q1.1) translocations were
found in a Large White 3 French Landrace boar, and in a commercial male line
boar with decreased litter size, respectively. A Gascon breed boar with reduced
prolificacy also had an abnormal karyotype, namely 38 XY, rcp(1;6)(q1.2;q2.2). Reduction in prolificacy was estimated accurately in cases 3, 5, 6, 7, and 9 (35%, 30%,
35%, 41%, and 56%, respectively). Rcp(1;6)(q1.2;q2.2) and rcp(6;16)(q1.1;q1.1)
seemed to have been of de novo origin.
Among livestock mammals, reciprocal
translocations are best known in the domestic pig (Sus scrofa domestica L.) and
represent the most widespread chromosome aberration in this species (Popescu
1989). Since the first case reported by
Henricson and Backström (1964), more
than 60 different translocations have been
found ( Ducos et al. 1996). In most instances, isolated detection of a hypoprolific boar, or national programs for herd
management (Gustavsson and Jonsson
1992 ; Popescu and Legault 1988) motivated cytogenetic investigation. More than
50% of all boars with reproductive problems would thus carry a chromosome abnormality (Gustavsson and Jonsson 1992).
In this work, nine new cases of reciprocal
translocation detected in hypoprolific
boars or in pigs sired by a hypoprolific
boar are cytogenetically identified. Estimation of their consequences on prolificacy together with putative origin and
transmission in a pedigree are also reported.
Materials and Methods
From the URA INRA-ENVT de Cytogenetique des Populations Animales, Ecole Nationale Veterinaire de Toulouse
23, chemin des Capelles, 31 076 Toulouse Cedex 3, France.
Address correspondence to Dr. Ducos at the address
above or e-mail: [email protected].
Journal of Heredity 1998;89:136–142
136
Animals
Cases 1 and 2. Chromosome analyses were
performed on a Large White sow reared in
a farm producing pigs for slaughter and on
a Large White boar bred in an experimental herd. Both animals were brought to our
attention because of decreased litter size
(about 25% reduction in prolificacy of the
sow and of the boar’s mates compared
with contemporary boars and sows).
Cases 3, 5, and 7. A Large White purebred boar, a Pietrain 3 Large White boar,
and a Large White 3 French Landrace
boar were spotted by the French National
Programme for Computerized Sow Herd
Management ( NPHM) and analyzed cytogenetically. The mean litter sizes of their
mates were 6.2, 8.2, and 7.2 piglets estimated over 11, 21, and 10 litters, respectively.
Cases 4 and 6. A Large White purebred
boar and a Pietrain 3 Large White boar
with low prolificacy were spotted by the
NPHM again, but were already slaughtered
by the time of detection. Chromosome
analyses were performed on two daughters of the Large White boar (case 4—one
of them exhibited a reciprocal translocation) and on one son of the Pietrain 3
Large White boar (case 6).
Case 8. A boar of a commercial male line
with decreased litter size was suspected
to carry a chromosomal abnormality and
was analyzed cytogenetically. Two full sibs
and 34 offspring of the boar were also investigated.
Case 9. A 2-year-old Gascon breed boar,
having sired less than 5 live-born piglets
per litter for each of 21 litters was analyzed cytogenetically. By investigating 35
relatives of the proband boar, 2 males and
12 females became available for analysis.
Figure 1. Giemsa stained karyotype showing two rearranged chromosomes: 1p2 and 9p1.
Cytogenetic Analysis
The mitotic chromosomes of the translocated pigs and their relatives were prepared from nonsynchronized cultures of
peripheral blood lymphocytes (cases 1–3),
or from synchronized cultures of peripheral blood lymphocytes and fibroblasts
(cases 4–9). Cytogenetic identification was
carried out in cases 1 and 2 on chromosome preparations conventionally stained
with Giemsa. Unfortunately both animals
were slaughtered after this preliminary
analysis. Whole blood (0.5 ml) was cultured during 72 h in a medium consisting
of 8 ml TC199 (Gibco), 20% autologous serum, 500 UI heparin (Sanofi), and stimulated with 0.2 ml pokeweed mitogen (Gibco). Hypotonic treatment (10 ml 1/6 calf
serum) was followed by prefixation and
fixation in ethanol:acetic acid (3:1). Chromosome preparations were spread on
cold wet slides and air dried. Slides were
treated with 0.1% trypsin ( Difco) and
stained with 3% Giemsa solution to generate GTG banding (Seabright 1971). The
FPG technique earlier described for humans ( Dutrillaux and Couturier 1981;
BrdU incorporation during the last 7 h)
was carried out to obtain RBG banding
patterns. Chromosomes were arranged according to the standardized karyotype of
the domestic pig (Committee for the Standardized Karyotype of the Domestic Pig
1988).
Results
Figure 2. Giemsa stained karyotype showing a reciprocal exchange between chromosomes 11 (11q1) and 13
(13p2).
Cytogenetic Investigations
Giemsa staining performed in cases 1 ( Figure 1) and 2 ( Figure 2) yielded information
regarding the chromosomes involved in
the reciprocal translocation. Both translocations result from unequal exchange
leading to rearranged chromosomes much
shorter (or longer) than their normal homologs.
Case 1: rcp(1p2;9p1).Blood lymphocytes demonstrated a 2n 5 38 chromosomal complement with two normal X
chromosomes. All metaphases analyzed
showed two altered chromosomes: a large
telocentric corresponding to chromosome
1 shortened on its small arm (1p2) and a
modified metacentric created by lengthening of the short arm of chromosome 9
(9p1).
Case 2: rcp(11q1;13q2).Giemsa stained
metaphases displayed a 2n 5 38 karyotype for all cells studied. However, most
Ducos et al • Reciprocal Translocations in Pigs 137
Figure 3. GTG-banding karyotype of a boar with the reciprocal translocation rcp(3,13)(p1.5;q3.1).
Figure 4. GTG-banding karyotype of a sow with the reciprocal translocation rcp(15,17)(q1.3;q2.1).
138 The Journal of Heredity 1998:89(2)
of 13q is transferred to chromosome 11
(11q1), whereas chromosome 13 remains
as a minute element (13q2) shorter than
the smallest acrocentric.
Case 3: rcp(3;13)(p1.5;q3.1). Conventional staining demonstrated a large metacentric chromosome just smaller than pair 1.
Application of GTG banding revealed a reciprocal exchange between 3p and 13q.
Break points presumably occurred in
bands 3p1.5 and 13q3.1 ( Figure 3).
Case 4: rcp(15;17)(q1.3;q2.1). This abnormality could not be exhibited by conventional Giemsa staining. GTG banding
indicated a reciprocal exchange between
chromosomes 15 and 17. A distal segment
of the long arm of chromosome 15 was
translocated with a distal segment of the
long arm of chromosome 17. Break points
were likely to occur in the G-banded negative regions of chromosomes 15 (q1.3)
and 17 (q2.1) ( Figure 4).
Case 5: rcp(11;16)(p1.4;q1.4). Application of GTG banding revealed a reciprocal
exchange between 11p and 16q. Break
points presumably occurred in bands
11p1.4 and 16q1.4 ( Figure 5).
Case 6: rcp(6;14)(q2.7;q2.1). Both GTG
and RBG banding techniques indicated the
occurrence of a reciprocal translocation
between autosomes 6 and 14. The break
points have been determined using the
RBG banding pattern (6q2.7 and 14q2.1;
Figure 6).
Case 7: rcp(9;15)(p2.4;q1.3). Application
of GTG banding revealed a breakage in the
negative band q1.3 of the long arm of chromosome 15. The fractured segment was
translocated on the short arm of chromosome 9. A breakage in the terminal G-negative band of the short arm of chromosome 9 (p2.4) and the following translocation of the small resulting fragment on
the extremity of the shortened arm of
chromosome 15 was hypothesized ( Figure
7).
Case 8: rcp(6;16)(q1.1;q1.1). RBG staining was applied to elucidate the chromosome’s recombinations involved in this
abnormality. The whole long arm of chromosome 6 ( break point in the 6q1.1-positive RBG band) was translocated on chromosome 16. Another breakage in the centromeric region of chromosome 16 (RBGpositive band q1.1) and the consecutive
translocation of the small resulting fragment on the extremity of the shortened
arm of chromosome 6 was hypothesized
( Figure 8).
Case 9: rcp(1;6)(q1.2;q2.2). RBG banding
indicated the presence of a reciprocal
translocation between autosomes 1 and 6.
Break points can be seen in the RBG-positive regions in the long arms of the chromosomes within bands 1q1.2 and 6q2.2
( Figure 9).
Figure 5. GTG-banding karyotype of a boar with the reciprocal translocation rcp(11,16)(p1.4;q1.4).
Figure 6. RBG-banding karyotype of a boar with the reciprocal translocation rcp(6,14)(q2.7;q2.1).
Effect of the Translocations on
Prolificacy
Data on boar’s mates prolificacy was provided by the NPHM and used to estimate
the effect of reciprocal translocations 3, 5,
6, and 7 ( Table 1; the translocation 6 was
found in a daughter of a hypoprolific boar,
which was likely to also carry the abnormality). The decrease in prolificacy due to
the translocations ranged from 30% (case
5) to 41% (case 7). The boar carrier of
translocation 9 had sired 21 litters on a
single farm with a mean of 3.8 live-born
piglets (range 2–5). Compared with the average prolificacy in the Gascon breed (8.6;
Lucquet J, personal communication), this
represents a reduction of 56%. The mates
of the boar carrier of translocation 8 exhibited a low prolificacy (results of seven
litters were available, from which six included only six piglets each). Unfortunately, results related to contemporary boars
were not provided by the selection company.
Origin and Transmission of the
Translocations
Pedigree studies and cytogenetic investigations of relatives were performed for
translocations 8 and 9.
Case 8. The karyotypes of 34 offspring
(from seven sows) of the boar were analyzed. Normal piglets and translocation
carriers were found in all the litters. The
total number of carriers was 17 (i.e., exactly 50%). The karyotypes of two full sibs
of the boar (one male and one female) did
not exhibit any abnormality. The prolificacy of the parents and grandparents of
the boar appeared normal (sire: 12 litters
known, with 11.4 piglets born/litter on average; dam: 2 litters known, with 12 piglets
born/litter on average; paternal grand-sire:
7 litters known, with 13.8 piglets born/litter on average; paternal grand-dam: 7 litters known, with 12.3 piglets born/litter on
average; maternal grand-sire: 4 litters
known, with 11.4 piglets born/litter on average; maternal grand-dam: 6 litters
known, with 15.3 piglets born/litter on average). These results suggest a de novo origin of translocation 8.
Case 9. Eight offspring (from three sows)
of the translocated proband boar were
karyotyped. Three of them were found to
be carriers of the same translocation. The
dam of the translocated boar demonstrat-
Ducos et al • Reciprocal Translocations in Pigs 139
ed a normal karyotype. The sire, culled in
1992, could not be investigated. However,
two paternal half-sisters had a normal
karyotype, as did four female offspring of
one half-sister of the sire. Moreover, mean
prolificacy of four male parents of the
boar (the sire, the grand-sire, . . . , etc.)
ranged from 5.2 to 7.6 piglets per litter
(rather normal litter sizes in this breed).
Therefore rcp(1;6)(q1.2;q2.2) also seemed
to have occurred spontaneously.
Discussion
Figure 7. GTG-banding karyotype of a boar with the reciprocal translocation rcp(9,15)(p2.4;q1.3).
Figure 8. RBG-banding karyotype of a boar with the reciprocal translocation rcp(6,16)(q1.1;q1.1).
140 The Journal of Heredity 1998:89(2)
With regard to cases 1–8, no similar translocation has been reported in the literature. However, limited reliability associated with the lack of discrimination of conventional staining does not allow us to
thoroughly determine whether or not
rcp(1p2;9p1) and rcp(11q2;13q1) represent new abnormalities. Moreover, more
accurate molecular techniques (in situ hybridization with adequate molecular
probes) should be used in the future to
confirm the chromosomal rearrangements
hypothesized for translocations rcp(9;15)
(q1.3;p2.4) and rcp(6;16)(q1.1;q1.1).
A reciprocal exchange between 1p1.1
and 6q3.5 was found in a Large White boar
with 25% decreased litter size ( Lockniskar
et al. 1976). A reciprocal whole-arm translocation, rcp(1;6)(1p6;1q6), was also identified in a Swiss Large White boar with reduced fertility ( Yang et al. 1992). Nevertheless, the chromosomal abnormality discovered in the Gascon breed, that is,
rcp(1;6)(q1.2;q2.2), seems to represent a
distinct case.
Any effect of reciprocal translocations
on the phenotype of balanced carriers
might be discarded by now. Only two
cases of congenital malformations (Gustavsson and Jonsson 1992; Hansen-Melander and Melander 1970) and four pigs with
full sterility (Astachova et al. 1991; Bouters et al. 1974; Madan et al. 1978; Parkanyi
et al. 1992) including an intersex (Madan
et al. 1978), were recorded out of more
than 60 translocations. Quantitative consequences of embryonic death on the reduction of litter size differ from one translocation to another [range 5% (Golish et
al. 1982) to 100% (Astachova et al. 1991;
Bouters et al. 1974; Madan et al. 1978; Parkanyi et al. 1992)] and from one carrier to
the other for the same chromosomal abnormality [range 31% ( Bonneau et al.
1991) to 72% (Popescu and Boscher
1986)]. These last differences could be
due in part to different breeding management practices such as the use of double
Table 1. Effects of the reciprocal translocations
on prolificacy
Translocation case no.
3
Number of litters sired by
the translocated boar
11
Mean litter size (number of
piglets born) of the trans7.1
located boara
Mean litter size (number of
piglets born) of the contem10.9
porary boarsa
Decrease in litter size due
to the translocation
35%
a
Figure 9. RBG-banding karyotype of a boar with the reciprocal translocation rcp(1,6)(q1.2;q2.2).
service or variable parity degrees of sows
for data uncorrected from this effect. Both
figures obtained in cases 3, 5, 6, 7, and 9
(35%, 30%, 33%, 41%, and 56%, respectively) border on the average effect observed
until now (a total reduction of 43% can be
computed from 40 anomalies for which reliable figures are available).
The de novo origin of a reciprocal translocation has rarely been established thoroughly in the pig ( Konfortova et al. 1995),
though paternal or maternal transmission
was proven in several instances ( Förster
et al. 1981; Gustavsson et al. 1989). Ancestors usually are not available for pedigree
studies, being culled at the time of analysis. On the basis of normal or above average prolificacy, the authors frequently
infer that the sire (and/or the dam) should
not carry the translocation ( Bonneau et
al. 1991; Gustavsson et al. 1988; Kuokkanen and Mäkinen 1987, 1988; Mäkinen et
al. 1987). Variability of the effect of translocations on prolificacy seems to cast a
doubt on such conclusions: on the one
hand a translocated carrier may demonstrate a reproductive performance within
normal range; on the other hand, two related pigs carrying the same translocation
can demonstrate a drastic reduction in
prolificacy and nearly acceptable litter
size. Insemination of females with frozen
sperm sampled from the sire of the translocated Gascon boar and kept at the INRA
Center of Rouille, or cytogenetic analysis
of such spermatozoa using the heterospecific zona-free hamster oocyte penetration technique ( Benkhalifa et al. 1992;
Bonneau et al. 1992) could dispell the uncertainty remaining for the (sire) origin of
translocation case 9.
The discovery of nine new cases of reciprocal translocation, either fortuitous or
issued from elaborated screening programs, allowed us to complete in part our
knowledge about chromosomal structural
abnormalities in the domestic pig.
Through studies carried up to 1990, we
were able to probe the range of basic
questions raised by these chromosomal
peculiarities: do reciprocal translocations
take place randomly along the genome or
especially on some chosen segments
(chromosomes, bands, DNA sequences)?
Is there a balance between hereditary
transmission of these anomalies and their
de novo origin? Do they beget significant
effects on carrier phenotype characteristics?
Pieces of information relative to these
topics, which are still discussed in most
species including humans, could arise
from a more systematic approach (screening, modelization, eradication) of the re-
5
6
7
21
37
10
8.2
8.0
7.2
11.7
12.3
12.3
30%
35%
41%
Data corrected for sow parity effect.
ciprocal translocations, which were until
now looked upon as interesting oddities
and essentially considered from an individual point of view. Logistic constraints
and financial cost have restricted the number of studies carried out in the domestic
pig. However, increasing use of chromosome markers in gene mapping could tip
the balance. For instance, a reciprocal
translocation involving both chromosome
1 and 6 centromeric regions recently provided a unique chromosome marker to accurately localize the calcium release channel and glucose phosphate isomerase
genes ( Yang et al. 1992). Otherwise prolificacy is from now on the most important
component of the selection objective of
most pig selection schemes ( Ducos 1995).
Great endeavors have been made to improve the prolificacy of most pig populations by selection ( Bidanel and Ducos
1994). Screening and eradication of reciprocal translocations (which counteract
current selection objectives) appear more
and more necessary to pig breeders. In
France, the main pig artificial insemination
centers recently decided to analyze the
karyotypes of all purebred boars before
service to ensure the chromosomal quality of these animals.
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Corresponding Editor: Robert J. Baker