MEIOSIS IN MALE DROSOPHILA MELANOGASTER.
11. NONRANDOM SEGREGATION OF
COMPOUND-SECOND CHROMOSOMES.1
RICHARD C. GETHMANN
Department of Biological Sciences,
University of Maryland Baliimore County,
Caionsuille, Maryland 21228
Manuscript received April 9, 1975
Revised copy received March 8, 1976
ABSTRACT
The segregation of compound-second chromosomes in males from two different stocks has been examined. Segregation is random in males from the
C(2L)RM4, dp; C(2R)RM4, px stock. Gametes containing only one of the two
compound chromosomes comprise 50% of the gametes, and gametes containing
either both elements or neither element make up the other 50% of the gametes.
-In
males from the C(2L)RM, b; C(2R)RM, cn stock, gametes containing
either C(2L)RM, b or C(2R)RM, cn make up the majority of the gametes.
Gametes containing both chromosomes or neither chromosome account for only
2-3% of the gametes. The nonrandom segregation is due to the C(ZR)RM, cn
chromosome.--Viability
is reduced in flies carrying the C(2R)RM, cn
chromosome. This includes larval lethality, delayed development and premature adult lethality. Cytologically, this chromosome contains a large duplication of 2L material, which includes material proximal to region 38 or 39. It
is suggested that the viability and segregational properties associated with this
chromosome are due to the duplicated 2L material.
COMPOUND chromosomes are a class of rearranged chromosomes in which
two homologous arms are attached to the same centromere, rather than being attached to different centromeres. For the two major autosomes, the diploid
complement is represented by a compound-left chromosome and a compoundright chromosome. These chromosomes have been a valuable tool in studying
problems of meiosis in Drosophila. They have been used to study crossing over
(BALDWIN
and CHOVNICK
1967; LEWIS1967), radiation-induced nondisjunction
and compound formation (BATEMAN1968), nonhomologous pairing in females
( GRELL1970; HOLM
and CHOVNICK1975) and gene conversion (see CHOVNICK,
BALLANTYNE
and HOLM
1971 for a review).
With respect to the segregational behavior of compound autosomes, GRELL
(1975) concluded that in females, they are
(1970) and HOLMand CHOVNICK
regular members of the distributive pool. In females lacking any other type of a
rearranged chromosome, the two compound chromosomes regularly disjoin from
Supported by Grant GB38446 from the National Science Foundation and Grant GM 22050-01 from National Institutes
of Health.
Genetics 83: 743-751 August, 1976
744
R. C. GETHMANN
each other, resulting in gametes containing either a compound-left chromosome
or a compound-right chromosome.
I n males, BALDWINand CHOVNICK(1967); HOLM,
DELAND
and CHOVNICK
(1967) ; GRELL(1970) and HOLM
and CHOVNICK(1975) concluded that segregation is random or near random. SANDLER
et al. (1968) used compound-2 males
to measure second chromosome nondisjunction in females and reported that
males from different compound-2 stocks appeared to produce different arrays of
gametes. Specifically they found that males from one stock [C(2L)RM4, d p ;
C(2R)RM4, px] produced more C(2L); C(2R) and nullo-2 gametes than did
males from another stock [C(2L)RM, b; C(2R)RM, c n ] . EVANS(1971) found
a deficiency of C(BL);C(ZR) and nullo-2 gametes from C(2L)RM, b; C(2R)RM,
cn males and suggested that chromosome segregation in these males was nonrandom. The following is an analysis of the two compound stocks used by SANDLER et al. I n the C(2L)RM4, d p ; C(2R)RM4, px stock, segregation is random;
whereas in the C(2L)RM, b; C(2R)RM, cn stock, segregation is nonrandom.
The nonrandom segregation is due to the C(2R)RM, cn chromosome.
MATERIALS A N D METHODS
The four compound chromosomes examined in this study were X-ray induced several years
ago at Cal Tech by I. E. RASMUSSEN,
E. ORIASand E. B. LEWIS(E. B. LEWISpersonal communication; RASMUSSEN
1960). Two other compound stocks were used extensively in testing these two
stocks. One was a C(I)RM, y / B s Y ; C(,?L)RM,
C(,?R)RM, f stock synthesized by E. H.
GRELL.The other compound chromosome was the C(2) EN chromosome of NOVITSKI.This
chromosome is an attachment of two complete second chromosomes to one centromere. The
chromosome is a reversed metacentric of the order 2RZL.ZLZR (NOVITSKIpersonal communication). Flies from this stock can produce only two types of gametes, diplo-,?and nullo-,?.
All egg-count tests were made with single virgin females 2-3 days old mated with three young
males. The parents were transferred every 12 hours for four consecutive days, after which they
were discarded. Egg counts were made immediately after transferring and egg-hatch counts were
made 24 hours later. Crosses to the C ( I ) R M , y/BsY; C(,?L)RM,
C(ZR)RM, females were
made with three females and four males and were transferred every four days for a total of five
transfers. Flies were raised on a standard cornmeal, molasses and agar media at 25".
+;
+;
+
RESULTS
The results of crosses designed to examine the kinds and frequencies of segregation in C(2L)RM4, d p ; C(2R)RM4, px andC(2L)RM, b; C(2R)RM, cn males
are listed in Table 1. The crosses to C(2L)RM4, d p ; C(2R)RM4, px o r C(2L)RM,
b; C(2R)RM, cn females measure the frequency of C(2L) and C(2R) gametes,
and the crosses to C(2)EN, c bw females measure the frequency of C(2L); C(2R)
and nullo-2 gametes. Cross 3 is a test of the segregation in C(2L)RM4, dp;
C(2R)RM4, px females. In this cross, the only viable progeny are those resultifig
from C(2L); C(2R) and iiullo-2 gametes from the female, as the C(2)EN, c bw
males can produce only two types of gametes, diplo-2 and nullo-2. Only 0.5% of
the eggs hatched, indicating that in females, the two compound chromosomes
regularly separate from each other.
745
NON-RANDOM SEGREGATION IN DROSOPHILA
TABLE 1
Survival of progeny from crosses of compound-2 flies
Cross'
9
Cross no.
X
d"
Number
hatch
Freq.
hatch
Number
adults
Freq.
adults
dp;px x dp;px
dp;px x b;cn
dp;px x c b w
853
1052
754
214
438
4
0.25 1
0.416
0.005
208
350
3
0.24-1.
0.333
0.004
5.
b;cn X dp;px
b;cn x b;cn
627
270
132
108
0.21 1
0.400
98
36
0.156
0.133
6.
7.
8.
cbw
cbw
cbw
x dp;px
x b;cn
x c bw
1051
1030
1037
185
9
339
0.176
143
8
300
0.136
0.008
0.289
1.
2.
3.
4.
o.o(E9
0.327
* Different compound-second chromosomes are indicated by their genetic markers.
When C(2L)RM4, dp; C(2R)RM4, px males are crossed to C(2L)RM4, dp;
C(2R)RM4, px females, 25% of the eggs hatch and eclose (cross 1 ) . This indicates that 50% of the male gametes contain either C ( 2 L ) or C(2R). When
C(2L)RM, b; C(2R)RM, cn males are crossed to C(2L)RM4, dp; C(2R)RM4,
px females (cross 2),over 40% of the eggs hatch.
When C(2L)RM4, dp; C(2R)RM4, px males are crossed to C(2)EN, c bw
females, 18% of the eggs hatch (cross 6). Assuming random segregation in the
dp; px males, one would predict a 25% egg hatch. When C(2L)RM, b; C(2R)
R M , cn males are crossed to C(2)EN, c bw females, less than one percent of the
eggs hatch (cross 7). Taken together, these results indicate that C(2L)RM4, dp;
C(2R)RM4, px males produce more C ( 2 L ) ; C(2R) and nullo-2 gametes than
do the C(2L)RM, b; C(2R)RM. cn males.
The reduced egg hatch observed in the crosses with the C(2)EN, c bw females
is most likely a lethal effect associated with the C(2)EN chromosome. This is
illustrated by the results of cross 8. I n cross 8, C(2)EN males were crossed to
C(2)EN females. Assuming random segregation in either parent, a 50% egg
hatch should result, but only 33% of the eggs hatched. If one assumes no prehatch lethality, a 33% egg hatch would require a 4:1 segregation in both parents
(i.e., 80% diplo-2 gametes and 20% nullo-2 gametes, or vice versa). It seems
highly unlikely that the gametic array from both sexes would deviate this much
from a 1:l ratio. As an alternative, a pre-hatch lethality could explain the reduction in egg hatch. If this were the case, then only 65% of the diploid zygotes
survived. If this correction is applied to crosses 6 and 7, then the corrected hatch
frequency for the C(2L)RM4, dp; C(2R)RM4, px males is 26.9%, and for C ( 2 L )
R M , b; C(2R)RM, cn males, 1.3%.
Several problems were encountered with crosses involving the C ( 2 L )RM,
b; C(2R)RM, cn flies. First, there is a high larval mortality rate. This can be seen
in crosses 2, 4 and 5 of Table 1 . In all three crosses, a significant number of the
larvae failed to survive. I n cross 5, larvae could be observed crawling about on
the surface of the food twelve to fourteen days after the parents were removed.
These larvae failed to burrow into the food and eventually died.
746
R . C. GETHMANN
TABLE 2
Progeny recovered from crosses of C(2L)RM4, dp; C(2R)RM4, px X C(2L)RM, b; C(2R)RM, cn
dp;px x b;cn
b;cn x dp;px
TOTAL
8 =225
67
15
82
0 = 223
106
35
141
dp;cn = 180
81
17
98
b;px = 268
96
31
127
350
98
448
* Different compound-second chromosomes are indicated by their genetic markers.
The progeny from crosses 2 and 4 are given in Table 2. I n both crosses, four
classes of offspring were expected: dp; c n males and females, and b; px males
and females. These should occur with equal frequency. As can be seen in Table
2, the b; px flies occur more frequently than do the d p ; cn flies. These progenies
were recovered from single females and the cultures were relatively uncrowded.
When mass crosses were made between C(2L)RM4, dp; C(2R)RM4, px females
and C(2L)RM, b; C(2R)RM, cn males, only b; px offspring were recovered.
Thus, it would appear that in a competitive situation, dp; c n flies cannot successfully compete with their b; px sibs. This also appears to be true to a lesser degree
in uncrowded cultures.
I n general, stocks containing the C(ZR)RM, c n chromosome have been difficult to maintain. Surviving adults appear to be phenotypically normal, although
there is a high mortality rate. Many of the adults die within a week or so after
eclosion.
In C(2L)RM4, dp; C(2R)RM4, px males, gametes containing either C ( 2 L )
or C(2R) make up 50% of the gametes, and C ( 2 L ) ; C(2R) and nullo-2 gametes
make up the other 50%. Thus, for this combination of compound chromosomes,
segregation is random.
I n males from the C(2L)RM, b; C(2R)RM, c n stock, segregation is not random. The majority of the gametes contain only one of the two compound chromosomes. Because of viability problems with the C(ZR)RM, cn chromosome, it is not
clear what the actual gametic frequencies are. Based on the crosses in Table 1,
it appears that the two compound chromosomes separate in at least 80% of the
meiocytes (from cross 2) and perhaps in as many as 97% of the meiocytes (from
cross 7). These conclusions are confirmed by the data given in Table 3, which
C(2R)RMy f
lists the results of crosses to C ( I ) R M , y/BsY; C(2L)RMy
females. GRELL(1970) used this stock to examine distributive pairing of compound autosomes in females. He concluded that the three compound chromosomes and BSY were all members of the distributive pool. When these females
were crossed to C ( 2 L ) ; C(2R) males, he found that 10-15% of the progeny
received both of their compound autosomes from the same parent.
Crosses were made with males from the two stocks, as well as crosses with
C(ZL)RM, b; C(2R)RM4, px and C(2L)RM4, dp; C(2R)RM, cn males. These
latter two males carry the C(2L) chromosome from one stock and the C(2R)
chromosome from the other stock. Considering first the cross with C(2L)RM4,
+;
747
NON-RANDOM SEGREGATION IN DROSOPHILA
TABLE 3
+;
Offspring from cross of C(1)RM, y/BsY; C(2L)RM,
C(2R)RM, f females
crossed to different C (2L)R M ; C (2R) RM males
Parental male*
Male gamete
x;C(2L)
Y ; C(2L)
X ; C(2R)
Y;C(2R)
X ; C ( 2 L ) ; C(2R)
Y ; C ( 2 L ) ; C(2R)
0
Y ;0
TOTAL
Freq. ( 2 L 2R)
Freq. ( 2 L ; 2R SO)
x;
+
dp;px
b;cn
dp;cn
b;px
138
133
85
110
1
18
30
14
529
0.881
0.119
400
428
338
346
0
1
244
209
182
21 1
129
107
115
130
2
4
1
1518
0.996
0.004
1
0
6
1
854
0.991
0.009
21
36
18
558
0.862
0.138
* Different compound-second chromosomes are indicated by their genetic markers.
dp; C(2R)RM4, px males, 19 C(2L); C(2R) and 44 nullo-2 gametes were recovered from a total of 529 offspring. This is a frequency OP 11.9%. The distribution
of the offspring in this cross was the same as that found by GRELL(1970) in his
crosses. When C(BL)RM, b; C(PR)RM, cn males were tested, only one C(2L);
C(2R) gamete and 5 nullo-:! gametes were recovered from 1518 offspring. This
is a frequency of less than one-half of a percent. Since the females used in these
crosses were the same, the differences in the distribution of progenies must be due
to differences in the segregation in the males. These results confirm the conclusions of the egg-count experiments.
Crosses were also made with C(2L)RM4, d p ;C(2R)RM, cn and C(2L)RM, b;
C(2R)RM4, px males to determine which chromosome was responsible for the
nonrandom segregation. From the dp; cn males, less than one percent of the
gametes were C(2L); C(2R) and 1111110-2, whereas from the b; px males, 13.8%
of the gametes were of those two types. This indicates that the nonrandom segregation is due to the C(2L)RM, cn chromosome.
It is unlikely that the differences between these crosses are due to viability
problems associated with the various combinations of the compound chromosomes. In all four crosses, nulio-2 gametes from the male parent will yield offspring with both compound chromosomes from the female parent, and these
should have the same viability. In the crosses with dp; px and b; px males,
nullo-2 gametes accounted for 6.4% (34/529) and 9.7% (54/558) of the total
progeny, while in the crosses with the b; cn and dp; cn males, nullo-2 gametes
accounted for 0.3% (5/1518) and 0.8% (7,4354) of the total progeny.
The data in Table 3 can be used to estimate the frequency of C(2L); C(2R)
and nullo-2 gametes from the males carrying C(BR)RM, cn. The frequency of
C(2L); C(2R) and nullo-2 gametes from the female parent can be estimated
from the crosses to males carrying the C(2R)RM4, px chromosome, if it is
748
R. C. GETHMANN
assumed that segregation in these males is random. With this assumption, the
frequency of C(2L); C(2R) and nullo-2 gametes from the female is 13%. Using
this figure, one can estimate that the frequency of C(2L); C(2R) and nullo-2
gametes from the males carrying C(2R)RM, cn is about 4%.
From the crosses in Table 1. the corrected estimates for C(2L); C(2R) and
nullo-2 gametes are 2.6% (cross 7) and 17% (cross 2). Most likely, the true
value is somewhere between these two extremes, although given the viability
problems associated with the C(2R)RM, cn chromosome, the estimates from
cross 7 (Table 1) and from Table 3 are probably closer to the true value. Regardless of what the actual frequency may be, it is clear that segregation is not random, and that the two chromosomes disjoin at a high frequency.
Finally, an attempt was made to localize the region of C(2R)RM, cn responsible for its segregational behavior. Specifically, could this behavior be due to a
meiotic mutant carried by this chromosome, or is it due to some structural
rearrangement of the chromosome? Since most meiotic mutants are recessive, this
possibility could be examined by selecting recombinants between a normal second chromosome and the C(2R)RM, cn chromosome from triploids. Triploid
females of the constitution Pin2/C(2L)RM, b; C(2R)RM, cn were constructed
and crossed to C(2L)RM, b; C(2R)RM4, px males. Diploid b; cn Pin2 flies were
collected and stocks were established from these. Ten such recombinants were
found, but only one stock was successfully established. Approximately half of the
recombinants recovered were either sterile or produced too few progeny, while
the other half died a few days after eclosion.
The b; cn Pin2 stock was established from a single male and was maintained
by backcrossing b cn Pin2 males to C(2L)RM, b; C(2R)RM4, px females. The
segregation of the recombinant compound chromosome in males was the same
as that in males from a C(2L); C(2R)RM. cn stock. This would suggest that the
nonrandom segregation was not due to a distally located, recessive meiotic mutant. Thus, although only one recombinant was successfully tested, it would
appear that the reason for the nonrandom segregation of this chromosome is due
to something in the proximal part of the chromosome, rather than the distal part.
DISCUSSION
The results of these experiments indicate that segregation in C(2L)RM, b;
C(2R) RM, cn males is nonrandom. Furthermore, the nonrandom segregation is
due to the C(2R)RM, cn chromosome, and the region responsible f o r this is most
likely proximal.
Two possible mechanisms have been suggested for the formation of compound
(1940) and BATEMAN
(1968) suggested the possibility
autosomes. DARLINGTON
of centromere misdivision, while others (RASMUSSEN
1960; LEIGHand SOBELS
1969; BALDWIN
and SUZUKI1971) favored a two-break mechanism. This latter
mechanism involves breaks on either side of the centromere in two homologous
chromosomes, with subsequent joining to produce the compound chromosomes.
By this mechanism, each compound would be deficient f o r some unknown portion of the proximal centric heterochromatin and duplicated f o r some unknown
N O N - R A N D O M SEGREGATION IN DROSOPHILA
749
portion of the proximal heterochromatin of the other chromosome arm (i.e.,
C(2R) would be deficient for some of the proximal 2R heterochromatin and
duplicated for some proximal 2 L heterochromatin). By the misdivision model,
all compound chromosomes would be expected to have a diploid complement of
heterochromatin, which should be structurally normal. Considering what is
known about compound chromosomes and their behavior, it seems reasonable
to conclude that the mechanism of formation of compound autosomes is not by
centromere misdivision, but rather, is by asymetrical exchanges on opposite sides
of the centromere.
The developmental properties of C(2R)RM, cn are consistent with this notion.
Thus, the reduced viability, delayed development and premature adult lethality
characteristic of this chromosome could be due to the duplicated and/or deficient
regions of the chromosome. Cytologically, C(2R)RM7 cn is characterized by a
large duplication of 2 L material (LEWIS,personal communication). This duplication apparently includes all of the material proximal to region 38 or 39. Thus,
it includes all of the heterchromatin of 2L, as well as a relatively large block of
euchromatin. A duplication of this size would be expected to have developmental
properties Characteristic of C(2R)RM, cn. It is tempting to speculate that the
duplication is also responsible for the nonrandom segregation.
In females, nonrandom segregation of compound chromosomes results from
the pairing of the two chromosomes in distributive pairing (GRELL1970; HOLM
and CHOVNICK
1975). HOLM
and CHOVNICK
(1975) examined the segregation of
several combinations of compound-3 chromosomes. In all cases, the compounds
disjoined from each other in females, although there were differences for different combinations of chromosomes, especially when other competitive chromosomes were present. They concluded that the differences in the distributive disjunction of the compound chromosomes was probably due to differences in the
breakpoints in the centric heterochromatin, which affected the compethve pairing ability of these chromosomes at distributive pairing. They found no evidence
that segregation of compound chromosomes in males was nonrandom.
C(2R)RM, cn is an exception to the rule of random segregation of compound
autosomes in males, and it differs from other C(2R) chromosomes by the size of
the duplicated 2 L material. For example, C(2R)RM4, px is not duplicated for
the light locus ( GETHMANN
unpublished). Thus, C(2R)RM4, p z is duplicated
for only the proximal 2 L heterochromatin, as compared to C(2R)RM, cn, which
is duplicated for all of the 2L heterochromatin, as well as the euchromatin proximal to region 38 or 39. Presumably, the large block of 2 L heterochromatin in
C(2R)RM, cn is responsible for the nonrandom segregation. Two possible mechanisms for nonrandom segregation are nonhomologous pairing and meiotic drive.
Meiotic drive normally renders one of the two reciprocal segregational classes
nonfunctional. However, in the case of C(2R)RM, cn, the C(2L); C(2R) and
nullo-2 gametes are the deficient classes, and these are reciprocal segregants.
Thus, meiotic drive would have to cause dysfunction of both reciprocal classes
when the compound chromosomes segregated together, but would have no effect
when they segregated to opposite poles.
750
R. C. GETHMANN
A more plausible explanation is nonhomologous pairing. Since C ( 2 R ) R M , cn
is duplicated for all of the 2 L heterochromatin, nonhomologous pairing could be
occurring because of either the presence of specific pairing sites in the heterochromatin, or because of the presence of the unbroken block of heterochromatin.
Both possibilities suggest that the centric heterochromatin has an important function in synapsis and disjunction of autosomes in males.
With respect to the first possibility, the segregation of Y-2 translocations in
males has suggested that there may be specific pairing sites in the heterochromatin (GETHMANN
1974 and unpublished). In males heterozygous for a Y-2
translocation, where the second chromosome break is close to the centromere,
homologous centromeres almost always disjoin from each other. Homologous
arms attached to nonhomologous centromeres (i.e., a normal second chromosome
and a 2 L or 2R arm attached to a Y centromere) often segregate together. Several
translocations with breaks in different regions of the heterochromatin have been
examined, and all give this kind of a segregational pattern. Thus, the segregation
of these translocations suggests that some region in the heterochromatin that is
close to the centromere is involved in chromosome pairing and/or disjunction in
males.
With respect to the second possibility, C(2R)RM, cn would be able to pair and
disjoin from a C ( 2 L ) chromosome because both chromosomes contained an
intact, unbroken section of 2L heterochromatin. Other compound-second chromosomes would be unable to synapse and disjoin because the breaks in the heterochromatin would be sufficient to disrupt pairing. Thus, by this interpretation,
the critical region for chromosome pairing is the heterochromatin, but for pairing
to be effective, the region must be unbroken. This possihility is similar to that
reported by HOLMand CHOVNICK(1975) for distributive pairing in females.
Thus, it may be that in both sexes, pairing and disjunction can be disrupted by
breaks in the centric heterochromatin. This, in turn, raises the possibility that
chromosome pairing in males may have some features in common with distributive pairing in females. Possibly, these two systems may have been derived from
some common ancestoral system, although certainly, each has become greatly
modified.
Clearly, further experiments on the role of the centric heterochromatin in
chromosome pairing are needed. Such experiments might include a cytological
analysis of meiosis in compound autosome males, experiments designed to determine the extent of the duplicated regions in various compound chromosomes, and
the synthesis of new compound autosomes with known rearrangements in the
heterochromatin.
I would like t o thank DR. E. B. LEWISfor his generosity and time for the cytological examination of C(2R)RM, cn. I would also like to thank DRS.E. H. GRELL
and E. NOVITSKI
for making
available their compound-second chromosome stocks.
LITERATURE CITED
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NON-RANDOM SEGREGATION I N DROSOPHILA
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A. J., 1968 Nondisjunction and isochromosomes from irradiation of chromosome 2 in
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A., G. H. BALLANTYNE
and D. G. HOLM,1971 Studies on gene conversion and its
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