Acta Theriologica 55 (1): 1–8, 2010.
doi: 10.4098/j.at.0001-7051.048.2009
PL ISSN 0001-7051
Non-disjunction frequency in male complex Robertsonian
heterozygotes of the common shrew
Stanis³aw FEDYK and W³odzimierz CHÊTNICKI
Fedyk S. and Chêtnicki W. 2010. Non-disjunction frequency in male complex
Robertsonian heterozygotes of the common shrew. Acta Theriologica 55: 1–8.
Common shrews display two types of Robertsonian (Rb) heterozygosity:
simple (where CIII configurations are formed at meiosis I) and complex (which
have longer meiotic chains or rings). Based on an analysis of large sample
sizes (over 100) of MII cells per specimen, we estimated the non-disjunction
frequency in seven Rb homozygotes and 21 complex Rb heterozygotes (CIV
and CV) of Sorex araneus Linnaeus, 1758. The analysis showed high betweenindividual variability. The mean level of non-disjunction in homozygotes
(2.01%) was significantly lower than in CIV and CV heterozygotes (4.27% and
5.78%, respectively). The study demonstrated that non-disjunction frequency
in male CIV and CV heterozygotes was similar to that in simple heterozygotes
in the common shrew.
Institute of Biology, University of Bia³ystok, Œwierkowa 20B, 15-950 Poland, e-mail: [email protected]
Key words: Sorex araneus, hybrid zones, meiotic segregation, fertility of hybrids
across the entire species range (Wójcik et al.
2003, Averianov 2007). These races come into
contact and form hybrid zones. Two types of
hybrid zones are known. (1) A wide area of
hybridisation with production of simple Rb
heterozygotes (hybrids forming chain-of-three
(CIII) configurations at meiosis I) because of the
presence of metacentric chromosomes in one
race and homologous acrocentric chromosomes
in the other (Lukáèová et al. 1994). (2) Narrow
hybrid zones between races which differ in the
arm combination of metacentric chromosomes,
and in which hybrids are complex Rb heterozygotes, ie which form chains or rings of at least
4 chromosomes at meiosis I (Searle 1986, Narain
and Fredga 1996). In the case of contact between
polymorphic races the two types of heterozy-
Introduction
In the common shrew Sorex araneus Linnaeus,
1758 Robertsonian (Rb) processes (centric fusions of acrocentric chromosomes) and most
probably also whole-arm reciprocal translocations (WARTs), are responsible for chromosomal
variation in both the number of chromosomes
(2N = 20–33) and the combination of arms of
metacentric chromosomes (cf Searle and Wójcik
1998). As a consequence, within a single population both acrocentric and metacentric morphs
may occur, and there also exists enormous geographic differentiation. Over 70 chromosomal
races that differ in arm combinations of metacentric chromosomes have been described to date
[1]
2
S. Fedyk and W. Chêtnicki
gotes co-occur in the hybrid zone (Fedyk 1986,
Fedyk et al. 1991, Fredga and Narain 2000).
Both types of heterozygotes are suspected to
be less fertile than homozygotes due to meiotic
abnormalities. The formation of trivalents or
longer meiotic complexes instead of normal bivalents may result in abnormal pairing of chromosomes at pachytene and/or lead to non-disjunction
of chromosomes in anaphase I, and in consequence, increase germ cell death or reduce fetal
viability. Such results were convincingly documented for heterozygous mice and other mammals (for review see Searle 1988, 1993).
There are suggestions that complex Rb heterozygotes in S. araneus are less fertile than simple Rb heterozygotes, and above all, less fertile
than homozygous shrews (cf Searle and Wójcik
1998). Based on this premise, Hatfield et al.
(1992) created a model that treated the hybrid
zone of Oxford and Hermitage races as a tension
zone. Computer simulations demonstrated that
the acrocentric peak, treated as a post-hybridization modification, may reach the level observed
(Searle 1986), provided that selection against
complex Rb heterozygotes will be sufficiently
strong in relation to selection against simple Rb
heterozygotes (Hatfield et al. 1992). This model,
however, has not been unambiguously confirmed
by empirical studies. Although meiotic disturbances have been observed in the common shrew
(Garagna et al. 1989, Searle 1990, Narain and
Fredga 1996, 1997, Banaszek et al. 2000, 2002),
both types of heterozygous S. araneus do not sustain as large a decrease in fertility as the house
mouse and several other mammal species. It also
should be emphasized that larger sample sizes of
MII cells were used sporadically in meiotic studies of S. araneus (eg Banaszek et al. 2002). In the
majority of previous papers small numbers of
cells were scored: 86 in 13 shrews (Fedyk 1980),
198 in 6 shrews (Searle 1986a), 277 in 17 shrews
(Mercer et al. 1991), 91 in 11 shrews (Jadwiszczak and Banaszek 2006), 16 in 3 shrews (Mercer
et al. 1992), which casts doubt on the reliability of
the estimated rate of gamete aneuploidy.
Recently, we had the opportunity to score large
numbers of MII cells in male common shrews;
data concerning percentage of non-disjunction
in 12 simple Rb heterozygotes have been pub-
lished (Fedyk and Chêtnicki 2007). The present
study focused on frequencies of non-disjunction
in male common shrews that are homozygotes
and complex Rb heterozygotes expected to form
chain-of-four (CIV) and chain-of-five (CV) configurations during meiosis (see Searle 1993 for
diagrams of these meiotic configurations).
Material and methods
Materials
This study estimated the frequency of non-disjunction
based on an analysis of large sample sizes of MII cells from
male common shrews. Shrews in which less than 100 MII
cells were scored were excluded from this study. The study
material included 7 homozygous males representing three
chromosomal races (Table 1) and 21 complex (CIV and CV)
heterozygotes (Table 2). These heterozygous shrews were
captured at several populations within the contact area of
four chromosomal races: Drnholec (Dn), Popielno (Po), £êgucki M³yn (£g), and Guzowy M³yn (Gu) (cf Fedyk et al.
2008).
Karyotypes of all examined males were determined
based on mitotic preparations from the spleen. The G-banding technique (Seabright 1971) was used to identify the specific chromosomal arms according to generally accepted
nomenclature for S. araneus chromosomes (Searle et al.
1991). Meiotic preparations were made according to the Evans et al. (1964) method, with prolonged exposure to colcemid
(Fedyk et al. 2005). Arm combinations of the variable part
of the karyotype and race affiliation are provided in Tables
1 and 2.
Non-disjunction analysis
S. araneus is characterized by very high between-individual variability in the number of chromosomes (2N),
whereas the number of chromosomal arms is constant
(NF = 40). It is expected that at meiotic metaphase II (MII)
the number of arms will be reduced to NF = 20 (modal,
euploid number; Fig. 1 a-e), while non-disjunction of chromosomes should lead to formation in even proportions of
hypomodal (NF < 20) and hypermodal (NF > 20) MII cells
(Fig. 1 f-l). In order to select an appropriate method for estimation of non-disjunction in the initial stages of microscopic examination we scored all MII cells (range NF =
17–23). Pooled results of this preliminary analysis are included in Table 3 (part of this material was excluded from
final analyses because the number of analyzed MII cells
was less than 100 per specimen). The ratio of hypoploid to
hyperploid cells equaled 531/113 = 4.7, which suggested
that the majority of hypomodal spreads represented artifacts caused by damage of MII cells during preparation.
Also, the values of NF = 19, which were almost two times
higher than NF = 21, must have been a result of artifactual
losses of chromosomes. Therefore, it is obvious that inclu-
Non-disjunction in hybrids of common shrew
3
Table 1. Incidence of non-disjunction in homozygous common shrews of different races. Abbreviations of
race names: Po – Popielno, Gu – Guzowy M³yn, Bi – Bia³owie¿a.
No. of shrew
2N
Race
Variable part
of karyotype
Counts
of hyperploid
MII cells
Total
of scored
MII cells
Nondisjunction
(%)
3933
4181
4195
4299
4171
4294
4479
25
25
25
25
23
23
23
Po
Po
Po
Po
Gu
Gu
Bi
jl,ki,gr,mn,h,o,p,q
jl,ki,gr,mn,h,o,p,q
jl,ki,gr,mn,h,o,p,q
jl,ki,gr,mn,h,o,p,q
jl,hi,ko,gr,mn,p,q
jl,hi,ko,gr,mn,p,q
jl,ki,hn,gr,mp,o,q
3
2
1
0
1
3
2
145
248
250
160
129
153
178
4.05
1.60
0.80
0
1.54
3.85
2.22
12
1263
2.01 ± 1.50
1.88
Average ± SD
Pooled values
Table 2. Non-disjunction frequencies in chain IV-forming (A) and chain V-forming (B) complex Rb heterozygotes of the common shrew. Abbreviations of race names: Po – Popielno, Gu – Guzowy M³yn, £g –
£êgucki M³yn, Bi – Bia³owie¿a, Dn – Drnholec.
No. of shrew
2N
Type of
hybrids
Variable part of karyotypes
Counts of
hyperploid
MII cells
Total of
scored
MII cells
Nondisjunction
(%)
A
25
25
25
25
25
25
25
Po/Gu
Po/Gu
Po/£g
Po/£g
Po/£g
Po/£g
Po/Bi
jl,h/hi/ik/k,gr,mn,o,p,q
jl,h/hi/ik/k,gr,mn,o,p,q
jl,h/hk/ki/i,gr,mn,o,p,q
jl,h/hk/ki/i,gr,mn,o,p,q
jl,h/hk/ki/i,gr,mn,o,p,q
jl,h/hk/ki/i,gr,mn,o,p,q
jl,ik,gr,n/nm/mp/p,h,o,q
7
3
7
5
5
3
3
193
144
263
355
251
211
142
7.00
4.08
5.18
2.78
3.91
2.80
4.14
Average ± SD
Pooled values
33
1559
4.27 ± 1.46
4.15
jl,o/ok/ki/ih/h,gr,mn,p,q
jl,o/ok/ki/ih/h,gr,mn,p,q
jl,o/ok/ki/ih/h,gr,mn,p,q
jl,o/ok/ki/ih/h,gr,mn,p,q
jl,o/ok/ki/ih/h,gr,mn,p,q
jl,o/ok/ki/ih/h,gr,mn,p,q
jl,o/ok/ki/ih/h,gr,mn,p,q
jl,o/ok/ki/ih/h,gr,mn,p,q
jl,o/ok/kh/hi/i,gr,mn,p,q
jl,o/ok/kh/hi/i,gr,mn,p,q
jl,o/ok/kh/hi/i,gr,mn,p,q
jl,o/ok/kh/hi/i,gr,mn,p,q
jl,o/oi/ik/kh/h,gr,mn,p,q
jl,hi,ko,g/gm/mn/nr/r,p,q
3
9
4
7
7
8
6
4
1
7
15
5
5
12
147
349
224
137
225
357
194
242
284
157
272
157
159
344
4.00
5.03
3.51
9.72
6.03
4.64
6.00
3.25
0.70
8.54
10.45
6.17
6.10
6.74
Average ± SD
Pooled values
93
3228
5.78 ± 2.61
5.60
B
4295
4296
4489
4500
4501
4518
4385
3932
3934
4184
4292
4293
4297
4400
4503
4244
3930
3929
4502
4291
4188
24
24
24
24
24
24
24
24
24
24
24
24
24
24
Po/Gu
Po/Gu
Po/Gu
Po/Gu
Po/Gu
Po/Gu
Po/Gu
Po/Gu
£g/Gu
£g/Gu
£g/Gu
£g/Gu
£g/Po
Dn/Gu
4
S. Fedyk and W. Chêtnicki
a
b
c
d
e
f
g
h
i
j
k
l
Fig. 1. Normal (euploid) MII spreads (NF = 20) with 11 (a), 12 (b-d), and 13 (e) chromosomes. Hyperploid MII cells: f – with
one metacentric extra (n = 12, NF = 22); g – with two acrocentrics extra (n = 15, NF = 22); h – with one acrocentric chromosome extra (n = 12, NF = 21); i-k – with single acrocentric chromosome extra (n = 13, NF = 21); l – with two Y2 chromosomes
(n = 15, NF = 21).
Table 3. Comparison of two methods of non-disjunction estimates.
Arm counts
The bases of non-disjunction estimates
< 19
19
20
21
> 21
Hypo- and Hypermodal cells
2 ´ Hypermodal cells
361
170
4587
89
25
(170 + 89) ´ 100
= 5.34%
4846
2 ´ 89 ´ 100
= 374
. %
4765
(531 + 113) ´ 100
= 12.31%
5231
2 ´ 113 ´ 100
= 47
. %
4813
531
113
sion of counts of both hypoploid and hyperploid spreads
would generate overestimated non-disjunction frequencies
(Table 3). For this reason equation “2 ´ hypermodal cells/
sum of scored cells” prevailed in the earlier studies. However, one should take into account that this formula leads to
underestimation of non-disjunction frequency because the
denominator is saddled with an excess amount of hypomodal
cells. In the present study the percentage of non-disjunction
was calculated based on equation which equalizes proportion of hypo- and hyperploid cells:
2 ´ hyperploid cells ´ 100/sum of modal
and 2 ´ hyperploid cells.
Results
In general, the study demonstrated very high
individual variability of non-disjunction frequency
in all three karyological categories of shrews. In
seven homozygous males, the non-disjunction
frequency ranged from 0 to 4.05% (mean 2.01 ±
1.50%), with an overall value of 1.88% based on
pooled counts (Table 1). Differences between the
shrews with 2N = 23 and 2N = 25 were not signif2
icant (c = 0.97, df = 1, p > 0.3).
In hybrids, the frequency of non-disjunction
was distinctly higher. In complex CIV heterozygotes, the level of non-disjunction ranged from
2.78 to 7.00% (mean 4.27 ± 1.46%), with 4.15%
overall, based on pooled counts. The highest between-individual variation, from 0.70 to 10.45%
(mean 5.78 ± 2.61%), were found in CV heterozygotes with an overall non-disjunction frequency
of 5.60%, based on pooled counts (Table 2). These
Non-disjunction in hybrids of common shrew
5
Table 4. Counts of aneuploid MII cells. Abbreviations: NF – number of chromosome arms, Hna – haploid number of chromosome arms, loss (–) or addition (+) of acrocentric (a) or metacentric (m) chromosomes.
NF 20
NF 21
NF 22
NF 23
Karyotypic status
Totals
Hna-1m+2a
Hna+1a
Hna+1m-1a
Hna+2a
Hna+1m
Hna+2m-1a
Homozygotes
CIV complex heterozygotes
CV complex heterozygotes
0
1
0
10
19
75
0
3
1
1
2
1
1
7
16
0
1
0
12
33
93
Totals
1
104
4
4
24
1
138
two types of complex heterozygotes formed a ho2
mogeneous group (c = 2.40, df = 1, 0.10 > p >
0.05), but differed significantly from homozy2
gous shrews (c = 12.67, df = 1, p < 0.01).
We found 138 hyperploid spreads out of the
total 6050 analyzed MII cells. The vast majority
of these spreads had one extra acrocentric
(75.4%) or metacentric (17.4%) chromosome (see
Fig. 1). Two additional acrocentrics (Fig. 1g)
were found only on four spreads. The remaining
6% of hyperploid cells represented more complex
cases – these were combinations of lost and extra chromosomes (Table 4).
Discussion
Previous technique of meiotic chromosome
preparation (Evans et al. 1964) did not provide
large samples of MII cells from individual shrews
(Fedyk 1980, Searle 1986a, Mercer et al. 1991,
1992, Banaszek et al. 2002, Jadwiszczak and
Banaszek 2006). Obtaining representative sample sizes of more than 300 MII cells suitable for
analysis from a single shrew proved to be possible due to a prolonged period of exposure to
colcemid (Fedyk et al. 2005, Fedyk and Chêtnicki
2007 and present study). This approach revealed
that S. araneus is characterized by high individual variability. In simple (CIII) Rb heterozygotes (n = 12), the frequency of non-disjunction
ranges from 1.2 to 7.4% (Fedyk and Chêtnicki
2007). The present study confirmed also high individual variability in complex heterozygotes,
particularly in CV heterozygotes (Table 2), as
well as in homozygous shrews (Table 1), though
to a lesser extent.
The existence of high variability between individual shrews was not surprising. According
to a study by Gropp and Winking (1981) based
on large sample sizes (200–300 MII cells per
specimen), the level of non-disjunction in 16 simple Rb heterozygotes of the house mouse ranged
between 2 and 28%. High individual variability
was also found in other mammal species (Ovis
aries, Bos taurus, Akodon molinae) (cf Searle
1988).
Meiotic abnormalities reduce fertility; therefore, it was assumed a priori that there exists a
simple relationship between the fitness of S.
araneus hybrids and the lengths of meiotic complexes. Indirect proof confirming this assumption can be drawn by comparing widths of clines
of metacentrics in hybrid zones of different chromosomal races. The widths of clines should
be inversely proportional to selection pressure
against the hybrids (Barton and Hewitt 1985).
For instance, in the contact zone between the
Drnholec and Ulm races, where hybrids form
meiotic trivalents, cline widths have been recorded as 36–44 km (Lukáèová et al. 1994). In
contrast for the contact zone between Drnholec
and £êgucki M³yn races, standardized widths of
clines of metacentrics forming a C1 meiotic complex, that is a ring-of-four (RIV) configuration,
were 15.9–16.0 km and clines of metacentrics
forming C2 meiotic complex (CV and CIV configurations) were only 7.5–7.7 km (Fedyk 1995). In
such a situation, one can expect that, under the
pressure of selection, a modification lowering
6
S. Fedyk and W. Chêtnicki
the chance of formation of meiotic complexes
longer than trivalents should appear in the hybrid zone. Two such modifications have been described. (1) In the Drnholec/£êgucki M³yn hybrid
zone where hybrids formed two independently
segregating meiotic complexes (C 1 and C 2 ),
shifts in position of clines caused the rising of
the frequency peak of recombinants (homozygous shrews or, at most, simple Rb heterozygotes) in the contact zone centre, at the cost of
hybrids forming both meiotic complexes (C1 +
C2). Hybrids with single meiotic complexes were
recorded on both sides of this recombinant peak
(Fedyk et al. 1991, Fedyk 1995). (2) Much more
common is a modification known as an acrocentric
peak, where the opposing clines of race-diagnostic
metacentrics cross at a frequency lower than 0.5
(Searle 1986, Fedyk 1986). In consequence the
chance of formation of the complex heterozygotes lowers proportionally to the magnitude of
the acrocentric peak.
Can these post-hybridization modifications
really arise under selection pressure? A model
based on empirical data collected in the hybrid
zone of the Oxford and Hermitage races provided theoretical premises confirming this possibility (Hatfield et al. 1992). This model assumed
that the fitness of simple Rb heterozygotes was
reduced to 0.02, and that of complex heterozygotes, to 0.20. Computer simulations confirmed
that with these differences in selection pressures against the heterozygotes, the occurrence
of an acrocentric peak, as observed by Searle
(1986) in the contact zone near Oxford, was possible. Our research showed no difference between complex heterozygotes CIV and CV, and
furthermore, the level of non-disjunction in simple Rb heterozygotes, that form CIII meiotic configuration (Fedyk and Chêtnicki 2007), was even
slightly higher than in CIV heterozygotes and
varied insignificantly from both CIV and CV
(Fig. 2). Therefore, the differences in fitness between simple and complex heterozygotes assumed in the Hatfield et al. (1992) model cannot
readily be attributed to the reduction in fertility
associated with non-disjunction in males, on the
8
B
7
B
Non-disjunction (%)
6
B
5
4
A
3
2
F = 5.25
p = 0.0042
1
0
CIII
Homozygotes
CIV
CV
Heterozygotes
Fig. 2. Single factor ANOVA of level of non-disjunction in homozygotes, simple Rb heterozygotes (according to data by Fedyk
and Chêtnicki 2007) and two kinds of complex heterozygotes. Karyological categories designated by different letters (A, B) are
statistically significant at p < 0.05.
Non-disjunction in hybrids of common shrew
basis of our data. Further studies are needed to
investigate the whole range of factors that influence fitness of Rb heterozygotes, including nondisjunction in females (which is expected to be
higher than in males; Searle 1993) and frequency of sterility due to germ cell death. Only
then will it be possible to fully assess the Hatfield et al. (1992) model.
Acknowledgements: We are grateful to Professors P. Borodin,
J. Zima, and J. B. Searle for valuable comments and improving English. The study was supported by Polish State
Committee for Scientific research within the Project No.
3PO4C 058 23.
References
Averianov A. O. (ed) 2007. Proceedings of the ISACC’s
Seventh International Meeting St. Petersburg, Russia
August 28 – September 1, 2005. Russian Journal of
Theriology 6: 1–122.
Banaszek A., Fedyk S., Sza³aj K. A and Chêtnicki W. 2000.
Reproductive performance in two hybrid zones between
chromosome races of the common shrew Sorex araneus
in Poland. Acta Theriologica 45, Suppl. 1: 69–78.
Banaszek A., Fedyk S., Fiedorczuk U., Sza³aj K. A. and
Chêtnicki W. 2002. Meiotic studies of male common
shrews (Sorex araneus L.) from a hybrid zone between
chromosome races. Cytogenetic and Genome Research
96: 40–44. doi: 10.1159/000063025)
Barton N. H. and Hewitt G. M. 1985. Analysis of hybrid
zones. Annual Review of Ecology, Evolution and Systematics 16: 113–148. doi: 10.1146/annurev.es.16.110185.
000553
Evans E. P., Breckon G. and Ford C. E. 1964. An air – drying method for meiotic preparations from mammalian
testes. Cytogenetics 3: 289–294. doi: 10.1159/000129818
Fedyk S. 1980. Chromosome polymorphism in a population
of Sorex araneus L. at Bia³owie¿a. Folia Biologica (Kraków) 28: 83–120.
Fedyk S. 1986. Genetic differentiation of Polish populations
of Sorex araneus L. II. Possibilities of gene flow between
chromosome races. Bulletin of Polish Academy of Sciences. Biological Science 34: 161–171.
Fedyk S. 1995. Regional differentiation and hybrid zones
between chromosomal races of Sorex araneus L. in
north-eastern Poland. Dissertations Universitatis Varsoviensis 439: 1–125. Bia³ystok. [In Polish]
Fedyk S., Bajkowska U. and Chêtnicki W. 2005. Sex chromosome meiotic drive in hybrid males of the Common
Shrew (Sorex araneus). Folia Biologica (Kraków) 53:
133–141.
Fedyk S. and Chêtnicki W. 2007. Preferential segregation of
metacentric chromosomes in simple Robertsonian heterozygotes of Sorex araneus. Heredity 99: 545–552. doi:
10.1038/sj.hdy.6801036
7
Fedyk S., Chêtnicki W. and Banaszek A. 1991. Genetic differentiation of Polish populations of Sorex araneus L.
III. Interchromosomal recombination in a hybrid zone.
Evolution 45: 1384–1392.
Fedyk S., Wójcik J. M., Chêtnicki W. and M¹czewski S.
2008. Invalidation of Stobnica chromosome race of the
common shrew Sorex araneus. Acta Theriologica 53:
375–380.
Fredga K. and Narain Y. 2000. The complex hybrid zone between the Abisko and Sidensjö chromosome races of
Sorex araneus in Sweden. Biological Journal of the Linnean Society 70: 285–307. doi: 10.1111/j.1095-8312.
2000.tb00211
Garagna S., Zuccotti M., Searle J. B., Redi C. A. and
Wilkinson P. J. 1989. Spermatogenesis in heterozygotes
for Robertsonian chromosomal rearrangements from
natural populations of the common shrew, Sorex araneus. Journal of Reproduction and Fertility 87: 431–438.
doi: 10.1530/jrf.0.0870431
Gropp A. and Winking H. 1981. Robertsonian translocations:
cytology, meiosis, segregation patterns and biological consequences of heterozygosity. Symposia of the Zoological
Society of London 47: 141–181.
Hatfield T., Barton N. and Searle J. B. 1992. A model of a
hybrid zone between two chromosomal races of the common shrew (Sorex araneus). Evolution 46: 1129–1145.
Jadwiszczak K. A. and Banaszek A. 2006. Fertility in the
male common shrews, Sorex araneus, from the extremely narrow hybrid zone between chromosome races.
Mammalian Biology 71: 257–267. doi: 10.1016/j.mambio.
2006. 02.004.
Lukáèová L., Piálek J. and Zima J. 1994. A hybrid zone between the Ulm and Drnholec karyotypic races of Sorex
araneus in the Czech Republic. Folia Zoologica 43,
Suppl. 1: 37–42.
Mercer S. J., Searle J. B. and Wallace B. M. N. 1991 Meiotic
studies of karyotypically homozygous and heterozygous
male common shrews. Mémoires de Société Vaudoise
des Sciences Naturelles 19: 33–43.
Mercer S. J., Wallace B. M. N. and Searle J. B. 1992. Male
common shrews (Sorex araneus) with long meiotic chain
configurations can be fertile: implications for chromosomal models of speciation. Cytogenetics and Cell Genetics 60: 68–73. doi: 10.1159/000133298
Narain Y. and Fredga K. 1996. A hybrid zone between the
Hällefors and Uppsala chromosome races of Sorex araneus in central Sweden. Hereditas 125: 137–145. doi:
10.1111/j.1601-5223.1996.00137
Narain Y. and Fredga K. 1997. Meiosis and fertility in common shrews, Sorex araneus, from a chromosomal hybrid
zone in central Sweden. Cytogenetics and Cell Genetics
78: 253–259. doi: 10.1159/000134668
Seabright M. 1971. A rapid banding technique for human
chromosomes. Lancet 2: 971–972.
Searle J. B. 1986. Factors responsible for a karyotypic polymorphism in the common shrew, Sorex araneus. Proceedings of the Royal Society of London B 229: 277–298.
Searle J. B. 1986a. Meiotic studies of Robertsonian heterozygotes from natural populations of the common shrew,
8
S. Fedyk and W. Chêtnicki
Sorex araneus L. Cytogenetics and Cell Genetics 41:
154–162. doi: 10.1159/000132220
Searle J. B. 1988. Selection and Robertsonian variation in
nature: the case of the common shrew. [In: The cytogenetics of mammalian autosomal rearrangements. A.
Daniel, ed]. Alan Liss, New York: 507–531.
Searle J. B. 1990. A cytogenetical analysis of reproduction
in common shrews (Sorex araneus) from a karyotypic
hybrid zone. Hereditas 113: 121–132. doi: 10.1111/j.
1601-5223.1990.tb00075.
Searle J. B. 1993. Chromosomal hybrid zones in eutherian
mammals. [In: Hybrid zones and the evolutionary process. R. G. Harrison, ed]. Oxford University Press, New
York, Oxford: 309–353.
Searle J. B., Fedyk S., Fredga K., Hausser J. and Volobouev
V. T. 1991. Nomenclature for the chromosomes of the
common shrew (Sorex araneus). Mémoires de Société
Vaudoise des Sciences Naturelles 19: 13–22.
Searle J. B. and Wójcik J. M. (1998). Chromosomal evolution: The case of Sorex araneus. [In: Evolution of shrew.
J. M. Wójcik and M. Wolsan, eds]. Mammal Research
Institute, PAS, Bia³owie¿a: 221–268.
Wójcik J. M., Borodin P. M., Fedyk S., Fredga K., Hausser
J., Mishta A., Orlov V. N., Searle J. B., Volobouev V. T.
and Zima J. 2003. The list of the chromosome races of
the common shrew Sorex araneus (updated 2002).
Mammalia 68: 169–178.
Received 28 June 2009, accepted 8 September 2009.
Associate editor was Andrzej Zalewski.