chromosomal evolution in the rodent family gerbillidae
TRANSCRIPT
CHROMOSOMAL EVOLUTION IN THE
RODENT FAMILY GERBILLIDAE
by
MAZIN BUTROS HANNA QUMSIYEH, B.S., M.S
A DISSERTATION
IN
ZOOLOGY
Submitted to the Graduate Faculty of Texas Tech University in
Partial Fulfillment of the Requirements for
the Degree of
DOCTOR OF PHILOSOPHY
May, 1986
^0/
1906^ r'^* v^^ ACKNOWLEDGMENTS
I am deeply indebted to Professor Robert J. Baker for
his continued support, help, and advice during my graduate
career. Thanks are due to members of my advisory
committee Drs. Robert J. Baker, Ronald K. Chesser, Ray C.
Jackson, Clyde Jones, and J. Knox Jones, Jr., for their
critical comments and advice, which helped bring this work
to completion. For their advice and friendship, I thank
fellow students, especially: Mike W. Haiduk, Craig S.
Hood, Fred B. Stangl, Jr., Robert R. Hollander, David A.
McCullough, and Cindy G. Dunn. Specimens from South
Africa and Namibia were collected by Duane A. Schlitter,
C. G. Coetzee, and I. L. Rautenbach, to whom I am greatly
appreciative. I am also greatly indebted to my wife and
family for their support, help, and patience during my
graduate career. The field trip to Jordan was supported
by the Museum Support Fund of Texas Tech University.
Laboratory work was supported by a Grant-in-Aid of
Research from the American Society of Mammalogists and by
NSF grant DEB-83-000934 to R. J. Baker.
11
TABLE OF CONTENTS
ACKNOWLEDGMENTS ii
LIST OF TABLES iv
LIST OF FIGURES v
CHAPTER
I. INTRODUCTION 1
II. METHODS AND MATERIALS 8
III. RESULTS 15
IV. DISCUSSION 45
Chromosomal Evolution 45
Systematic Implications 65
Modes of Chromosomal Evolution in Gerbillidae 71
LIST OF REFERENCES 8^
APPENDICES
A. Karyotypic Data for Gerbillidae 99
B. Specimens Examined 108
111
LIST OF TABLES
TABLE PAGE
1. Character states for chromosomes of the Gerbillidae examined and of the outgroups 41
2. Interpretations of chromosomal events for the different character states as listed in Table 1 43
3. Corresponding linkage groups between Peromyscus and the Gerbillidae 83
IV
LIST OF FIGURES
FIGURE PAGE
1. G-banded karyotype of Tatera leucogastor . . . . 13
2. Example of chromosomal character states and
their coding 14
3. G-banded chromosomes of Gerbillurus paeba. . . . 22
4. Intraspecific chromosomal variation in Gerbillurus paeba 23
5. The three types of heterochromatic additions in
Gerbillurus paeba 24
6. G-banded chromosomes of Gerbillurus vallinus . . 25
7. Comparison of haploid complements of Tatera leucogastor, T. brantsii, and T. afra 26
8. G-banded karyotype of a female Desmodillus auricularis 27
9. Some of the homologous elements between (left to right): Desmodillus auricularis, Tatera leucogastor, Gerbillurus paeba, and G. vallinus . . 28
10. C-banded chromosomal complements of Tatera afra (top), Gerbillurus vallinus (middle), and Desmodillus auricularis 29
11. G-banded chromosomes of Psammomys obesus. . . . 30
12. C-banded chromosomes of Psammomys obesus. . . . 31
13. G-banded chromosomes of Sekeetamys calurus. . . 32
14. G-banded chromosomes of Meriones unguiculatus . 33
15. C-banded karyotypes of two Meriones species 34
V
16. Presumed homologous elements between Desmodillus auricularis, Psammomys obesus, Meriones shawi, and M. unguiculatus (Teft to right). T". . . . 35
17. G-banded chromosomes of Meriones crassus. . . . 36
18. G-banded chromosomes of Gerbillus dasyurus. . . 37
19. Presumed homologous elements between two Meriones and two Gerbillus species 38
20. Comparison of chromosomes of Gerbillidae with the outgroups 39
21. Interspecific variation in sex chromosomes of the Gerbillidae 40
22. Character states and tree stems for the
Gerbillidae and the outgroups 77
23. Tree for the Tatera/Gerbillurus group 78
24. The most parsimonious tree for the Meriones group 79
25. Tree for the two Gerbillus species examined 80
26. Histogram to illustrate distribution of diploid numbers in the family Gerbillidae 81
27. Tree for the Tatera/Gerbillurus group to illustrate change in diploid numbers by fissions and fusions 82
VI
CHAPTER I
INTRODUCTION
Data from G- and C-band chromosomes have been
utilized in deducing phylogenies of various groups of
mammals using cladistic methodology: cricetine rodents
(Baker et al., 1983; Koop et al., 1985; Robbins and Baker,
1981; Stangl and Baker, 1984; Yates et al., 1979),
phyllostomid bats (Baker et al., 1979; Bass and Baker,
1979; Haiduk and Baker, 1982), vespertilionid bats
(Bickham, 1979); Megachiroptera (Haiduk et al., 1981).
These data on mammals as well as data from other groups of
animals—for example, turtles, (Bickham and Baker, 1976)
and morabine grasshoppers, (White, 1968)--also provided
critical tests as well as data for hypothesis concerning
the role of chromosomal evolution in speciation (Matthey,
1978; White, 1979; Baker and Bickham, 1980; Bickham and
Baker, 1979). Such data are also useful in recognizing
sympatric, cryptic species of mammals (Baker, 1984) and in
differentiating between morphologically similar species
(Qumsiyeh and Baker, 1985).
The rodent family Gerbillidae contains about 86
species in 14 genera (Corbet and Hill, 1980; Honacki et
al., 1982).
The Gerbillidae represent a morphologically well-
defined assemblage of muroid rodents. However, their
relationships to other groups within the Muroidea have
been debated. The various hypotheses that have been
postulated are as follow:
1. Gerbillinae is a subfamily of Cricetidae equal in
rank to Microtinae and Cricetinae and exclusive of the
family Muridae (Miller and Gidley, 1918; Simpson, 1945;
Corbet, 1978).
2. The Gerbillinae is a subfamily of the family
Muridae (sensu lato, which also includes Cricetinae,
Microtinae, and Murinae (Ellerman, 1941).
3. The Gerbillidae is a well-defined family equal in
rank to the Muridae and Cricetidae within the superfamily
Muroidea (Chaline et al., 1977).
The most recent re-evaluation of the superfamily
Muroidea was that of Carleton and Musser (1984), who
concluded that the subfamilial relationships and the
taxonomy of this group of rodents are still unresolved,
and that it is better to treat each group as an equal
family or subfamily within the Muroidea. These authors
used subfamilial names without any recognition of family
status. In this paper, I follow Chaline et al. (1977) in
using the name Gerbillidae for this group of rodents. This
seems to be the best arrangement until new data sets are
available to determine relationships of the various
assemblages of muroid rodents (Carleton and Musser, 1984).
If the gerbils are a monophyletic and well-defined
group of muroid rodents, then we must determine if there
are major subdivisions within that assemblage. Earlier
workers (for example, Ellerman, 1941) did not use any
supergeneric classification for the gerbils. Chaline et
al. (1977) were the first to recognize a subfamilial
division within the group. The two subfamilies recognized
by these authors are the Taterillinae (Tatera, Taterillus,
and Gerbillurus) and Gerbillinae (all other genera).
Pavlinov (1982) recognized three subdivisions of gerbils
to which he gave the rank of tribes: Taterillini and
Gerbillini, which correspond to the two subfamilies of
Chaline et al. (1977), and the tribe Ammodillini to
include only Ammodillus imbelis. Pavlinov (1982)
suggested that the Ammodillini is a primitive group with
few unique morphological features (absence of a coronoid
process on the lower jaw and convergence of upper
toothrows, for example). The tribe Gerbillini of Pavlinov
(1982) (subfamily Gerbillinae of Chaline et al., 1977) has
the following morphological advances: completely or almost
completely pneumatized auditory drum, rhomboid type of
molars, and internal mastoid septum of auditory drum
(Pavlinov, 1982). The tribe Taterillini is characterized
by modification the anteroconulid of Ml, enlargement of
the masseteric area of the upper jaw, and a lophodont
tooth crown. Thus, most recent workers (Chaline et al.,
1977; Pavlinov, 1982) agree on at least the distinctive
nature of the Taterillinae and Gerbillinae.
Karyotypic data from nondifferentially stained
chromosomes reported in the literature (Appendix A)
illustrate diploid numbers for gerbils ranging from 18 in
Ammodillus imbellis to 74 in Gerbillus dunni and G.
latasti. Chromosomal variation in Gerbillidae also
includes variations in sex determining mechanisms and the
structure of the X-chromsome (Wahrman and Zahavi, 1955;
Zahavi and Wahrman, 1957; Wassif et al., 1969; Wassif,
1977, 1981; Wahrman et al., 1983).
In France, studies on gerbil chromosomes have
utilized C- and R-banding techniques (Benazzou et al.,
1982a, 1982b, 1984). These papers document the large
amount of variation observed in gerbil chromosomes.
However, four shortcomings to these studies make it
difficult to utilize them in either a taxonomic or an
evolutionary cytogenetic context. First, no outgroups were
used, thus resulting in primitive and derived conditions
that were not tested scientifically (see Discussion).
When characters were used as synapomorphies (shared
derived conditions), it was assumed that the most common
condition was primitive. This is, however, not
necessarily true as I will argue later (fission results).
Second, no standard numbering system was utilized even
though each species was compared to the chromosomes of
Meriones tristrami. Each of the species examined was
given its own numbering system. Third, in figures of
karyotypes, different species were not compared on a
side-by-side basis. Fourth, only one or two specimens of
each species were examined and, as such, no individual
variation was observed.
Other works that have utilized differentially stained
chromosomes include G- and C-band studies by Wassif (1977,
1981). Her work was the first to examine G-banded sex
chromosomes in gerbils and to comment on the evolution of
a sex chromosome complex. It was, however, limited to
eight members of the hairy-footed gerbils,
(Dipodillus-Gerbillus), including Gerbillus calurus
(=Sekeetamys calurus). As will be discussed later, the
latter species is not a member of that group but is more
closely related, both chromosomally and morphologically,
to members of the genus Meriones. Gamperl and Vistorin
(1980) recorded homology of 11 chromosomal arms of
Meriones unguiculatus with those of Gerbillus campestris.
Studies using synaptonemal complex analysis were performed
on inversions in chromosomes of Psammomys obesus (Ashley
et al., 1981; Solary and Ashley, 1977) and on sex
chromosomes of Gerbillus (Wahrman et al., 1983).
The objectives of this study were to: 1. Assess
intraspecific variation in G- and C-band patterns from
series of specimens. Characterizing intraspecific
variation has been neglected in previous studies based on
one or few species. Intraspecific variation can be
significant in understanding the dynamics involved in
chromosomal evolution (Baker et al., 1981); 2. Use G-band
sequences to infer the nature and direction of chromosomal
evolution of Gerbillidae by the use of cladistic
methodology. 3. Further use this information in deducing
a phylogenetic tree for Gerbillidae and compare it with
hypotheses based on morphological data sets. The
limitations and benefits of such an analysis were
discussed by Baker et al. (1983).
Taxonomic problems to be specifically addressed with
this study include: 1) the position of the monotypic genus
Sekeetamys (variously allied with Gerbillus or Meriones);
2) the position of the genus Psammomys and its
relationship to Meriones; 3) the validity of the tribe
Taterillini (Tatera and Gerbillurus); and 4) the position
of Desmodillus (allied either with Taterillini or
Gerbillini).
In addition to the taxonomic problems that can be
solved with G- and C-band data, questions concerning the
direction of chromsomal change in mammals in general (e.g.,
fissions versus fusions) can be evaluated. The group
chosen for analysis contains both high and low diploid
numbers. For many authors it is tempting to postulate a
pattern of either decreasing (Benirschke et al., 1965;
Grobb and Winking, 1972; Gustavson and Sundt, 1969;
Jotterand, 1972) or increasing (Hansen, 1975; Kato et al.,
1973; Imai and Crozier, 1980) diploid numbers during the
course of chromosomal evolution. However, conclusions
concerning chromosomal homology, primitive and derived
conditions, and the direction of evolution should be drawn
only after chromosomes are identified (e.g., by banding)
and traced back in evolutionary history across members of
an evolutionary line and outgroups for that group.
Primitive conditions must be determined by outgroup
methods before any assesment of changes in character
states is attempted.
CHAPTER II
METHODS AND MATERIALS
Specimens were collected from natural populations
using Sherman live traps baited with oatmeal. This is
true of all specimens listed in Appendix B with the
exception of Meriones unguiculatus (Mongolian Jird,
domestic animal) and Sekeetamys calurus (raised in
captivity but parents collected in the field). Lung
biopsies were taken from these two species and primary
fibroblast cultures initiated following the techniques of
Baker and Qumsiyeh (1985). All other animals, a total of
95, were karyotyped by the yeast stress method of Lee and
Elder (1980). Voucher specimens were prepared as museum
skins and skulls (or skeletons) and deposited in the
following institutions: Carnegie Museum, Natural History
(CM), The Museum, Texas Tech University (TTU), and Jordan
University Museum of Natural History (JU). The specimens
examined are listed by species and locality in Appendix B.
G-bands were obtained by the method of Seabright
(1971) as modified by Baker et al. (1982) and Baker and
Qumsiyeh (1985). C-bands were obtained by the method of
Stefos and Arrighi (1971) as modified by Baker and
Qumsiyeh (1985). Medium or large species of gerbils
(e.g., Tatera, Desmodillus, and Psammomys) had bone marrow
that was high in fat content and the cells tended to clump
8
together after hypotonic treatment and show little
spreading of mitotic chromosomes. To alleviate this
problem, cells in the hypotonic solution were incubated
for 27 minutes (instead of 25) with frequent but gentle
mixing. After the hypotonic treatment, a few drops of
fixative solution (three parts absolute methanol to one
part glacial acetic acid) were added to the bottom of the
tube before centrifugation. The remainder of the
procedure and all other procedures were as described in
Baker and Qumsiyeh (1985).
Banded chromosomal spreads were photographed and the
photographs cut and matched. A minimum of five spreads
were counted, a minimum of three of these G-banded were
cut and matched first to each other and then to other
members of the same species. Only when chromosomes of each
species were matched and their morphology well known were
interspecific comparisons made. Each figure was
constructed using chromosomes from a single spread. This
was done to reduce possible errors in recognizing the
small chromosomal elements. Similarly, the comparison
figures were made using haploid complements from one
spread for each species. The numbers in the comparison
figures indicate homologous elements relative to those for
Tatera leucogastor but do not indicate identity of
character states.
10
The karyotype of T. leucogastor (Fig. 1) was chosen
for a numbering system for all gerbils examined because
all arms are easilly differentiated (with the possible
exception of 27/28 discussed later), heterochromatin is
restricted to the centromeres on all autosomes, and the
quality of bands obtained on this species is better than
on others (Fig. 1).
Once all species of gerbils available were compared,
outgroups were examined to determine the direction of
chromosomal change (primitive and derived states). To do
this, an examination of outgroups was critical.
Peromyscus boyli i was chosen as an outgroup because it has
a primitive karyotype for the New World Cricetidae that
has been extensively studied chromosomally (Robbins and
Baker, 1981, Stangl and Baker, 1984; Rogers et al., 1984).
Rattus surifer also was used as an outgroup because it has
a primitive karyotype for the family Muridae (Hollander
and Baker, pers. comm.). The karyotype of this animal is
used with permission of R. R. Hollander and R. J. Baker.
To analyse the chromosomal data cladistically, each
chromosome or part thereof that is conserved and is
recognizable in the species studied by G-banding, was
considered a character and its various conditions,
representing rearrangements, were considered as character
states. An example is shown in Fig. 2. The linkage group
11
in this figure occurs in the primitive condition (state 1)
in both outgroups and several ingroup taxa (Table 1).
Fusions with linkage groups 1 and 31 produces states 3 and
4 respectively. A paracentric inversion produces
character state 2 and a pericentric inversion state 5.
State 5 gives rise to state 6 by centric fission (all taxa
that have state 6 also have the remaining arm, 2
proximal). Fusion of 2 distal (state 6) to linkage groups
1, 32, and 3 produces character states 7, 8, and 9,
respectively.
Character states were coded binomially by the method
of Sokal and Sneath (1963) as further developed by Kluge
and Farris (1969). To obtain the most parsimonious tree
or trees for the species, the method of Farris (1970,
1978) was used. Coded data for each species were entered
into the program in different orders until a consistent
tree with the least number of steps was obtained.
Abbreviations and symbols used in this work are as
follows: 1/2, linkage group 1 fused with linkage group
2; 1,2, linkage group 1 exists separate from linkage
group 2; 2i, inversion in linkage group 2; -E deletion of
a euchromatic segment; +E, addition of a euchromatic
segment; +H, addition of a heterochromatic (C-band
positive) material; to 33, a translocation to chromosome
33; 2p or 2prox, proximal part of linkage group 2; 4d or
12
4dist, distal part of linkage group 4; 1^, character state
three of linkage group 1.
13
1
2
11
ft«
I •
12
21
22
35
30
4
13
14
23
24
31
6 15
«
16
25
u 26
32
8
17
10
19
18
27
28
20
*
29
: i I 33
Figure 1. G-banded karyotype of Tatera leucogas tor . This karyotype was used to iden t i fy and number proposed homologous segments as they r e l a t e to a l l other species examined.
14
- • f - e r J - I Character v . . States 1 2 3 4 5 6 7 8 9
Character State Tree
3 | 1 I 5 ^ 6 | 8
Figure 2. Example of chromosomal character states and their coding. Stars indicate position of the centromeres and the character states refer to the various conditions of this linkage group which is termed 2d (2distal). See text for explanation. The taxa to which these chromosomes belong to are, from left to right: Gerbillus dasyurus, G. nanus, Tatera leucogastor, Gerbillurus paeba, Desmodillus auricularis, Meriones shawi, Psammomys obesus, M. unguiculatus, and Sekeetamys calurus.
CHAPTER III
RESULTS
The results of the kayotypic studies are presented in
figures 1-21. Following is a summary of the results for
each species.
The karyotype of Gerbillurus paeba (2n=36, FN=68,
Fig. 3) has all biarmed autosomes, a large submetacentric
X, and a small acrocentric Y. A polymorphic condition for
chromosome 29/32 was observed in one specimen from Cape
Province, South Africa (TK 25665), and one from
Keetmanshoop District, Namibia (TK 25654). All other
specimens from Namibia and South Africa had the normal
29/32 (Fig. 4A). Another polymorphism observed was in the
relative size of chromosome 33 (Fig. 4B).
Heterochromatin is restricted to the centromeric
region on all chromosomes except for: 1) an interstitial
band in arm 10 (stains G-negative, see Fig. 5), 2)
chromosome 27/28 is heterochomatic, and 3) telomeric
heterochromatin was found on the q arm of the X and Y
chromosomes (Fig. 5).
Gerbillurus vallinus has a 2n=60, FN=70-74 (Fig. 6).
Schlitter et al. (1985) reported a FN=74 for the standard
karyotype of this species. My sample of 5 individuals had
FNs of 70, 72, 73, and 74, which represents hetero
chromatic short arm additions to chromosomes 1 and 8
15
16
(see Figs. 6 and 10). Other than these variable short
arms and the centromeric areas, heterochromatin is also
found in a small band on chromosome 10 (not particularly
clear in Fig. 10 because the chromosomes are short). The
X and Y chromosomes are similar in G- and C-band pattern
to those of Gerbillurus paeba.
Tatera leucogastor (2n=40, FN= 66, Figs. 1, 7) was
first examined karyologically from a specimen from South
Africa (no exact locality) by Matthey (1954b), who
reported a 2n=42. Examination of 72 individuals of this
species from Namibia, Zimbabwe, and South Africa by Gordon
and Rautenbach (1980) showed that all had 2n=40. Gordon
and Rautenbach report a FN of 70, but they probably
counted the sex chromosomes. These authors also
misidentified the X and Y chromosomes (see their figure 3
and compare with Figs. 1 and 7). The X chromosome is a
large submetacentric and the Y a small submetacentric. I
examined several individuals (see specimens examined) from
Namibia and South Africa (Transvaal Province) which had
2n=40, FN=66.
The G-banded karyotype of this species (Fig. 1) was
chosen for a standard numbering system for reasons given
earlier. Tatera leucogastor differs from both T. afra and
T. brantsii in having two fusions (1/2, 7/8) and the
condition of the Y chromosome. Heterochromatin is
17
restricted to the centromeric regions, but also occurs
extensively in chromosome 25/26 and the X and Y.
The G-banded karyotype of Tatera afra (2n=44, FN=66,
Fig. 7) is similar to that of T. leucogastor with three
differences. Tatera leucogastor has fusions of
acrocentric pairs 1 and 2 and 7 and 8, and the Y
chromosome is a small acrocentric, whereas in T. afra it
is a relatively large metacentric. The heterochromatin
pattern is similar to that of T. leucogastor.
Heterochromatin is found in the centromeric region on all
autosomes but is more pronounced in the
acrocentric/telocentric elements. The X and Y chromosomes
also contain large quantities of heterochromatin (Fig.
16).
The karyotype of Tatera brantsii (2n=44, FN=66, Fig.
7) is similar to that of T. afra with only two chromosomes
being slightly different in G-band pattern (8 and Y).
The karyotype of Desmodillus auricularis (2n=52,
FN=78, Fig. 8) consists of 28 metacentric or
submetacentric autosomes and 22 acrocentric or telocentric
autosomes. The X chromosome is a large metacentric
chromosome that is not surpassed in relative size except
by that of Psammomys obesus. Similarly, the Y chromosome
(a medium sized acrocentric) shows a relative size that is
unusual for many mammals (Fig. 8). Heterochromatin is
18
restricted to the centromeric region on all chromosomes
except an interstitial band on arm q of the largest
autosome (chromosome number 8), diffused heterochromatin
on chromosome 27/28, and extensive heterochromatin on the
X.
The karyotype of Psammomys obesus (2n=48, FN=74, 75,
Fig. 11) includes 18 acrocentric and 28 biarmed autosomes.
The X chromosome is a large metacentric and the Y
chromosome is a medium-sized metacentric. The relative
sizes of the sex chromosomes in this species surpasses
those of any of the other species examined. All G-band
sequences of this species are identifiable to those of the
Tatera leucogastor standard except for the arm fused to
chromosome 31 (Fig. 11). This arm may represent an
inverted 27/28, a linkage group deleted from the analysis
because it lacks sufficient differential banding to be
positively identified. A polymorphism involving an
addition of a heterochromatic short arm to chromosome 2p
was found in one male (TK 25551, Figs. 11 and 12). Other
than this and the X and Y chromosomes, all heterochromatin
was restricted at the centromeric regions (Fig. 12).
All autosomes of Sekeetamys calurus (2n=38, FN=74,
Fig. 13) are metacentric or submetacentric except for
acrocentric pair 9. G-band sequences for this species
show many unique arm combinations (Fig. 13, Table 1).
19
Another feature is large blocks of G-band negative
material around all centromeres (Fig. 13), a feature first
noted by Wassif (1977, 1981). This material is not
heterochromatic and centromeric heterochromatin is even
less pronounced than in members of the Meriones group
(Fig. 15).
The karyotype of Meriones shawi (2n=44, FN=72, Fig.
16) has 12 acrocentric and 30 biarmed autosomes. Although
it has a nondifferentially stained karyotype similar to
that of M. unguiculatus (2n=44), the G-band sequences of
the two species show that there are many different arm
combinations (Fig. 16, Table 1). The X is a large
submetacentric identical in G-band sequences to those of
M. unguiculatus and S. calurus.
The karyotype of Meriones unguiculatus (2n=44, FN=78,
Figs. 14, 15) has 34 metacentric or submetacentrics and 10
acrocentric or telocentric chromosomes. The X is a large
metacentric. No males were examined in this study, but
the Y chromosome has been reported as a medium
submetacentric (Nadler and Lay, 1967). Heterochromatin is
restricted to the centromeric region on all chromosomes
but additionally is added to chromosome 33 (Fig. 15).
The karyotype of Meriones tristrami (2n=72, FN=
76-80, Figs. 15, 19) consists of 70 euchromatic arms with
a variable number of heterochromatic short arm additions
20
(6-10). These arms are also variable in size and in some
cases (see Fig. 15) could not be distinguished from
centromeric areas on acrocentric elements. The X
chromosome is a large submetacentric and the Y a medium
metacentric. Heterochromatin is distributed on the sex
chromosomes, in autosomal centromeric regions, and in
variable short arm additions (Fig. 15). These findings
agree with Korobitsina and Korablev (1980) for the
variability of heterochromatic short arm additions.
The karyotype of Meriones crassus (2n=60, FN= 72,
Figs. 17, 19) has six pairs of metacentric and
submetacentric autosomes and 24 pairs of acrocentric or
telocentric autosomes. The X is a large submetacentric
and the Y a medium metacentric chromosome. Hetero
chromatin is located in the centromeric regions, as two
short arm additions, and on the sex chromosomes.
The karyotype of Gerbillus dasyurus (2n=60, FN=68,
70,72, Fig. 18) has four pairs of submetacentric or
metacentric autosomes and 25 pairs of acrocentric or
telocentric autosomes. In addition to the centromeric
heterochromatin, variable short arm additions (0, 2 and 4)
occur in individuals from Jordan making 12 the maximum
number of biarmed chromosomes observed. The X chromosome
is a large metacentric and the Y a small acrocentric
element.
21
The karyotype of Gerbillus nanus (2n=52, FN= 60, Fig.
19) consists of 40 acrocentric and 10 biarmed autosomes.
The X is a large submetacentric and the Y is a small
acrocentric chromosome. Only two individuals of this rare
species were examined and the quality of the banded
karyotypes were not as good as in those of species
examined. Even though several elements could not be
identified, those linkage groups identifiable (e.g., 7, 8,
30) are identical to, or slightly modified from those of
the morphologically similar species, G. dasyurus (Fig.
19).
22
Figure 3. G-banded chromosomes of Gerbillurus paeba. Numbers in this figure and all subsequent figures refer to the standard numbers for Tatera leucogastor (Fig. 1).
23
Figure 4. Intraspecific chromosomal variation in Gerbillurus paeba. A. Inversion in the centromeric region of chromosome 29/32. B. Chromosome pair 33 normal individual on the left and an individual polymorphic for an addition on 33.
24
Figure 5. The three types of heterochromatic additions in Gerbillurus paeba. G-banded (left chromosome for each pair) and C-banded (right) selected chromosomes are shown with C-band positive material being interstitial in 9/10, diffused in 33, and telomeric in X.
25
11 15 17 21 23 ^^
M JV ^ H it II « !i 12 16 18 22 24 8
IJO!? «<i« »p r ,2' I
1 10 32 30 29 33 31 27/28
W !C > i ?l tt i> ** " 5 9 26 6 3 7 20
14 13 25 19 ^ Y
Figure 6. G-banded chromosomes of Gerbillurus vallinus.
26
11
^n K¥
10 21
12 23
Figure 7. Comparison of haploid complements of Tatera leucogastor, T. brantsii, and T. afra. The Y chromosomes from three males are shown in the lower right-hand corner.
27
2prox 13 4prox 15 17
8 29
25
2dist 14 16
19 21 27
30 26 20 22 28
>t li ii K
18
23
UH<»*<I"^' 24
Figure 8. G-banded karyotype of a female Desmodillus auricularis. Inset shows the Y. chromosome from a male.
28
."? •» r,t= iiiii* . 5
:ll ^It* ?•-•-? l i s ' ^•*«^ 19
i^ 20
12
21
22
14 16
23 27
^ 1 - 1 —
24 28
18
31
Figure 9. Some of the homologous elements between (left to right): Desmodillus auricularis, Tatera leucogastor, Gerbillurus paeba, and G. vallinus.
29
*• j» % " t . k % hll
M M h *! f* r '* -• ii ft' ti ^
X X
t)i It ft B isi s $% fk^
11 : ' l §P 11 * .u^^-.^i ? g *r-i!' f i
III ' *
'i *p n ? iH I t « » * • f ! 1^ ^
f ^ I p -I I X Y
Figure 10. C-banded chromosomal complements of Tatera afra (top), Gerbillurus vallinus (middle), and Desmodillus auricul"aris.
30
32
8 17
18
1 ^ ^rt
22
^ ^
12
1
•
2dist
• •
29
23
• " N ^
24
5
4dist
(19/20)i
^ • .
0^
miff % 0
6
7
4« 31 15
MH 16
10
Alf n
13
• * >
MM
14
9
ii 25 26
2prox
4prox
3
9%n
U9 30
^
rf^ 1« 1^ X Y
Figure 11. G-banded chromosomes of Psammomys obesus Note polymorphic condition for the smallest autosome (2prox) involving a short arm addition.
31
a If I I #? I* It n 11 *' 'I »•
• %
Vi?^. \
aCG B
t /r«
Figure 12. C-banded chromosomes of Psammomys obesus. C-banded karyotype of a female (top) and a spread from the male with the polymorphic condition for 2prox (bottom). Triangle encloses the biarmed 2prox and arrows point to the X and Y chromosomes.
32
32
• *
8
11
• • k • •• 1
(19/20)1
5
27 28
23
24
1
29
17
12
15
16
? 9
2prox
31
33
10
Hi 6
V 30
9
3
2dist
4prox
7
21
>
22
» '
13
H «
14
18
4dist
25
2 I 26
If X
Figure 13. G-banded chromosomes of Sekeetamys calurus.
33
6 1 -•.
5!* / *••• 8" 13 f
14 25
*f' 1
26
"
F i g u r e 1^
(19/20)i
i
•^1 «!
^ . . '
29 23
24
- ^
16
32
2dist 4dist
'-3,^1 11 21
22
«2^
2prox
33
i>-17
*.-.
18
1
5
27 28
9 4prox
^m
3
4 » 4<lkl
IB 31
\, G-banded chromosomes of
7
•V-1" 12
4Q * * ^
30
<{ 10 ^ • '
^5. i i l X X
Mer iones unguiculatus
34
- " II •
• i * ^
%
t % A # • • •
• ^ * <• • *
A
iJ'^i • •?? i " ' 5 » . B
• r i t -' t # *•*
^ f . |
4^;**r t i ^ V- '
n • • • • -
*•
• • • •
•u X Y
•i
i • ^
X X
Figure 15. C-banded karyotypes of two Meriones species. At top is M. tristrami and at bottom is M. unguiculatus. The autosome with interstitial heterochromatin in M. unguiculatus is number 33. Variable heterochromatic short arm additions occur in M. tristrami.
35
Figure 16. Presumed homologous elements between Desmodillus auricularis, Psammomys obesus, Meriones shawi, and M. unguiculatu (left to right).
36
4prox \
W^W mm 31 I 15
16
10
17
f^ ;i 4 If 8
' (
18 30 29 25
# 5 mm fi.
32 2dist 4dist 23
$g .='••• i:i I i « , : - : ife ••' 26 33 (19/20)i 6
mm
24
r ft. •;;' 9 ^f 15 ft r" ui sj v- f
12 22 14 11 2prox 21 XY
Figure 17. G-banded chromosomes of Meriones crassus.
37
i, il*'i-'r ^3 i 25 26 30 31 8
PP'ii^iud 29 17 10 22
23 24 4dist 33 12 3 13
^ *i :: «: *e 18 14 11 21
X X
Figure 18. G-banded chromosomes of Gerbillus dasyurus.
38
2prox
8 2dist 4dist
14 29 20 33
23
iiVi i l b ."Jfl 'SHi a ts 30
1.^ 4prox
13
17
32
15
24
4 iH W"'" * • • ^
n% 10 18 31 16 W
Figure 19. Presumed homologous elements between two Meriones and two Gerbillus species. From left to right: Meriones tristrami, M. crassus, Gerbillus dasyurus, and G. nanus.
39
8
• ' i lSi ^. -stw • GMPR
f:.«-i?3 >^^ Sir ^-i^^'lis 2
17
10
' * L
14 18 30 29 31
^M- U?^ s4? 4dist
Figure 20. Comparison of chromosomes of Gerbillidae with the outgroups. From left to right are chromosomes of: Gerbillurus vallinus, Meriones unguiculatus (Gerbillidae), Peromyscus boylii (Sigmodontinae of the Cricetidae), and Rattus surifer (Muridae, sensu stricto).
40
Figure 21. Interspecific variation in sex chromosomes of the Gerbillidae. X chromosomes shown from the following species (left to right): Meriones crassus, M. shawi, M. unguiculatus, Gerbillus dasyurus, Psammomys obesus, Desmodillus auricularis, Gerbillurus paeba, G. vallinus, Tatera leucogastor, T. afra. The Y chromosomes are from Desmodillus auricularis, Psammomys obesus, Tatera leucogastor, T. afra, and Gerbillurus vallinus.
41
Table 1. Character states for chromosomes of the Gerbillidae examined and of the outgroups. The numbering system relates to the karyotype of Tatera leucogastor (Fig. 1). A= Maxomys surifer (Muridae), B= Peromyscus boylii (Sigmodontidae), C= Tatera leucogastor, D= T. afra, E= T. brantsii, F= Gerbillurus paeba, G= G. vallinus, H= Desmodillus auricularis, 1= Psammomys obesus, J= Meriones tristrami, K= M. crassus, L= M. unguiculatus, M= M. shawi, N= Sekeetamys calurus, 0= Gerbillus dasyurus, P= G. nanus.
Linkage Species
Group A B C D E F G H I J K L M N O P
I 5 9 2 1 1 3 4 1 6 1 1 8 1 7 1 ?
2prox 1 1 2 1 1 3 1 5 6 6 6 6 6 7 1 4
2dist 1 1 3 1 1 4 1 5 7 6 6 8 6 9 1 2
3 6 4 3 3 3 3 1 2 2 1 1 2 2 5 1 ?
4prox 5 5 3 3 3 3 4 2 2 1 1 2 2 6 ? ?
4dist 1 1 2 2 2 2 3 1 5 1 1 4 4 6 1 ?
5 1 1 2 2 2 2 1 4 1 1 1 1 1 3 1 1
6 5 5 2 2 2 2 1 1 1 1 1 3 4 6 1 1
7 6 2 3 2 2 5 1 1 1 1 1 4 4 7 2 2
8 8 8 2 1 1 5 3 4 7 1 1 6 7 7 9 9
9 1 1 2 2 2 3 1 1 4 4 4 5 6 4 1 1
10 1 5 2 2 2 3 4 1 1 1 7 1 1 6 1 1
II 5 4 2 2 2 2 2 1 1 1 1 3 3 6 1 ?
12 5 4 2 2 2 2 2 1 1 ? 1 3 3 6 1 ?
13 1 1 2 4 4 2 1 2 2 1 1 2 2 2 1 ?
14
42
Table 1 . Continued
S p e c i e s
Char. A B C D E F G H I J K L M N O P
15 /16 ? ? 1 1 1 1 4 1 1 1 1 2 2 1 1 3
17 1 2 1 1 1 1 1 1 1 2 1 1 1 3 2 2
18 1 2 1 1 1 1 1 1 1 2 1 1 1 3 2 2
19/20 7 7 1 1 1 1 2 1 4 3 3 6 5 8 1 1
21/22 2 2 1 1 1 1 1 1 1 3 3 1 1 1 3 ?
2 3 / 2 4
2 5 / 2 6
29
30
31
32
33
X
Y
2
2
1
1
1
6
1
6
8
2
2
1
1
2
6
•
5
9
1
1
2
1
1
1
1
2
1
1
1
2
1
1
1
1
2
2
1
1
2
1
1
1
1
2
2
1
1
3
3
3
3
2
3
3
1
3
9
1
1
1
1
3
3
1
1
5
2
1
1
1
1
4
1
1
7
2
4
4
1
7
5
1
1
1
4
1
1
1
9
6
1
1
8
4
7
1
1
9
6
1
1
7
2
1
5
4
4
7 •
1
1
7
2
5
4
1
4
7
1
1
6
2
6
4
3
4
7 •
1
2
1
1
2
2
1
8
7
1
7
4
1
8
7
1
8
7
43
Table 2. Interpretation of chromosomal events for the different character states as listed in Table 1.
Linkage Character State
Group 1 2 3 4 5 6
I 1 1/2 1/30 1+H 1/? l/2di 1/29 1/ (l/?)i {19/20)i
2p 2 2/1 2/31 2i? 2i 2p (2p)i
2d 2 2i? 2/1 2/31 2i 2d 2d/l 2di/32 2di/3
3 3 3/4p 3/4 (3/4pr)i 3/2d (3/?)i
4p 4p 3/4p 3/4 4 (3/4p)i 7/4p
4d 4d 3/4 4 ll/4d 4d/ 4d/18 (19/20)i
5 5 5/6 5/ 5i (27/28)
6 6 6/5 6/8 6/ 6/8 6/10
(19/20)i Part.
7 7 7+E 7/8 7/12 7/8i 7+E 7/4p
8 8 8/7 8+H 8i+H 8i/7 8/6 8/32 8 part/ 8part 6
9 9 9/10 9/10+ 9i 9/(27/ 9i/31 H+C 28)i
10 10 10/9 10+H+ 10+H+ 10/E 10/6 10/E E/9 E
II 11 11/12 ll/4d (ll/12)i (11/ 11/ 12)par (19/20)i
12 12 12/11 12/7 (ll/12)i (11/ 12/17 12)par
13 13 13/14 (13/14)i
44
Table 2. Continued
Linkage Character states Groups 1 2 3 4 5
14 14 14/13 (13/14)i
15/16 15/16 15,16 (15/ (15/
16)+E 16)-E
17 17/18 17 17/12
18 18/17 18 18/4d
19/20 19/20 19,20 i i/4d i/6 i/1 i+E i/11
21/22 21/22 i 21,22
23/24 23/24 i
25/26 25/26 i 25,26 29
30
31
32
33
X, Y
29
30
31
32
33
See
29+E
30i
31 part.
32+E
33+H
29/32
30/1
31/2
32/29
33/31
Text for these
i 29/E 29/1
30i(partial)
31/? 31/9 31/33
32/8 32/2d 32i
33/?
linkage groups
i'29/:
31/4p 31/?
CHAPTER IV
DISCUSSION
Chromosomal Evolution
Chromosomal character state changes
With the advent of modern cytological techniques such
as differentially stained mitotic chromosomal studies,
systematists have attempted to use data from these
techniques in formulating more rigorous hypotheses
concening phylogenies of the taxonomic units they were
investigating. To formulate these hypotheses concerning
relationships, a determination of the primitive karyotype
(the karyotype proposed to have been possessed by the
ancestor of the taxa examined) is essential. Chromosomal
rearrangements that are modified from the primitive
karyotype are derived character states that can be used in
a similar fashion to morphological characters as
characterizing a certain subgroup or assemblage of the
taxa examined. On the other hand, the fact that two taxa
share a primitive condition cannot be used as a valid test
of their relationship (Engelmann and Wiley, 1977).
Various methods for determining ancestral characters have
been utilized in recent karyologic literature but these
methods can be grouped into three categoies:
45
46
1. "Common equals primitive": This method assumes
that if a character is found in several taxa in the group
investigated, it is assumed to be primitive. This method
was used by Dutrillaux et al. (1981, 1983) for a study of
murid chromosomes and by Bennazzou et al. (1980, 1981,
1983) for a study of gerbil chromosomes.
2. Use of an assumption (specific criterion)
regarding the direction of chromosomal evolution: Some
authors portray chromosomal evolution as resulting in a
general decrease of diploid number by fusions and as such
high diploid numbers are considered to be primitive a
priori (e.g., Freitas et al., 1983). The reverse
(increase in 2n by fissions), can also be assumed.
3. Use of outgroups: In this method determination
of a character state as being primitive is done only if
the state is shared by one or more of the ingroups with
the outgroup. This method of analyses has been used on
chromosomal studies of phyllostomid bats (Baker et al.,
1978, 1979), vespertilionid bats (Bickham, 1978, 1979;
Baker et al., 1985), cricetid rodents (Baker et al., 1983;
Koop et al., 1983; Stangl and Baker, 1984).
Many cytogeneticists who utilize chromosomal
rearrangements as character states failed to utilize the
vast literature on philosophy of systematics based on
morphological data. I will not attempt here to review the
47
arguments in the vast literature in that area. Rather, I
think it is useful to present a method of utilizing
chromosomal data in formulating phylogenetic hypotheses
similar to those utilizing morphologic data. The methods
of using ontogenesis and fossil evidence are inapplicable
to chromosomal data and this simplifies the task of
comparing the various methods even further. Chromosomal
data is also more amenable in some cases to use as
taxonomic characters than morphological characters as will
be discussed below.
The use of "common equals primitive" has been used in
few studies utilizing morphological data (see Estabrook,
1977). One reason why this method is largely rejected now
(Wiley, 1981: 153) is simply that common sometimes does
not equal primitive. For a good discussion of the
inadequacy of the commonality principle on philosophical
grounds, see Watrous and Wheeler (1981) and Wheeler
(1981). It may be that the primitive character state was
retained by only one of the taxa examined and all others
share a derived character state. In many cases, however,
the common character state does turn out to be the
primitive character state.
The method of assuming a direction for chromosomal
evolution based on fissions or fusions can be rejected on
both philosophical and cytogenetic grounds. Proposing a
48
specific criterion (e.g., fissions) represents a
"descriptive generalization of low explanatory value"
(Crisci and Stuessy, 1980). On cytogenetic grounds, all
types of rearrangements have been recorded in various
organisms from Drosophila to man. Also inversion data,
widely prevalent in peromyscine rodents for example,
cannot be used in this method. The most widely accepted
method for phylogenetic reconstruction using morphological
data is the outgroup method (see Maddison et al., 1984).
The outgroup method makes the assumption that ingroup taxa
comprise a monophyletic group based on some previous data
set. The choice of outgroup is thus critical. For
chromosomal data, the outgroup not only has to be far
removed that it cannot later be recognized as an ingroup
taxon, but it cannot be so far removed that it shares
little chromosomal homology with any of the ingroup taxa.
The outgroup method allows for consructing more
parsimonious ingroup trees (Farris, 1980, 1982; Maddison
et al., 1984).
Using Peromyscus boylii and Rattus surifer as
outgroups, the direction of chromosomal rearrangements for
each of the linkage groups can be determined. An
assumption of this methodology is that a character state
shared by ingroups and outgroups represents the primitive
state for the ingroup taxa. Some primitive states are
49
inferred if they are intermediate states between the
character states found in ingroups and outgroups. An
example of this is linkage groups 11, 12. These are found
in the outgroups (11^, 12^, 11^, 12^) and the states 11^,
12^ differ by a pericentric inversion and the fission
state (11 , 12- ) can only be derived by a centric fission
of 11^, 12^. Thus 11^, 12^ are assumed to be primitive
for the Gerbillidae by the rules of parsimony because they
require just one step from the state found in the
outgroup. Another assumption involves the complexity and
cytogenetic effect of the rearrangement considered.
Convergent identical inversions and fusions are assumed to
be much more rare events than producing acrocentric
character states by fissions in independant lineages.
This point is further discussed on page 69.
Following this philosophy of parsimony, I will
summarize some of the important features and alternative
interpretations for the direction of some of the more
important rearrangements. For a list of all conditions
and rearrangements see tables 1-2.
Linkage group 1. The primitive arm 1 is recognizable
and changed only by fusions (1^, 1^, 1^, 1^, l" , 1^) or
heterochromatic additions (1^) in the species of gerbils
examined and in Rattus surifer. In P. boylii, the
condition of Rattus is inverted (1 ).
50
Linkage groups 2p and 2d. The ancestral condition
for these linkage groups (2p^, 2d^) is found in both
outgroups and in several species of gerbils and can be
characterized as a telocentric chromosome like that found
in such diverse species as Tatera afra, Gerbillus
dasyurus, and Peromyscus. This chromosome is fused to
different elements in the Tatera/Gerbillurus group (e.g.
to 1 in T. leucogastor, and to 31 in G. paeba). In the
lineage leading to the Meriones group, an inversion
occurred producing a biarmed chromosome (still occurs in
Desmodillus, Figs. 2,8). A fission would then allow the
two segments (2p and 2d) to follow independent changes.
These two segments occur separately in M. tristrami and M.
crassus. 2d is fused to arms 1, 32, and 3 (2d^, 2d^, 2d^)
in Psammomys, M. unguiculatus, and S. calurus,
respectively. 2p is further inverted (2p') in S. calurus.
Linkage groups 2 rici 4p. These two groups occur
together (3^, 4p^) in Psammomys, Desmodillus, Meriones
shawi, and M. unguiculatus. This condition probably arose
from an inversion of the condition found in Peromyscus
(3^, 4p^) and then further fusion to an element (4d) to
form the arm combination 3/4 as found in T. afra, T.
leucogastor, and Gerbillurus paeba (Fig. 14). The
condition in G. vallinus arose by centric fission (3- ,
4p^, 4d^). The telomeric fusion of 4p and 4d occurs only
51
in the Tatera/Gerbillurus lineage. Centric fissions
producing an independent chromosome 3 (3^) must have
occurred at least three times in gerbil evolution: in G.
vallinus, in Meriones tristrami and M. crassus, and in the
Gerbillus lineage. These fissions can be regarded
however, as different events because, as exemplified by G.
vallinus, the fission was between 3 and 4 whereas in
Meriones it must have been 3 and 4p.
Linkage group 4d. The primitive condition (4d- )
occurs in several ingroup an outgroup species. As
mentioned above, it is fused to 3/4p in the lineage
leading to Tatera and Gerbillurus and 4d is fused to 3
different elements (4d^, 4d^, 4d°) in some members of the
Meriones group. Its fusion to 11 (4d^) provides a
synapomorphy for M. shawi and M. unguiculatus.
Linkage group ^. An independent chromosome 5 (5^)
occurs in outgroups and ingroups and thus represents the
primitive condition. It is fused to 6 in the
Tatera/Gerbillurus lineage and to another element
(probably 27/28) in Sekeetamys. This condition is
inverted (5^) in Desmodillus.
Linkage group ^. This linkage group represents part
of a large chromosome present in both outgroups (6^, see
Fig. 33). An acrocentric 6-'' is present as an independent
52
element in several species and fused to others in
different lineages.
Linkage group 2* Condition 7^ is the primitive
character state that occurs in both outgroups and some
ingroups. Depending on which interpretation of directions
of fusions and fissions, this character always produced
some degree of homoplasy in reversal to state 7^. One
explanation may be that once 7^ fuses with other elements
(e.g., to 8, Fig. 11) it loses the proximal part and with
fission events always produces the acrocentric, short 7
(7^). Fusion of 7 to 12 (7^) provides a synapomorphy for
M. shawi and M. unguiculatus.
Linkage group §. The character state of chromosome 8
in the outgroups (8°) is not found in any of the ingroups,
but the linkage group is identified in all taxa. 8- is
assumed to be primitive for all gerbils because it occurs
either by itself or it is fused to other elements in all
species examined. The condition in Gerbillus (8^) may
have arisen by a deletion or a fission of 8- (Fig. 32).
Alternatvely 8^ may be primitive for gerbils retained only
in Gerbillus, thus 8^ is a derived condition for the
remaining taxa. Because only two species of Gerbillus are
available and the condition does not occur in the
outgroups, this problem cannot be resolved until more data
become available. An inversion and an interstitial
53
heterochromatic addition are found in D. auricularis.
Although 8 is fused to 7 in T. leucogastor and G. paeba,
these represent two different states (8^, 8^), with the
difference being an inversion in 8. It is more
parsimonious to assume that the inversion occurred before
the fusion (because of the distribution of characters in
the Taterillini - both Gerbillurus species have the
inverted condition but in paeba it is fused to 7, whereas
in vallinus a heterochromatic short arm addition occurs
(8^).
Linkage group ^. Primitive state (9^) in outgroups
and ingroups is fused to different elements and is
inverted (9^) and then fused to other elements.
Linkage group 10. The acrocentric condition, 10- is
found in many gerbil species and in Rattus. In
Peromyscus, an additional euchromatic short arm is fused
to it. This primitive condition (lO"*-) is further modified
by fusions of chromosomal arms in various taxa. In the
genus Gerbillurus, this arm includes a euchromatic and a
heterochromatic addition. The direction of events for
10^, 10^ and 10^ is not clear. If the 10^ state is
primitive, then 10" resulted from an insertion of
euchromatin and heterochromatin, and 10^ by a subsequent
fission. Alternatively, the insertions occurred in the
unfused state (10^) followed by a fusion to form state
54
10 . Both alternatives are equally parsimonious and do
not affect the topology of the tree produced (Fig. 40).
Linkage groups LI and ]^. The fused 11/12 arises
from an an inversion of the condition in the outgroups
(11 , 11 , 12^, 12^). This fused condition is maintained
only in the Tatera/Gerbillurus lineage. In all other
genera, 11 and 12 occur independently or are fused to
different elements.
Linkage groups 13 and 14. Outgroups and some
ingroups have separate chromosomes 13 and 14 (IS-'-, 14-^).
If we assume these states to be primitive then the fused
condition (13^, 14^) is derived and forms a synapomorphy
for all taxa examined except the two Gerbillus species.
Two reversals to the fissioned state must have occured in
G. vallinus, and in the M. tristrami-M. crassus branch.
Alternative explanations would require more reversals. An
inversion in 13/14 (13^, 14- ) forms a synapomorphy for T.
afra and T. brantsii.
Linkage group 15/16. This linkage group could not be
identified in the outgroups. However, most gerbils
examined including all three major groups have the fused
state 15/16- . The fissioned state occurs only in the M.
tristrami-M. crassus branch and thus is assumed to be
derived. Gerbillus nanus contains an additional
euchromatic segment on this chromosome (15/16-^).
55
Linkage groups 17 and 18. Because both fused states
(17^, 18^) and unfused states (17^, 18^) for these two
chromosomes are found in both outgroups and ingroups, it
is particularly difficult to identify the primitive
condition. However, it is more parsimonious to assume the
convergent fissions in such diverse taxa as P. boylii, M.
tristrami, and Gerbillus than to assume identical fusions
in all other taxa examined. In Sekeetamys, chromosome 17
is fused to 12 (17^) and 18 is fused to 4d (18^).
Linkage group 19/20. Character state 1 of chromosome
19/20 is primitive for gerbils because it arises from an
inversion in character state 7 in the outgroups. This
state (19/20^) is conserved in many members of the
Tatera/Gerbillurus group, and in Gerbillus and
Desmodillus. An inverted state (19/20^), represents a
derived condition for the remaining members of the
Meriones group. This pericentric inversion produces an
acrocentric condition (19/20^) which further fuses with
linkage groups 4d, 6, and 1 to form biarmed chromosomes
(character states 19/20^, 19/20^, 19/20^, respectively) in
some taxa of the Meriones group.
Linkage group 21/22. The fused character state
21/22^ arose by a pericentric inversion of 21/22^ found in
both outgroups. Fissions produced state 21/22- and must
56
have occured twice—in G. dasyurus (and probably nanus)
and in M. crassus- M. tristrami branch.
Linkage group 23/24. All gerbils share the biarmed
23/24 (character state 1), which may have resulted from an
inversion of the acrocentric state (23/24^) found in the
outgroups.
Linkage group 25/26. The acrocentric state (25/26^)
found in the outgroups occurs only in Gerbillus. All
other gerbils have either state 25/26" (derived) or a
fission (25/26- in Gerbillurus vallinus).
Linkage group 27/28. This linkage group was not used
in the analysis because it lacks enough uniqueness in
differential banding to be recognizable. A biarmed small
chromosome probably representing this linkage group is
found in several genera examined and may have occured in
the ancestor of the Gerbillidae.
Linkage group 29. The primitive character state for
this linkage group (29^) is found both in outgroups and
ingroups. Further modifications involved fusions (29- ,
29^, 29^), a pericentric inversion (29^), euchromatic
insertion (29^), inversion plus euchromatic insertion
(29"^).
Linkage group 30. The acrocentric character state
30- is present in the outgroups, in the Tatera/Gerbillurus
group, and in Gerbillus, and thus represents the primitive
57
condition. Gerbillurus paeba is characterized by a fusion
of this acrocentric state to chromosome 1 (30^). A
pericentric inversion (character state 30^) occurs in all
members of the Meriones group (Meriones, Desmodillus,
Psammomys, Sekeetamys). Meriones tristrami and M. crassus
are characterized by a further rearrangement (30^,
probably a tandem fission).
Linkage group 31. An acrocentric 31 (character state
SI-*") is the primitive condition because it is found in
both ingroups and outgroups. All further rearrangements
in gerbils were by fusions to different elements.
Linkage group 32. Chromosome 32 is found in all
gerbils either in the acrocentric condition (32- ) or fused
to different elements. Because this character state can
arise by a pericentric inversion of the state found in the
outgroups (32°), it is assumed to be the primitive
condition for gerbils.
Linkage group 33. An acrocentric 33 (character state
33- ) is found in outgroup and ingroup taxa and is thus the
primitive condition. A heterochromatic addition is found
in Gerbillurus paeba (33^). A centric fusion to
chromosome 31 produced character state 33* found in
Sekeetamys and fusion to a small unidentified chromosome
in Meriones crassus produces 33 .
58
The primitive character states for the linkage groups
of the Gerbillidae thus probably had the following
acrocentric or telocentric autosomes: 1, 2 (2p and 2d),
4d, 5, 6, 7, 8, 9, 10, 13, 14, 29, 30, 31, 32, 33 and the
following biarmed autosomes: 3/4p, 11/12, 15/16, 17/18,
19/20, 21/22, 23/24, 25/26, and possibly 27/28 (Fig. 22,
Tables 1 and 2). Together with the sex chromosomes, the
primitive diploid number for the Gerbillidae would be 52,
with 32 acrocentric and 18 biarmed autosomes (FN=68).
Euchromatic autosomal rearrangements
From the proposed primitive karyotype for gerbils
(see above), the following autosomal rearrangements must
have occurred to account for the variation in euchromatic
morphology of the species studied:
1) Pericentric inversions: These must have occurred
at least nine times: in linkage group 2 in the Meriones
group (2p^,2d^), 2p in Sekeetamys (2p'), 5 in Desmodillus
(5^), 8 in Desmodillus (8^), 13/14 in Tatera afra and T.
brantsii, 19/20 in the Meriones group (19/20^), 25/26 in
both the Meriones and the Tatera/Gerbillurus groups
(25/26-^), 29 in Psammomys, M. shawi and M. unguiculatus
(29^), 30 in the Meriones group (30^). Of these, only one
(29) may have involved a reversal event (in Sekeetamys,
Fig. 44).
59
2) Paracentric inversions: This rearrangement was
recognized in chromosome 8 of Gerbillurus group (8^), 2 of
Gerbillus nanus (2p5,2d2), and chromosome 9 of the
Meriones group (9^).
3) Robertsonian fusions: This is the most common
type of rearrangement in the group of gerbils examined and
occurred at least 40 times. The resulting conditions in
various species are complex and the reader is referred to
Tables 1 and 2 for a summary. It is interesting to note
that the patterns of these fusions in different species
indicate monobrachial homology similar to patterns
described by by Baker et al. (1985) and Baverstock et al.
(1982).
4) Tandem fusions: The only clear example of this is
fusion of 4p/4d to form chromosome 4 in the Tatera/
Gerbillurus group. The area joining these two primitive
linkage group in the Tatera/Gerbillurus group forms a
neck-like structure similar to that described by Wahrman
et al. (1983) as characteristic of breakage and reunion
events involving loss of a centromere (Fig. 9). Several
other examples are listed below as euchromatic additions
because the added elements could not be identified to any
of the numbered linkage groups.
5) Robertsonian fissions: Fissions occurred a
minimum of 18 times in the following chromosomes: 2 in
60
the Meriones group, 3/4 in Gerbillurus vallinus, 3/4p (2
times), 7/8 in G. vallinus, 9/10 in G. vallinus, 11/12 in
the Meriones group and in the Gerbillus group (2 times),
13/14 (2 times), 15/16 in M. shawi and M. unguiculatus,
17/18 (2 times), 19/20 in Gerbillurus vallinus, 21/22 (2
times), and 25/26 in G. vallinus.
6) Other rearrangements: Some rearrangements are
identified as additions of euchromatic segments. This
occurred in chromosomes 7, 8, 10, 15/16, 32, and 33. The
euchromatic segments added could not be identified in the
numbering system because they involved a small number of
bands. Similarly euchromatic deletions were observed but
only in chromosomes 15/16 and 29 in Gerbillurus vallinus,
and 31 in Gerbillus dasyurus. These rearrangements may be
added to fusions and fissions respectively if the segments
added or deleted could be identified accurately as
separate linkage groups. This is required to explain the
differences in diploid numbers exclusive of the major
fusions and fissions.
Heterochromatic rearrangements
Constitutive heterochromatin is usually characterized
as staining positive with the C-banding technique, having
late DNA replication, and consisting of repeated
nucleotide sequences (Peacock et al., 1981). The reaction
of these heterochromatic regions to other banding
61
techniques can vary widely; in gerbils heterochromatic
regions can stain G-negative to G-positive (e.g.. Fig. 5).
Because both the outgroups and all species of gerbils have
centromeric heterochromatin, it is reasonable to assume
that this is the primitive condition. Beyond this, many
species are characterized by heterochromatic additions and
these fall into four basic types:
1) Short arm additions which increase the fundamental
number without affecting the euchromatic segments. This
occurs in the following species (total number of
chromosomal pairs affected shown in parantheses):
Gerbillurus vallinus (2), Gerbillus dasyurus (2), Meriones
tristrami (3-5), M. crassus (2), Psammomys obesus (1), and
Tatera (4). In many of these species, short arm additions
also vary intraspecifically. The previous list of species
also represents those with high diploid numbers and thus
ones with many acrocentric euchromatic chromosomes.
2) Interstitial insertion of heterochromatic bands.
This was noted in chromosome 10 of Gerbillurus, 8 of
Desmodillus auricularis, and 33 in Meriones unguiculatus.
3) Telomeric addition. Observed in the sex
chromosomes of Gerbillurus.
4) Diffused heterochromatin occurs in chromosome
25/26 of Tatera and 33 of Gerbillurus paeba.
62
Two closely related species of Gerbillus (hesperinus
and nigeriae) have large amounts of heterochromatin almost
on every chromosome (Viegas-Pequignot et al., 1984). This
situation is similar to that found in Onychomys and
Thomomys of North America (Patton and Sherwood, 1982) and
suggests that orthoselection for addition of these
heterochromatic regions may occur independently and
frequently in rodent lineages (Baker et al., 1979). The
most widely held view is that heterochromatic short arm
additions are evolutionarly inert (Ohno, 1973; Korobitsyna
and Korablev, 1980). However, heterochromatic regions may
have functional loci and also may affect neighbouring
euchromatic loci (Peacock et al., 1981). Why many species
of gerbils show these heterochromatic addition that are
either fixed or variable must await further research.
Evolution of the Sex Chromosomes
The major G-banding sequence on the X chromosome is
conserved in many mammals. Furthermore, gene mapping
studies have shown that the X chromosome also contains
genes coding for the same products in many mammals (Ohno,
1984).
The X chromosome of Rattus surifer (Fig. 38) is a
small acrocentric and this condition is shared by many
murids (Baverstock et al., 1982). X chromosomes of all
species of gerbils examined are relatively larger and more
63
complex. It is possible to conclude that gerbil X
chromosomes represent derived conditions by which
additional material was added to the X chromosome.
Possible sources for this additional material include
duplication of pre-existing genosomal genes, autosomal
translocation on to the sex chromosomes, and
heterochromatic additions. In cases where the sex
determining mechanism shifted from an XY system to an
XY1Y2 system, the mechanism of autosome-sex chromosome
translocation has been well established (Wassif, 1977,
1981; Wahrman et al., 1983; Viegas-Pequignot et al.,
1982). The origin of the large X chromosomes of Psammomys
obesus and Desmodillus auricularis may have been by
heterochromatic additions, because these chromosomes stain
positively with C-banding.
In all species of gerbils examined, the Y chromosome
was almost entirely heterochromatic, but the shape and
size of this chromosome varied. In Gerbillurus vallinus
the Y chromosome resembles the terminal portion of the
long arm of the X chromosome in both G-banding (Fig. 6)
and C-banding (Fig. 10) preparations. In the genus
Tatera, this chromosome is small acrocentric (Y-*-) in T.
leucogastor, and a large metacentric in T. afra and T.
brantsii (Y^). Psammomys obesus and Desmodillus
auricularis show even larger metacentric Y's. Because
64
this element is composed mostly of heterochromatin and
shows little or no differentiation by the G-banding
technique, it is hard to determine the direction and
nature of events involved in its evolution. Many species
of mammals have a small Y chromosome that carries few
genes. If this is assumed to be the primitive state, then
the larger and metacentric Y's probably are derived by
addition of genetic material.
Chromosomal evolution in the Gerbillidae is complex,
with a minimum of 80 euchromatic autosomal rearrangements,
24 heterochromatic rearrangements (many of them variable
intraspecifically), and a minimum of 12 rearrangements
involving the sex chromosomes. Of the 80 euchromatic
autosomal rearrangements, centric fusions and fissions are
the most common (50% and 22.5% respectively). Based on
random distribution of breaks in the chromosomes, one
would expect fusions and fissions to occur equally in any
given lineage. Two facts may explain the higher number of
fusions relative to fissions. First, the occurrence of a
fusion is easier to document simply because fissioned
chromosomes are free to undergo further fusions and the
cladistic method would thus be constrained by loss of
intermediate stages. An example of this is chromosome
8/32, which occurs in Psammomys, Sekeetamys, and Meriones
shawi. By cladistic methodology, the ancestor of M. shawi
65
and M. unguiculatus must have had the fused 8/32 and thus
the presence of 8 fused to 6 in M. unguiculatus must have
been preceeded by fission 8/32 as a most parsimonious
route. On the other hand, M. crassus and M. tristrami
both with high diploid numbers may have had an ancestor
that possessed the fused arms that form synapomorphies for
other closely related species (for example 8/32, 7/12;
Fig. 24).
Second, only few of the taxa examined had high
diploid numbers and thus more fusions were traced. If
more taxa with high diploid numbers are added, one would
expect more fission events to be visible on the tree.
More of these high diploid number species may however
cause parsimony to favor using fissions as synapomorphies
for these taxa and place inversions as homoplasies. This
points out the danger of using strict parsimony when many
fusion results are observed simply because these events
are susceptible to reversals. The implications of these
and other events are discussed under the section on modes
of chromosomal evolution.
Systematic Implications
The analysis of derived character states can produce
different tree topologies but, according to cladistic
philosophy, the most parsimonious tree or trees should be
chosen to minimize convergence and reversals and as the
66
best estimate of the phylogeny of the group. The most
parsimonious arrangements show three well defined groups
of gerbils (Fig. 22):
1. "Tatera/Gerbillurus group."
2. "Meriones group" — includes Meriones, Psammomys,
Sekeetamys, and Desmodillus.
3. "Gerbillus group."
Each of these groups is characterized by several
synapomorphies and each is discussed separately below. In
addition to the characters unique to each of these groups,
there are few characters that resolve their trichotomy.
Two alternatives are available (Fig. 38):
1. The Meriones and Gerbillus groups share a common
ancestry characterized by a fission of 11/12 (11 , 12-^);
this is possible if we assume that 8-'" is primitive and 8^
is derived for Gerbillus. This alternative would agree
with the taxonomy of Chaline et al. (1977) and Pavlinov
(1982) but produces homoplasy in fusion of 13/14 (13^,
14^) and an inversion in 25/26 (25/26^)
2. The Meriones and the Tatera/Gerbillurus groups
share a common ancestry characterized by fusion 13/14
(13^, 14^) inversion in 25/26 (25/26^) and formation of
character state 1 for chromosome 8 (8-'-). This alternative
places Gerbillus as an early branch of the Gerbillidae.
This is further substantiated by the many primitive
67
chromosomal character states that it shares with the
outgroups (Table 1).
The second alternative is more parsimonious and best
represents the chromosomal data but is based on limited
data from two species of Gerbillus. Because some
morphological data lend support to the first alternative,
it is best to keep this as an unresolved trichotomy until
more species of the Gerbillus group and the Tatera/
Gerbillurus group are examined.
Tatera/Gerbillurus Group
Ellerman (1941: 503) placed the South African
Gerbillurus paeba and G. vallinus in the subgenus
Gerbillus (genus Gerbillus) and indicated that these taxa
are closely related. The soles of the feet in G. vallinus
are sparsely haired which make it "transitionally towards
Dipodillus" (Ellerman, 1941: 503). However, most recent
workers (Chaline et al., 1977; Pavlinov, 1982) allied
Gerbillurus with Tatera and Taterillus in a group
(Taterillinae or Taterillini) which is of equal rank to
that for the higher gerbils (Gerbillinae or Gerbillini).
A tree based on the chromosomal data for the genera Tatera
and Gerbillus is shown in Fig. 23. This tree places
emphasis on the identity of the derived X chromosome
(similar in both species of Gerbillurus and in both Tatera
species examined) and on the insertion of both
68
heterochromatin and euchromatin in chromosome 10 of
Gerbillurus (10^). The homoplasies in the tree (double
lines) are primarily fission events. An alternative tree
places Gerbillurus paeba with Tatera as a monophyletic
group and produces the same number of homoplasies. This
tree has some fission events and also has the X^ and 10^
as homoplasies. Although the number of homoplasies is
equal, this is misleading because data are duplicated in
fission results as two linkage groups and thus two
homoplasies. The fission event although coded as two
characters is as likely, if not more likely, to happen
than any other event. The chance that two identical
fissions occurring is certainly more than building two
identical X chromosomes or constructing an identical arm
10 (10^ and 10^).
The three species of Tatera examined are close
chromosomally (Figs. 23, 27). Based on G-band homology,
there is no chromosomal basis on which to predict
infertile hybrids. These taxa are morphologically similar
(Ellerman, 1941) and thus may represent an early stage in
speciation of this group.
Meriones Group
Ellerman (1941) recognized three subgenera of
Meriones: Parameriones (persicus, calurus), Meriones
(tamaricinus, libycus, meridianus, and unguiculatus
69
groups), and Cheliones (hurriana group). He recognized S.
calurus as a member of the subgenus Parameriones of the
genus Meriones. Chaworth-Musters and Ellerman (1947)
recognized M. calurus as a separate subgenus (Sekeetamys)
and Harrison (1972) and most recent authors recognized
this taxon as a separate genus, Sekeetamys, closely
related to Meriones. Wassif (1954), however, thought that
Sekeetamys was more closely related to the
Gerbillus/Dipodillus assemblage. Wassif (1977, 1981) even
included this species in a study of chromosomes of the
Dipodillus group from Egypt. Chromosomally, it shares
three characters (fission of 2, inversion in 9, and
inversion in 19/20) with Meriones and Psammomys (Fig. 24).
It further shares the fusion of arms 32 and 8 (32^, 8')
with Psammomys and M. shawi and the structure of the X
chromosome (X^) with M. shawi and M. unguiculatus. The
most parsimonious tree is shown in Fig. 42, and
surprisingly it shows both Sekeetamys and Psammomys as
being closely related to some members of Meriones (shawi
and unguiculatus). If this is true, then the genus
Meriones as currently understood is paraphyletic. An
alternative explanation is that the high diploid numbers
of M. tristrami (2n=72) and M. crassus (2n=60) resulted
from fissions involving chromosomal arm combinations that
now are thought to be synapomorphies for species with low
70
diploid numbers. Thus the ancestors of M. tristrami and
M. crassus may have had the combinations 8/32 (8* , 32^),
ll/4d (11^, 4d^) and others that by fissions obliterated
the relationships of these taxa. This points to a very
important consideration when analyzing chromosomal data in
Gerbillidae. Species with high diploid numbers provide
less information than those with low diploid numbers
unless inversions or other rearrangements other than
centric fission events are involved. In this case, there
are other characters (e.g., inversions in 2 and 19/20)
that clearly place the Meriones assemblage (including
Seleetamys and Psammomys) together but the position of the
various species of Meriones must await other data sets
(e.g., mitocondrial DNA and electrophoresis).
The monotypic genus Desmodillus was variously placed
near Pachyuromys in the Gerbillini (Lay, 1972) or as more
closely related to Desmodilliscus of the Taterillini
(Ellerman, 1941; Petter, 1975). Chromosomally, this taxon
is best considered as a more primitive member of the
Meriones group (Fig. 24). The most distinguishing
synapomorphies for this group are inversions in linkage
groups 2 (2p5, 2d5) and 30 (30^).
Gerbillus Group
Gerbillus (including Dipodillus) contains from 34 t
62 species depending on the authorities consulted with 2N
71
of 38 to 74 and thus would be expected to show extensive
chromosomal rearrangements. Wassif (1977, 1981) showed
that there was considerable homology between 4 species of
Gerbillus yet little homology between these four species
of Gerbillus and three species of Dipodillus. Although no
outgroup was examined, Wassif (1977, 1981) concluded that
these two groups do represent distinct genera.
In this study, only two species of this group were
examined and in one case (G. nanus), the G-banding
patterns were not well-resolved. These two species
retained primitive sequences for many elements (Table 1).
From the primitive karyotype for Gerbillidae they
underwent fissions in 3/4p, 13/14, 17/18, 21/22 and other
types of rearrangements (e.g., euchromatic addition to 32;
Fig. 25). This group is clearly in need of additional
study and may prove to contain species that have retained
all the primitive sequences for Gerbillidae.
Modes of Chromosomal Evolution in Gerbillidae
Wilson et al (1975) proposed that rapid chromosomal
evolution in mammals can be explained by their highly
social structure allowing small deme sizes. The genus
Sekeetamys is a rare and solitary gerbil that has
undergone a minimum of nine rearrangements since it shared
a common ancestor with Psammomys. Members of the latter
genus are highly social, forming colonies reminiscent of
72
Cynomys of the New World and yet this genus shows only
three rearrangements since the common ancestor. Clearly,
social structure is not adequate to explain this
difference in rate of chromosomal evolution.
- ® ^ ' alizatj on model of chromosomal evolution
(Bickham and Baker, 1979), based on the premise that
cjiromosomal rearrangements are adaptive^ predicts that a
group undergoes most of its chromosomal evolution early in
its evolutionary history and radiates into a new adaptive
zone. Once higher categories (e.g., genera) are
established, the rate of chromosomal evolution slows. In
the Cricetidae (Baker et al., 1983) and also clearly in
the Gerbillidae, the canalization model seems to be
inadequate to explain the pattern observed. Karyotypic
orthoselection (White, 1975) also does not seem to be
operating in gerbils because all types of chromosomal
rearrangements are observed. Similarly karyotypic
megaevolution (Baker and Bickham, 1980) is not observed in
any of the taxa examined although it may explain the low
diploid number (2n=18) of Ammodillus imbelis (not examined
here).
Several observations on chromosomal evolution in
Gerbillidae are worth summarizing here.
1. Many genera contain species with both high
(60-74) and low (30-50) diploid numbers (Fig. 26).
73
2. Unrelated species with high diploid numbers share
many acrocentric chromosomal conditions but this fact does
not make them closely related, because they share
inversions and other rearrangements with their congeners
and thus probably have undergone independent fissions
(homoplasy in the acrocentric character states).
3. The results of fissions of two sets of
chromosomes may be identical even though the unfissioned
sets may be very different (e.g., have monobrachial
homology).
4. Using the proposed primitive karyotype for
Gerbillidae (2n=52), some lineages underwent centric
fusions (e.g., to Gerbillurus paeba 2n=36), others only
fissions (e.g., to Gerbillus dasyurus 2n=60), and in some
cases a set of fusions followed by a set of fissions
(e.g., to Gerbillurus vallinus 2n=60)(Fig. 27).
5. In cases where fissions occurred, there were
other rearrangements (e.g., inversions, insertions) that
allowed the taxon to be placed with its unfissioned
congeners rather than with other species with high diploid
numbers.
These observations suggest a pattern of chromosomal
evolution in gerbils that is unique. Two assumptions must
be dealt with before discussing this further. First, that
the cladistic method applied here yields a fairly
74
congruent phylogeny to that proposed based on other data
sets by the rule of parsimony. This assumption can be
questioned if for example more taxa with high diploid
numbers were used or the resulting phylogeny was
questioned by other data sets. Recent morphological
(Pavlinov, 1982) and electrophoretic (Qumsiyeh,
unpublished) data support the phylogeny presented here.
Second, that the meiotic process in the Gerbillidae is not
much different from other groups on which cytogenetic
principles have been applied. Thus, inversions would
cause much more reduction in hybrid fertility than would
fusions or fissions. This assumption is substantiated in
previous studies on hybrids in gerbils. Wahrman and
Gourevitz (1972) found a range in diploid numbers in
Gerbillus pyramidium from 40 to 66 due to fusions with
apparently no affect on fertility of hybrids. Lay and
Nadler (1975), on the other hand, found severe impairement
of hybrid fertility in crosses between Meriones shawi and
M. libycus, which differ only by one inversion of the X
chromosome.
The data on prevalence of Robertsonian fission-fusion
heterzygotes (Patton et al., 1980; Koop et al., 1984) and
the few cytogenetic studies available (Elder and Pathak,
1980; Hall, 1973) document that this form of chromosomal
rearrangement can be fixed with little or no ill effects.
75
The chromosomal data presented in this work thus suggests
the following pattern of chromosomal evolution in this
group.
1. Starting with a primitive karyotype, some
chromosomes undergo alternate fusions in different
lineages and thus speciate by centric fusions with little
meiotic constraints (Baker et al., 1985; Baverstock et
al., 1982; John, 1981).
2. The resulting lineages are now independent and
can undergo further chromosomal evolution by inversions,
insertions, and other rearrangements as well as
accumulating genie and morphologic differences.
3. Only after fixation of the rearrangements that
cause major meiotic problems in hybrids (e.g.,
inversions), some members of the lineage underwent
fissions to return to a high diploid number or even exceed
that of the ancestral taxon. An example of this can be
seen in the lineage leading from the ancestor of the
Meriones group (2n=50) to M. tristrami (2n=72). If no
rearrangements other than fusions were fixed, then fission
results in two independent lineages can produce fertile
hybrids because they reversed to the condition found in
their ancestor.
4. The resulting species with high diploid numbers
but with quite different genomal organization and also
76
morphology and genie structure are now free to undergo a
further cycle of fusions and speciation.
This may be seen as a continuous cycle of events not
neccessarily affecting the total genome, but only small
subsets of chromosomes at a time. The steps listed above
are also simplified and the process is more complex. The
ancestor for Gerbillurus, for example, had a diploid
number of 44 similar to that of Tatera. Four fusions were
acquired in G. paeba (2n=36), whereas G. vallinus acquired
eight fissions (Fig. 27). These fissions and fusions
affected different linkage groups and were independent.
These observations contradict previous hypotheses based on
non-differentially stained karyotypes of a general pattern
of decreasing (Benirschke et al., 1965; Grobb and Winking,
1972; Gustavson and Sundt, 1969) or increasing (Hansen,
1975; Kato et al., 1973; Imai and Crozier, 1980) diploid
numbers during the course of chromosomal evolution.
77
Outgroups
Rattus myscus surifer ^^^ym
Tatera/ Gerbillurus Group
Meriones Group
122 112
Gerbillus Group
•81 •132 •142 •25/261
•89 •131 141
111 121
11 2pi 2di 32 4p2 4di 51 61
72 8? 91 IQi 112?122?13i?14i ?
15/161171181 19/201 21/221 23/241 25/262 27/28? 29' 301311321 331 X?Y?
Figure 22. Character s t a t e s and t ree stems for the Gerbi l l idae and the outgroups. The t r ees for the three recognized groups of Gerbil l idae are shown in Figs . 23, 24, and 25. See text for d i scuss ion .
Gerbillurus vallinus
V ^31 .4p4
:5i
•61 L7I •83 :9 i .10^ :i3i rl4i .19/202 5 21/223 -25/263 •299
Gerbillurus paeba
13 .2p3 •2d^ •75 •85 .93 •293 303 313 323 332
I 103 X3
Tatera Tatera Tatera leucogastor afra brantsii
78
52 62 92 132 142 33 4p3 4d2 102 25/261 292
Figure 23 . Tree for the Tatera /Gerbi l lurus group. This t r e e shows 33 apomorphies ( s i n g l e l i n e s ) and 11 homoplasies (double l i n e s ) .
79
y 3> <c s
- - 1 " . - 2 p ^
0 - - !«• - - 2 d 7 - - 4 d 5
- -19/20^4-^^ - - 3 1 4 __4p<^
- - 4d6 - - 5 3 - - 6 ' - - 7 7 - -10^ - -n*-- -12* 4=173
:183
5?
- -V - - 2d8
- - 2 d ' - - 1 9 / 2 0 5 - 6 3 -1-315 - - 8 6
- - 9 5 - -19/20* = =325 - - 3 3 «
- -6^ - -9< '
- -4d^ - -7< - - 1 1 3 - -123
Ti;/2o« t " / ' ' ' - -29*
31* 333
- - X 7
= =172 = =182
- -10" 298
•X<
- - 8 ^ =4=29
32"
Meriones Group
c ^
8* 295
- l - X ^
31 4pi 131 141 21/223 30* X'
2p* 2d* 9* 19/203
- - 2 p 5 - - 2 d 5
- - 302
Figure 24. The most parsimonious tree for the Meriones group. See text for discussion.
80
Gerbillus Gerbillus dasyurus nanus
.2p4
Gerbillus (Group
2d2 15/163
31*
31 89 172 182 21/223 312 322 X8
Figure 25. Tree for the two Gerbillus species examined.
81
V/)
R O
F S
PE
C
00
^ - ) z
1 A| Tr* TrTr fc"
Tr 3
o T
S G G
1 T M M G G G
M G*
Tr T T M M M M T
T T P
T M
T G G G
C* D TrG G G
M G G 3
o G r T M G
G G
1 a 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 58 60 62 64 66 68 70 72 74
DIPLOID NUMBERS
Figure 26. Histogram to illustrate distribution of diploid numbers in the family Gerbillidae. Abbreviations are as follows: A= Ammodillus, D=Desmodillus, G=Gerbillus, Gu=Gerbillurus, M=Meriones, R=Rhombomys, T=Tatera, Tr=Tate7TTlus. Two species of Gerbillus have diploid numbers that range from 38 to 66 (G. pyramidum) and 62 to 68 (G. hesperinus). Stars indicate species with sex chromosome/autosome translocations.
82
\
%
\
% «/>
3 (/> = S
O >
e
(A
3 S
a; («
^
i. -5r
t'
So 2
|2i
s • on
"D 0 E (/) &) O
tf)
• • t9
3 U • B
3 tz
m
tn
c o (/I
a> «N
1 UJ
• k ^ • ^ ^
v£
^ i n
""' 1
UJ . . k
ve > i n
( N
f N
ee
«^ eo
CN tn
e f N •
P^
1/30
, 2/
(/) c o . a .
3 u.
T-"
X •K
e
"o
>
ee v^ r r4 •v^
To 3
3
iions
T
3 U . <N
>• •«
• ^
1 "
^
c x: «N
^^ ^ B
•
a> • \D
in
«/) c 0
• • ^
3 uu
fn
. 1
0^ fN + UJ
• k
o fn
00
f S
a> f N
+ UJ
rr • ^
Q. o •T in • " ^ II
r Figure 27. Tree for the Tatera/Gerbillurus group to illustrate change in diploid numbers by fissions and fusions.
83
Table 3. Corresponding linkage groups between Peromyscus and the Gerbillidae. Standard numbers for Peromyscus chromosomes (Committee, 1977) and the corresponding linkage groups and their states for Gerbillidae are presented.
Peromyscus
1
2
3
4
5
6
7
8
9
10
11
12
Gerbillidae
6^/8^
1^/19/20*7
llS 12
2p^, 2d^
10^
32^
72
34/4p5
2gl
30^
9I
3l2
Peromyscus
13
14
15
16
17
18
19
20
21
22
23
X
Gerbillidae
18^
23/242
4d^
5I
25/262
21/222
part. 33?
141
172
131
-> •
X5
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Wassif, S. 1977. Untersuchungen uber Verwandtschaft bezeihungen in den genera Gerbillus und Dipodillus unter anwendung der chromosomen-Bandentechniken. Doctoral Dissertation at Georg-August- Universitat, Goettingen, 149 pp.
. 1981. Investigation on the relationships of the genera Gerbillus and Dipodillus (Rodentia, Cricetidae) by the use of chromosome banding techniques. Bull. Zool. Soc. Egypt, 31: 139-155.
Watrous, L. E. and Q. D. Wheeler. 1981. The out-group comparison method of character analysis. Syst. Zool., 30: 1-11.
Wheeler, Q. D. 1981. The ins and outs of character analysis: A response to Crisci and Stuessy. Syst. Bot., 6: 297-306.
White, M.J.D. 1968. Models of speciation. Science, 159: 1065-1070.
White, M.J.D. 1975. Chromosome repatterning — regularities and restrictions. Genetics, 79: 63-72.
. 1978. Chain process in chromosomal speciation. Syst. Zool., 27: 285-298.
Wiley, E. 0. 1981. Phylogenetics: The theory and practice of phylogenetic systematics. John Wiley and Sons Inc., New York, xv+439 pp.
Wilson, A. C , L. R. Maxson, and V. M. Sarich. 1974. The importance of gene rearrangement in evolution: evidence from studies on rates of chromosomal, protein, and anatomical evolution. Proc. Natl.. Acad. Sci., USA, 71: 3028-3030.
98
Wilson, A. C , G. L. Bush, S. M. Case, and M. C. King. 1975. Social structuring of mammalian populations and rate of chromosomal evolution. Proc. Nat. Acad. Sci., USA, 72: 5061-5065.
Yates, T. L., R. J. Baker, and R. K. Barnett. 1979. Phylogenetic analysis of karyological variation in Peromyscine rodents. Syst. Zool., 28: 40-48.
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APPENDIX A
Karyotypic Data for Gerbillidae
The diploid number is given for each species followed by the number of metacentric and submeta- centric autosomes (M), the numbers of acrocentric and telocentric autosomes (A), the size (small letters) and shape (capital letters) of the X and Y chromosomes, the locality and the reference. Some authors include sex chromosomal arms in counts of fundamental numbers, others only autosomal arms. Because of this, I give the number of biarmed autosomes and numbers of acrocentric autosomes rather than the fundamental number (unless this information is not obtainable from these references).
Species 2N M Locality and Reference
Ammodillus imbelis 18 18
Brachiones przewalski No data
Desmodilliscus breweri No data
52 ? Desmodillus
auricularis
Dipodillus maqhrebi
Dipodillus simoni
Dipodillus zakariai
? M M
52 28 22 IM mM
No data
60 8- 48- ? ?
10 50
60 0 58 IM sSM
60 8- 50 ? ?
10 50
No data
Somalia; 4 (M includes
South Africa; 27
South Africa;this paper
Egypt; 57
Egypt; 58, 59
Tun i s i a; 5
99
Appendix A. Continued
100
Gerbillurus paeba
Gerbillurus setzeri
Gerbillurus tytonis
Gerbillurus vallinus
Gerbillus agag
Gerbillus amoenus
Gerbillus andersoni
(=allenbyi)
Gerbillus aquilus
Gerbillus bottai
Gerbillus campestris
36
36 34 0 mSM sA
36 34 0 mSM sA
South Africa; 30
S. Africa, Namibia; 45
S. Africa, Namibia;
this paper
60
36
36
60
60
No
52
52
40
40
40
40
40
38
No
56
56
58
18
34
34
22
12-
20
data
9-
10
8
38
38
38
38
38
36
data
7
13-
15
8
40
0
0
36
38-
46
42-
43
44
0
0
0
0
0
0
7
41-
43
48
ISM
SM
mSM
IM
ISM
7
ISM
ISM
ISM
ISM
7
7
sA
7
SA
sA
sA
7
sA
sSM
mSM
sSM
7
7
ISM sM
SM
7
IM
SM
7
mM
Namibia; 45
Namibia; 2
Namibia; 45
S. Africa,Namibia; 45
S. Africa, Namibia;
This paper
Egypt; 57 (M includes
sex chromosomes)
Egypt; 58, 59
Egypt; 57
Egypt,Israel; 21
Egypt; 58, 59
Tunisia; 6
Israel; 56
Pakistan, Iran; 21, 23
Algeria; 25
Egypt; 57
Egypt; 58, 59
Appendix A. Continued
101
Gerbillus cheesmani
Gerbillus dasyurus
Gerbillus dunni
Gerbillus famulus
Gerbillus gerbillus 42,43 ?
42,43 38-
40
42 32
42,43 32
56,
57,5£
56
56
38
38
60
60
60
60
74
No
10-
1 12
10
14
34
34
6-8
6
9-10
8-
12
24
data
44-
48
44
40
2
2
52-
54
52
50-
51
46-
50
48
mM
IM
ISM
IM
mSM
7
IM
7
IM
ISM
sA
sSM
sSM
sSM
SM
7
7
7
SA
mM
Morocco; 21
Morocco; 9
Tunisia; 15
Iran; 21, 23
Iran; 12 (7:320)
Sinai; 56 (M includes
sex chromosomes)
Sinai; 21, 23
Egypt; 57
Jordan, Palestine; th
paper
Somalia; 4
42,43 34 6
42,43 34- ?
36
42,43 36 6
42,43 32 8
? ? Algeria; 25,26 (Y1,Y2)
ISM Y1Y2 Israel; 56(M includes
sex chromosomes)
ISM ? Morocco; 21
ISM Yl=sM
Y2=sSM Sinai, Egypt; 21, 23
ISM 2SM Egypt; 58, 59
ISM 2A Egypt; 57
ISM ? Tunisia; 15
lA sSM,sSM Egypt; 12 (7:321)
102
Appendix A. Continued
Gerbillus gleadoni 50,51 20 28
Gerbillus henleyi
Gerbillus hesperinus
Gerbillus hoogstraali
Gerbillus jamesi
Gerbillus latasti
Gerbillus mackillingi
Gerbillus mauritaniae
Gerbillus mesopotamiae
Gerbillus muriculus
Gerbillus nancilus
Gerbillus nanus
Gerbillus occiduus
Gerbillus perpallidus
Gerbillus poecilops
52 11- 39-
13 41
52 8 42
58 22 34
58 20 36
72 6 64
72 6 64
No data
74 20- 44
28 52
No data
No data
No data
No data
No data
54 ? ?
52 10- 36
14 40
52 8 42
52 8 42
52 10 40
40 38 0
40 34 4
40 34 4
No data
ISM mA,mM Pakistan;21,23,
12 (7:322)
? ? Egypt; 57(M includes
sex chromosomes)
ISM sA Morocco; 21
ISM M Morocco; 21
IM mM Morocco; 20
ISM mM Morocco; 20
ISM IM Morocco; 21
- ISM A
ISM ISM
_ 9
IM SA
IM SA
ISM sA
mM mM
ISM sM
ISM sM
Tun i s i a; 15
Algeria; 26
Israel; 56(M includes
sex chromosomes)
Morocco;Iran; 21; 23
Tunisia; 15
Jordan; this paper
Morocco; 20
Egypt; 21
Egypt; 58, 59
Appendix A. Continued
103
Gerbillus pulvinatus
Gerbillus pusillus
Gerbillus pyramidum
Gerbillus riggenbachi
Gerbillus rosalinda
Gerbillus ruberrimus
Gerbillus syrticus
Gerbillus watersi
Meriones chengi
Meriones crassus
Meriones hurrianae
Meriones libycxis
(incl. erythrourcus)
Meriones meridianus
Meriones persicus
62
34
40
38
40
40
40-
No
No
No
No
No
No
60
60
60
40
44
44
44
44
50
50
50
42
42
42
NF=84
18
36
36
36
14
2
0
2
7
mA
7
ISM
IM
•66 variable
data
data
data
data
data
data
10
12
12
36
30
30
30
26
26
26
34
34
34
48
46
48
2
12
12
12
22
22
22
6
6
6
ISM
ISM
ISM
ISM
IA
IA
IA
IM
IM
IM
ISM
ISM
ISM
7
SM
7
SM
IM
mSM
7
mM
SM
sSM
mSM
mSM
SA
var
sSM
mSM
7
mSM
Ethiopia; 13
Somalia; 4
Algeria; 24, 25, 56
Egypt; 21, 57, 58, 59
Tunisia; 15
Senegal; 14
Sinai/Israel; 56, 61
Egypt, Iran; 35
Iran; 1
Jordan; this paper
Iran; 35
25
USSR; 53
Transcaucasus; 18, 19
Iran; 35, 12(5:226), 1
Volga;38,17,53,54
variable Russia; 16
sSM Mongolia; 36, 39
Iran; 29
Iran; 2
Transcaucasus; 53, 54
Appendix A. Continued
104
Meriones
Meriones
Meriones
Meriones
rex
shawi
tamariscinus
tristrami
No
44
44
44
40
40
72
72
72
72
data
32
30
30
36
36
0
0
6-
16
8-
10
12
12
2
2
70
70
54-
64
51-
7
ISM
ISM
IM
IM
7
ISM
ISM
ISM
7
mSM
7
sSM
sSM
7
7
sSM
sSM
29
Egypt; 12
Jordan; this paper
USSR; 53, 54
Mongolia; 39
29
Iran; 1, 2
Transcaucasus; 38,19
Armenia S> Azerbaijan
19 62
72 4 66
72 0-6 64-
70
Meriones vinogradovi 44 32 10
44 32 10
44 32 10
Meriones unguiculatus 44 32 10
ISM mM
7
7
IM
ISM
7
7
SM
mSM
Meriones zarudayi
Microdillus peeli
Psammomys obesus
Psammomys vexillaris
44 32 10 ISM sSM
No data
No data
48 28 18 ISM sM
48
48 28 18 IM mM
No data
19, 53
Israel; 61
Jordan; this paper
No locality; 27
Iran; 35
USSR; 53,54,38,39
(Domestic);35,12
(6:274), this paper
Mongolia; 16, 53
(captive); 12(4:170)
46
Jordan; this paper
Appendix A. Continued
105
Rhombomys opimus
Sekeetamys calurus
Tatera afra
Tatera boehmi
Tatera brantsii
Tatera guineae
Tatera hopkinsoni
Tatera inclusa
Tatera indica
Tatera kempi
Tatera leucogastor
Tatera nigricauda
Tatera cf. nigrita
Tatera robusta
40 36 2 ISM SM
38 34 2 IM sA
38 32- ? ? ?
36
38 34 2 ISM ?
44 NF=70-76 ? ?
44 24 20 ISM mM
No data
44 NF=70-76 M M
44 24 20 ISM mM
50 16 32 ISM A
48 16 30 IA A
No data
72
72 NF=80
68 16 50 IM sA
36 22 14 ISM mSM
42 MF=72 M ?
40 28 10 mSM ISM
40 28 10 ISM sSM
40 32 6 ISM mSM
48 16 30 ISM mA
48 16 30 ISM mA
46 20 24 ISM mSM
Mongolia; 53
Egypt; 57, 58, 59
Sinai; 56(M includes
sex chromosomes)
Sinai; this paper
S. Africa; 27
S. Africa; this paper
S. Africa; 27
S. Africa; this paper
Upper Volta; 34
Upper Volta; 34
44
25
India; 60
C. Afr. Rep.; 34
South Africa; 27, 30
South Africa; 11
S. Africa, Namibia;
This paper
Ethiopia; 32
Upper Volta; 34
C. Afr. Rep., Chad; 47
(X polymorphic)
Upper Volta; 34
106
Appendix A. Continued
Tatera valida 52 14 36 ISM ? Senegal; 32
Taterillus arenarius 30 8 20 IM ? Mauritania; 32
(as T. nigeriae)
Taterillus congicus 54 12 40 ISM ? C. Afr. Rep.; 34
54 Chad; 50
54 ISM sSM C. Afr. Rep.; 10
Taterillus emini (see T. harringtoni)
Taterillus gracilis 36,37 10 24 IM SM,M Senegal; 33(Aut. poly
morphism in addition to
XY1Y2 system)
36,37 8 26 IM mSM,M Upper Volta; 34
36 ISM ? Senegal; 51
see also T. pygarus
Taterillus harringtoni 44 22 20 ISM ? Ethiopia; 32 (=emini)
44 C. Afr. Rep.; 10
44 18 26 ISM mSM Kenya; 40
Taterillus lacustris 28 18 8 ISM mSM Cameroon; 50
Taterillus nigeriae No data (see T. arenarius)
Taterillus pygargus 22,23 20 0 ISM SM,SM Senegal; 32,33 (Auto.
polymorphism in addition
to XY1Y2 system)
107
Appendix A. Continued
References: 1. Benazzou et al. (1982); 2. Benazzou et al. (1982b); 3. Benazzou et al. (1984); 4. Capanna and Merani (1981); 5. Cockrum et al. (1976); 6. Cockrum et al. (1977); 7. Cohen et al. (1971); 8. Ford and Hamerton (1956); 9. Gamperl and Vistorin (1980); 10. Genest and Petter (1973); 11. Gordon and Rautenbach (1980); 12. Hsu and Benirschke (1967-1971); 13. Hubert (1978); 14. Hubert and Boehme (1978); 15. Jordan et al. (1974); 16. Korobicyna (1969); 17. Korobicyna (1974); 18. Korobicyna (1975); 19. Korobitsyna and Korablev (1980); 20. Lay (1975); 21. Lay et al. (1975); 22. Lay and Nadler (1969); 23. Lay and Nadler (1975); 24. Matthey (1952); 25. Matthey (1953); 26. Matthey (1954a); 27. Matthey (1954b); 28. Matthey (1954c); 29. Matthey (1957); 30. Matthey (1958); 31. Matthey (1968a); 32. Matthey (1969); 33. Matthey and Jotterand (1972); 34. Matthey and Petter (1970); 35. Nadler and Lay (1967); 36. Nadler et al. (1969); 37. Nevo (1982); 38. Orlov (1969); 39. Orlov et al. (1978); 40. Robbins (1973); 41. Robbins (1974); 42. Robbins (1977); 43. Robbins and Baker (1978); 44. Sachs (1952); 45. Schlitter et al. (1985); 46. Smith et al. (1966); 47. Tranier (1974a); 48. Tranier (1974b); 49. Tranier (1976); 50. Tranier et al. (1974); 51. Viegas-Pequignot et al. (1982); 52. Viegas-Pequignot et al. (1984); 53. Vorontsov and Korobitsina (1969); 54. Vorontsov and Korobicyna (1970); 55. Wahrman et al. (1983); 56. Wahrman and Zahavi (1955); 57. Wassif et al. (1969); 58. Wassif (1977); 59. Wassif (1981); 60. Yosida (1981); 61. Zahavi and Wahrman (1957).
APPENDIX B
Specimens Examined
Desmodillus auricularis. NAMIBIA: Keetmanshoop Distr., Farm Welverdiend, 88 km E Koes (2 males, 1 female); Keetmanshoop Distr., 5 km NE Keetmanshoop (1 female); Maltahohe Distr., Zwartmodder 101, 70 km W Maltahohe (2 females); SOUTH AFRICA: Cape Prov., Farm Kamalboom, 18 km NE Marydale (1 female); Cape Prov., Farm Leelykstaat, 31 km NE Marydale (1 ).
Gerbillurus paeba. NAMIBIA: Keetmanshoop Distr., Farm Welverdiend 328, 17 km N, 88 km E Koes (3 males, 3 females); Keetmanshoop Distr., 6 km N Bethani (1 male, 1 female, 1 ?); SOUTH AFRICA: Cape Prov., Augrabies Falls National Park (1 female); Cape Prov., Farm Leelykstaat, 31 km NE Marydale (1 female); Cape Prov., Farm Kamalboom, 18 km NE Marydale (1 female, 2??); Cape Prov., Algeria Forestry Station (1 female).
Gerbillurus vallinus. NAMIBIA: Keetmanshoop Distr., 5 km NE Keetmanshoop (1 male); Keetmanshoop Distr., 6 km N Bethami (2 males, 1 female, 1 ?).
Gerbillus dasyurus. JORDAN: Al Ghor, Ghor Nimrin, near King Husain Bridge (1 male); Al Azraq, Lava Rocks South of Azraq ed Druz (4 males, 7 females); Southern Prov., Aqaba, Wadi E Marin Research Station (1 male).
Gerbillus nanus. JORDAN: Al Azraq Prov., Ain Al Atmash (1 female); Southern Prov., Aqaba, Wadi E Marine Research Station (1 male).
Meriones crassus. JORDAN: Azraq Prov., Al Azraq, 5 km W Azraq (1 male); EGYPT: Sinai Gov., Al Tor (1 male, 1 female, born in captivity).
Meriones shavi. JORDAN: Amman Gov., Al Halabat (1 male); Azraq Prov., Shawmari Wildlife Reserve, 6 km S Azraq (1 female); Azraq Prov., Azraq, Ain Al Atmash (1 male); Azraq Prov., 5 km W Azraq (2 females).
Meriones tristrami. JORDAN: Amman Gov., Al Muwaqqar, 14 mi E Amman (1 male, 1 female); Al Ghor, Ghor Nimrin, near King Hussain Bridge (2 males); Northern Gov., 7 mi E Irbid on Irbid-Mafraq Highway (3 males, 5 females).
108
109
Meriones unguiculatus. Domestic Mongolian Jird baught at pet store (1 female).
Psammomys obesus. .JORDAN: Amman Gov., Al Muwaqqar, 14 mi E Amman (2 males, 3 females); Al Halabat (1 male, 1 female).
Sekeetamys calurus. EGYPT: Sinai Gov., El Tor (2 females, born in captivity).
Tatera afra. SOUTH AFRICA: Cape Prov., 2 km NW Klapmuts (1 male, 2 females, 2 ?); Bredasdrop (3 females, 1 male).
Tatera leucogastor . NAMIBIA: Mariental Dist., Hardap Dam (1 male); Maltahohe Dist., Zwartmodder 101, 70 km W Maltahohe (1 male); SOUTH AFRICA: Traansvaal Prov., Lanner's Gorge, Kruger National Park (4 males).
Tatera brantsii. SOUTH AFRICA: Cape Prov., Farm Leelykstaat, 31 km NE Marydale (2 males, 2 females); Transvaal Prov., Nigel Municipal Park (1 male, 1 female).