MAZIN BUTROS HANNA QUMSIYEH, B.S., M.S. A DISSERTATION. IN. ZOOLOGY ...... John Wiley and Sons, New York, xii+686 pp. Chaline, J., P. Mein, and F.
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
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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. II. III. IV.
INTRODUCTION
1
METHODS AND MATERIALS
8
RESULTS
15
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
B.
Specimens Examined
99 108
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 5. The three types of heterochromatic additions in
23
Gerbillurus paeba
24
6. G-banded chromosomes of Gerbillurus vallinus . .
25
7. Comparison of haploid complements of Tatera leucogastor, T. brantsii, and T. afra 8. G-banded karyotype of a female Desmodillus auricularis 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
26 27
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 23. Tree for the Tatera/Gerbillurus group 24. The most parsimonious tree for the Meriones group 25. Tree for the two Gerbillus species examined 26. Histogram to illustrate distribution of diploid numbers in the family Gerbillidae 27. Tree for the Tatera/Gerbillurus group to illustrate change in diploid numbers by fissions and fusions
VI
77 78 79 80 81
82
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 welldefined 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: 2; 1,2,
1/2,
linkage group 1 fused with linkage group
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
4
11
13
6 15
8
10
17
19
ft«
I
• «
12 21
14
16
18
23
25
27
u 26
22
20
*
28
29
24
: i
35
I
32
30
33
31
Figure 1. G-banded karyotype of Tatera l e u c o g a s t o r . This karyotype was used to i d e n t i f y and number proposed homologous segments as they r e l a t e to a l l other species examined.
14
Character States
- • f - erJ -I v . . 1 2 3 4 5 6 7 8 9
Character State Tree
3| 1I
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 heterochromatic 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. metacentric.
The X is a large
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 paeba. Numbers in subsequent figures numbers for Tatera
chromosomes of Gerbillurus this figure and all refer to the standard 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
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r
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1
16
18
22
24
8
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14
9
26
6
3
13
25
19
7
Figure 6. G-banded chromosomes of Gerbillurus vallinus.
20
^Y
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
8
29 25
2prox
13
2dist
14
19
21
4prox
27
15
17
16
18 23
UH
4«
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18
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16
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24
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10
25 26
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30
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6
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22
14
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n
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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 »•
•%
B
Vi?^. \
aCGt /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
1
31
3
13
H
•
*
8 11 •
«
29 17
33
2dist
14
10
4prox
18
• k
• •• 1
Hi (19/20)1 5
12
6
15
V 27 28
16
30
23
4dist
21
25 >
2 I 22
26
If
»'
? 9 24
7
2prox
9
X
Figure 13. G-banded chromosomes of Sekeetamys calurus.
33
6
32
1 -•.
*•••
8" 13
(19/20)i i
•^1 «!
^..'
14 25
29 23
27 28
i>-
5!*/ f
33
2dist 4dist
•V-
1" 12
9 17
4prox
*.-.
^m
'-3,^1 11 21
7
4Q * * ^
30
3
18 1
4»
*f' 1
26
4^^ Sir ^-i^^'lis 2
10
17 ' * 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
14
1
2
4
4
2
1
2
2
1
1
2
2
2
1
?
42
T a b l e 1 . Continued Species Char.
A
B
C
D
E
F
G
H
I
15/16
?
?
1
1
1
1
4
1
1
17
1
2
1
1
1
1
1
1
18
1
2
1
1
1
1
1
19/20
7
7
1
1
1
1
21/22
2
2
1
1
1
1
J
K
L
M
N
O
P
1
1
2
2
1
1
3
1
2
1
1
1
3
2
2
1
1
2
1
1
1
3
2
2
2
1
4
3
3
6
5
8
1
1
1
1
1
3
3
1
1
1
3
?
23/24
2
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
25/26
2
2
1
1
1
1
3
1
1
1
1
1
1
1
2
7
29
1
1
2
2
2
3
9
5
7
1
8
7
7
6
1
4
30
1
1
1
1
1
3
1
2
2
4
4
2
2
2
1
1
31
1
2
1
1
1
3
1
1
4
1
7
1
5
6
2
8
32
6
6
1
1
1
3
1
1
4
1
1
5
4
4
2
7
33
1
•
1
1
1
2
1
1
1
1
1
4
1
3
1
1
X
6
5
2
2
2
3
3
1
7
9
9
4
4
4
8
8
Y
8
9
1
2
2
3
3
4
5
6
6
7 •
7
7 •
7
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
I
1
1/2
2p
2
2d
1/30
1+H
1/?
2/1
2/31
2i?
2i
2p
(2p)i
2
2i?
2/1
2/31
2i
2d
2d/l
3
3
3/4p
3/4 (3/4pr)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
6
6
6/5
3/2d
6 l/2di
1/29
1/ (l/?)i {19/20)i
2di/32 2di/3
(3/?)i
5/ 5i (27/28) 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
9
9
9/10
9i/31
10
10
10/9
9/(27/ 28)i 10/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
9/10+ 9i H+C 10+H+ 10+H+ E/9 E
10/6
10/E
8 part/ 8part 6
44 Table 2. Continued
Linkage Groups
1
Character states 3 4 5
2
14
14
14/13 (13/14)i
15/16
15/16 15,16
(15/
(15/
16)+E 17
17/18
17
17/12
18
18/17
18
18/4d
19/20
19/20 19,20
21/22
21/22
i
23/24
23/24
i
25/26 29
25/26 i 29 29+E
30
30
31
i
16)-E
i/4d
i/6
i/1
i+E
25,26 29/32
i
29/E
29/1
i'29/:
30i
30/1
30i(partial)
31
31 part.
31/2
31/?
31/9
31/33
31/4p
32
32
32+E
32/29
32/8
32/2d
32i
33
33
33+H
33/31
33/?
X, Y
See Text for these linkage groups
i/11
21,22
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
Gerbillus Group
•81 •132 •142 •25/261 122 112
•89 •131 141 111 121
11 2 p i 2 d i 32 4p2 4 d i 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 r e e stems for the G e r b i l l i d a e and the outgroups. The t r e e s for the t h r e e recognized groups of Gerbillidae are shown in F i g s . 23, 24, and 25. See text for discussion.
Gerbillurus vallinus
Gerbillurus paeba
V
78
Tatera Tatera leucogastor afra
Tatera brantsii
13 .2p3 •2d^ •75 •85
^31 .4p4 :5i •61
.93 •293
L7I
•83 :9i
303 313 323 332
.10^ :i3i rl4i .19/202
5 21/223 -25/263 •299
I
103 X3 52 62 92 132 142 33
4p3 4d2 102 25/261 292
Figure 2 3 . Tree for the T a t e r a / G e r b i l l u r u s group. T h i s 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 ) .
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LIST OF REFERENCES Arnold^ E.N. 1981.Estimating phylogenies at lower taxonomic levels. Z. Zool. Syst.Evolutionforsch., 19: 1-35. Ashley, T., M. J. Moses, and A. J. Solari. 1981. Fine structure and behavior of a pericentric inversion in the sand rat, Psammomys obesus. Jour. Cell Sci. 50: 105-119. Atallah, S.I. (1977)-1978. Mammals of the Eastern Mediterranean region; their ecology, systematics and zoogeographical relationships. Saugetirk. Mitt. 25: 241-320, 26: 1-50. Baker, R. J. 1984. A sympatric, cryptic species of mammal: A new species of Rhogeesa (Chiroptera: Vespertilionidae). Syst. Zool., 33: 178-183. Baker, R. J. and R. A. Bass. 1979. Evolutionary relationship of the Brachyphyllinae to glossophagine genera Glossophaga and Monophyllus. J. Mamm., 60: 297-306. Baker, R.J., and J.W. Bickham. 1980. Karyotypic evolution in bats: Evidence of extensive and conservative chromosomal evolution in closely related taxa. Syst. Zool., 29: 239-253. Baker, R. J. and J. W. Bickham. 1985. Matthayian speciation: speciation by centric fusions. Unpublished MS. Baker, R.J. and M.B. Qumsiyeh. 1985. Methods in Chiropteran chromosomal studies. I_n Ecological and behavioral methods for the study of bats (Thomas H. Kunz, ed.). Smithsonian Inst. Press, In Press. Baker, R. J., R. K. Barnett, and I. F. Greenbaum. 1979. Chromosomal evolution in grasshopper mice (Onychomys: Cricetidae). J. Mamm., 60: 297-306. Baker, R.J., R.A. Bass, and M.A. Johnson. 1979. Evolutionary implications of chromosomal homology in four genera of stenodermatine bats (Phyllostomatidae, Chiroptera). Evolution, 33: 220-226. 84
85 Baker, R. j., j. w. Bickham, and M. L. Arnold. 1985. Chromosomal evolution in Rhogeesa (Chiroptera: Vespertilionidae): Possible speciation by centric fusions. Evolution, 39: 233-243. Baker, R. j., B. F. Koop, and M. W. Haiduk. 1983. Resolving systematic relationships with G-bands: A study of five genera of South American cricetine rodents. Syst. Zool., 32: 403-416. Baker, R.J., M.W. Haiduk, L.W. Robbins, A. Cadena, and B. F. Koop. 1982. Chromosomal studies of South American bats and their systematic implications. Pp. 303-327 In: Mammalian Biology in South America (M.A. Mares and H.H. Genoways, eds.). Pymatuning laboratory of Ecology, Vol. IV, Pymatuning, Pennsylvenia, xii+539 pp. Baverstock, P. R., M. Gelder, and A. Jahnke. 1982. Chromosome evolution in Australian Rattus G-banding and hybrid meiosis. Genetica, 60: 93-103. Baverstock, P. R., C. H. S. Watts, M. Gelder, and A. Jahnke. 1983. G-band homologies of some Australian rodents. Genetica, 60: 105-117. Benazzou, T., E. Viegas-Pequignot, F. Petter, and B. Dutrillaux. 1982. Phylogenie chromosomique de quatre especes de Meriones (Rongeur, Gerbillidae). Ann. Genet., 25(1): 19-24. Benazzou, T., E. Dutrillaux. Gerbillidae gracilis et 212-217.
Viegas-Pequignot, F. Petter, and B. 1982. Phylogenie chromosomique des Etude de six Meriones, de Taterillus de Gerbillus tytonisT Ann. Genet., 25:
Benazzou, T., E. Viegas-Pequignot, M. Prod'Homme, M. Lombard, F. Petter, and B. Dutrilaux. 1984. Phylogenie chromosomique des Gerbillidae III. Etude d'especes des genres Tatera, Taterillus, Psammomys, et Pachyuromys. Ann. Genet., 27: 17-26. Benirschke, K., N. Malouf, R. J. Low and H. Heck. 1965. Chromosomal complement: Difference between Equus caballus and Equus przewalskii, Poliakoff. Science, 148:382-383.
86 Bickham, J. w. 1979. Chromosomal variation and evolutionary relationships of vespertilionid bats. J. Mamm., 60: 350-363. Bickham,. J. w. and R. J. Baker. 1976. Chromosomal homology and evolution of emydid turtles. Chromosoma, 54: 201-219. . 1979. Canalization model of chromosomal evolution. In Models and methodologies in evolutionary theory (J. H. Schwartz and H. B. Rollins, eds.). Bull. Carnegie Mus. Nat. Hist., No. 13, pp. 70-84. Bruere, A. N. and P. M. Ellis. 1979. Cytogenetics and reproduction of sheep with multiple centric fusions (Robertsonian translocations). J. Reprod. Fert., 57: 363-375. Capanna E. 1982. Robertsonian numerical variation in animal speciation: Mus musculus, an emblematic model. Pp. 155-177 In C. Baricozzi (ed.). Mechanisms of speciation. Liss, New York. Capanna, E. and M. S. Merani. 1981. Karyotypes of Somalian rodent populations. 2. The chromosomes of Gerbillus dunni (Thomas, 1904), Gerbillus pusillus Peters, 1878 and Ammodillus imbelis (de Winton] 1898) (Cricetidae, Gerbillinae). Monitore Zool. Ital. (Suppl.) 14: 227-240. Carleton, M. D., and G. G. Musser. 1984. Chapter 11: Muroid rodents. Pp 289-379 in Orders and Families of Recent Mammals of the World"Ts. Anderson and J. Knox Jones, Jr., eds.). John Wiley and Sons, New York, xii+686 pp. Chaline, J., P. Mein, and F. Petter. 1977. Les grandes lignes d'une classification volutine des Muroidea. Mammalia, 41: 245-252. Chaworth-Musters, J. L. and J. R. Ellerman. 1947. A revision of the genus Meriones. Proc. Zool. Soc. London, 117:478-504.
87 Cockrum, E. L., T. C. Vaughan, and D. J. Vaughan. 1976. A review of North African short-tailed gerbils (Dipodillus) with description of a new taxon from Tunisia. Mammalia, 40: 313-326. Cockrum, E. L., T. C. Vaughan, and D. J. Vaughan. 1977. Gerbillus andersoni de Winton, a species new to Tunisia. Mammalia, 40: 467-473. Cohen, M., C. Hastings, and C. F. Nadler. 1971. Random inactivation in interspecific hybrids of Meriones libycus ( ) X Meriones shawi ( ) (Rodentia: Gerbillinae). Experientia, 27: 1084-1086. Committee for standardization of chromosomes of Peromyscus. 1977. Standardized karyotype of deer mice, Peromyscus (Rodentia). Cytogenet. Cell Genet., 19: 38-43. Corbet, G. B. 1978. The mammals of the Palaearctic region. The British Museum (Natural History) and Cornell University Press, London and Ithaca, 314 pp. Corbet, G.B. and J.E. Hill. 1980. A world list of mammalian species. The British Museum (Natural History) and Cornell University Press, London and Ithaca, viii+226 pp. Crisci, J. V. and T. F. Stuessy. 1980. Determining primitive character states for phyllogenetic reconstruction. Syst. Bot., 5: 112-135. Dutrilaux, B. 1979. Chromosomal evolution in primates: Tentative phylogeny from Microcebus murinus (Prosimian) to man. Hum. Gen., 48: 251-314. Elder, F. F. B. and S. Pathak. 1980. Light microscopic observations on the behavior of silver-stained trivalents in pachytene cells of Sigmodon fulviventer (Rodentia, Muridae) heterozygous for centric fusion. Cytogenet. Cell. Genet., 27: 31-38. Ellerman, J. R. 1941. The families and genera of living rodents. British Museum (Natural History), London, Vol. 2, xii+690 pp. Engelman, G. F. and E. 0. Wiley. 1977. The place of ancestor- descendant relationships in phylogeny reconstruction. Syst. Zool., 26: 1-11.
88 Estabrook, G. F. .1977. Does common equal primitive? Syst. Bot., 2: 36-42. Farris, J. S. 1970. Methods for computing Wagner trees. Syst. Zool., 19: 83-93. . 1978. WAGNER78 (Phylogenetic progam package). Available through State University of New York, Brookline, New York. Ford, C. E. and J. L. Hampton. 1956. Chromosomes of five rodent species. Nature, 177: 140-141. Gamperl, R. and G. Vistorin. 1980. Comparative study of Gand C-banded chromosomes of Gerbillus campestris and Meriones unguiculatus (Rodentia, Gerbillinae). Genetica, 53: 93-97. Genest, H. and F. Petter. 1973. Les Taterillus de Republic Centrafricaine (Rongeurs, Gerbillides). Mammalia, 37: 66-75. Gordon, D. H. and I. L. Rautenbach. 1980. Species complexes in medically important rodents: Chromosome studies of Aethomys, Tatera and Saccostomus. (Rodentia: Muridae, Cricetidae). South Afr. J. Sci., 76: 559-561. Gropp, A. and H. Winking. 1972. Robertsonian chromosomal variation and identification of metacentric chromosomes in feral mice. Chromosoma, 39: 265-288. Gustavsson, I. and C. 0. Sundt. 1969. Three polymorphic chromosome systems of centric fusion type in a population of Manchurian sika deer (Cervus nippon hortilarum Swinhoe). Chromosoma, 28: 245-254. Haiduk, M.W., and R.J. Baker. 1982. Cladistical analysis of the G-banded chromosomes of nectar-feeding bats (Glossophaginae: Phyllostomidae). Syst. Zool. 31: 252-265. Haiduk, M. W., R. J. Baker, L. W. Robbins, and D. A. Schlitter. 1981. Chromosomal evolution in African Megachiroptera: G- and C-band assessment of the magnitude of change in similar standard karyotypes. Cytogenet. Cell Genet., 29: 221-232.
89 Haim, A. and A. Tchernov. 1974. The distribution of myomorph rodents in the Sinai peninsula. Mammalia, 38: 201-223. Hall, w. P. 1973. Comparative populations cytogenetics, speciation, and evolution of the iguanid lizard genus Seeloporus. Ph.D. dissertation. Harvard Univ., 193 pp. Hansen, S. 1975. A case of centric fusion in man. Humangenetik, 26: 257-259. Harrison, D. L. 1972. The mammals of Arabia, Vol. 3, Ernest Benn Limited. London, xvii+670 pp. Heptner, V. G. 1933. Notizen uber die Gerbillidae (Mammalia, Rodentia) VI> Uber die Einteilung der Gerbillidae. Zool. Anz. 102(3/4): 1940. Gerbil fauna of Iran and geographical characteristics of Asia Minor-Aphghanistan countries. Nov. Mem. Mosk. Obstich. Ispyl. Prirody, 20 (in Russian). Hermann, B. 1973. Donnees nouvelles sur 1'Assortiment chromosomique de Meriones tristrami Thomas (Rodentia: Gerbillidae). Genetica, 44: 579-587. Honacki, J. H., K. E. Kinman, and J. W. Koeppl. 1982. Mammal species of the world: A taxonomic and geographic reference. Allen Press, Inc. and the Association of Systematic Collections, Lawrence, ix+694 pp. Hsu, T. C. and K. Benirschke. 1967-1971. An atlas of mammalian chromosomes. Springer Verlag, N.Y. Hubert, B. 1978. Caryotype de Gerbillus pulvinatus Rhoads, 1896 (Rongeurs, Gerbillides) de la vallee I'Omo (Ethiopie). Mammalia, 42: 225-228. Hubert, B. and W. Bohme. 1978. Karyotype of Gerbillus pyramidum I. Geoffrey (Rodentia, Gerbillidae) from Senegal. Bull. Carnegie Mus. Nat. Hist., 6: 38-40. Imai, H. T. and R. H. Crozier. 1980. Quantitative analysis of directionality in mammalian karyotype evolution. Am. Nat., 116(4): 537-569.
90 John B. 1981. Chromosome change and evolutionary change: a critique. Pp. 23-51 ni W. R. Atchley and D. Woodruff (eds.) "Evolution and speciation essays in honor of M. J. D. White." Cambridge Univ. Press, Cambridge, 436 pp. Jong, R. de. 1980. Some tools for evolutionary and phylogenetic studies. Z. Zool. Syst. Evolution-forsch., 18: 1-23. Jordan, R. G., B. L. Davis, and H. Baccar. 1974. Karyotypic and morphometric studies of Tunisian Gerbillus. Mammalia, 38: 667-680. Kato, H., T. Sagai and T. H. Yosida. 1973. Stable telecentric chromosomes produced by centric fission in Chinese hamster cells in vitro. Chromosoma, 40:183-192. Kluge, A. G. and J. S. Farris. 1969. Quantitative phyletics and the evolution of Anurans. Syst. Zool., 18: 1-32. Koop, B. F., R. J. Baker, and J. T. Mascarello. 1985. Cladistical analysis of chromosomal evolution within the genus Neotoma. Occas. Papers Mus., Texas Tech Univ., Koop, B. F., R. J. Baker, M. W. Haiduk, and M. D. Engstrom. 1985. Cladistical analysis of the primitive G-band sequences for the karyotype of the ancestor of the Cricetidae complex of rodents. Genetica, 64: 199-208. Korobicyna, K. V. 1969. (Intraspecific variability of chromosomes of some species of gerbils (Meriones, Gerbillinae, Cricetidae, Rodentia)). Pp. 117-120 Ln N. N. Voroncov (ed.) "The mammals (evolution, taxonomy, fauna)". Acad. Sci. USSR, Novosibirsk. (In Russian). . 1974. (Analysis of the interpopulation karyotype variability in Meriones meridianus with special reference to the resistance against the plaque microbe). Zool. Z., 53: 1066-1069. (in Russian with English summary).
91 Korobitsyna, K. V. and V. P. Korablev. 1980. The interspecific autosome polymorphism of Meriones tristrami Thomas (Gerbillinae, Cricetidae, Rodentia). Genetica, 52/53: 209-221. Lay, D. M. 1972. The anatomy, physiology, functional significance and evolution of specialized hearing organs of Gerbilline rodents. J. Morph., 138: 41-120. . 1975. Notes on rodents of the Genus Gerbillus (Mammalia: Muridae: Gerbillinae) from Morocco. Fieldiana Zool., 65(8): 89-101. . 1983. Taxonomy of the genus Gerbillus (Rodentia: Gerbillinae) with comments on the applications of generic and subgeneric names and an annotated list of species. Z. Saugetierk., 48: 329-354. Lay, D. M. and C. F. Nadler. 1969. Hybridization in the rodent genus Meriones. I. Breeding and ecological analysis of Meriones shawi ( )x Meriones libycus (o ) hybrids. Cytogenetics, 8: 35-50. Lay, D. M. and C. F. Nadler. 1975. A study of Gerbillus east of the Euphrates river. Mammalia, 39: 423-445. Lay, D. M., K. Agerson, and C. F. Nadler. 1975. Chromosomes of some species of Gerbillus (Mammalia Rodentia). Zeit. Saugetierk., 40: 141-150. Lee, M.R., and F.F.B. Elder. 1980. Yeast stimulation of bone marrow mitosis for cytogenetic investigations. Cytogen. Cell Gen., 26: 36-40. Maddison, W. P., M. J. Donaghue, and D. R. Maddison. 1984. Outgroup analysis and parsimony. Syst. Zool., 33: 83-103. Matthey, R. 1952. Chromosomes sexuels multiples chez un Rongeur (Gerbillus pyramidum Geoffrey). Arch. Klaus-Stift., Vererb. Forsch., 27: 163-167. 1953. Les chromosomes des Muridae. de Zool., 60: 225-283.
Rev. Suisse
92 1954a. Nouvelles donnees sur les formules chromosomique des Muridae. 1954b. Nouvelles recherches sur les chromosomes des Muridae. Caryologia, 6: 1-44. 1954c. Un cas nouveau de chromosomes sexuels multiples dans le genre Gerbillus (RodentiaMuridae-Gerbillinae). Experientia, 10:464-465. 1957. Cytogenie et taxonomie du genre Meriones Illiger (Rodentia-Muridae-Gerbillinae). Saugetierk. Mitt., 5: 145-150. 1958. Les chromosomes et la position systematique de quelque Murinae Africains (Mammalia-Rodentia). Acta Tropica, 15: 97-117. 1968. General survey of the chromosome numbers of Eutherian mammals. Mammalian Chromosome Newsletter, 9: 17. 1969. Chromosomes de Gerbillinae. Genres Tatera et Taterillus. Mammalia, 33(3): 522-528. Matthey, R. and parment de confondues (Rongeurs,
M. Jotterand. 1972, L'analyse du caryotype reconnaitre deux especes cryptiques sous le de Taterillus gracilis (TH) GerbillidaeTi Mammalia, 36: 183-209.
Matthey, R. and F. Petter. 1970. Etude cytogenetique et taxonomie de 40 Tatera et Taterillus provenant de Haute Volta et de Republic Centrafricaine (Rongeurs, Gerbillidae). Mammalia, 34: 585-597. Miller, G. S., Jr. and J. W. Gidley. 1918. Synopsis of the supergeneric groups of rodents. J. Wash. Acad. Sci., 8(13): 431-448. Nadler, C.F, and D.M. Lay. 1968. Chromosomes of some species of Meriones (Mammalia: Rodentia). Z. Saugetierk., 32: 287-291. Nadler, C. F., D. M. Lay and J. D. Hassinger. 1969. Chromosomes of three Asian mammals: Meriones meridianus (Rodentia: Gerbillinae) Spermophilopsis leptodactylus (Rodentia: Sciuridae) Ochotona rufescens (Lagomorpha: Ochotonidae). Experientia, 25: 774-775.
93 Nevo, E. 1982. Genie structure and differentiation during speciation in fossorial gerbil rodents. Mammalia, 46: 523-530. Ohno, S. 1973. Evolution by gene duplication. Springer Publ., Berlin, 227 pp. Ohno, S. 1984. Conservation of linkage relationship between genes as the underlying theme of karyological evolution in mammals. Pp. 1-11 rn A. K. Sharma and A. Sharma (eds.). Chromosomes in evolution of eukaryotic groups. Vol. II. CRC press. Olert, J. 1973. A case of chromosome dissociation in a shrew. Genet. Res. (Cambridge), 22: 323-324. Orlov, V. N. 1969. (The chromosome complement of some species of Meriones from Armenia.) Pp. 121-123 Ln N. N. Vorontsov (ed.) "The mammals (evolution, taxonomy, fauna)". Acad. Sci. USSR, Novosibirsk. (In Russian). Orlov, V. N., S. I. Radjabli, V. M. Malygin, N. Chotolchu, Ju. M. Kovalskaja, N. S. Bulatova, and M. I. Baskevic. 1978. (Karyotypes of the mammals from Mongolia). Geografija i dinamika rastitelnigo i zivotnogo mira MNR, Nauka, Moskva, pp. 149-164• (In Russian). Osborn, D. J. and I. Helmy. 1980. The contemporary land mammals of Egypt (including Sinai). Fieldiana Zool., No. 5, 579 pp. Patton, J. C. and R. J. Baker. 1979. Chromosomal homology and evolution in phyllostomatoid bats. Syst. Zool., 27: 449-462. Patton, J. C , R. J. Baker and H. H. Genoways. 1980. Apparent chromosomal heterosis in a fossorial mammal. Amer. Nat., 166: 143-146. Patton, J. L. and S. W. Sherwood. 1982. Genome evolution in pocket gophers (genus Thomomys). I. Heterochromatin variation and speciation potential. Chromosoma, 85: 149-162.
94 Pavlinov, I. Y. 1982. "Phylogeny and classification of the subfamily Gerbillinae". Byull. Mosk. Obshch. Ispyt. Prirody, Otd. Biol., 87(2): 19-31. In Russian, English translation No. 1598, Medical Zool. Dept., U.S. NAMRU-3, Cairo, Egypt. Peacock, W. J., E. S. Dennis, A. J. Hilliker, and A. J. Pryor. 1981. Differentiation of heterochromatin. Pp. 78-100 rn Evolution and speciation: Essays in honor of M. J. D. White. Cambridge University press, Cambridge, 436 pp. Petter, F. 1975. La diversite de Gerbillides. Biol., 28: 177-183.
Monogr.
Qumsiyeh, M. B. and R. J. Baker. 1985. G- and C-banded karyotypes of the Rhinopomatidae (Microchiroptera). J. Mamm., 66: 541-544. Robbins, C. B. 1973. Systematic status and karyotypic relationships of the genus Taterillus (Rodentia: Cricetidae) from Kenya. Mammalia, 37: 642-645. . 1974. Comments on the taxonomy of the West African Taterillus (Rodentia, Cricetidae) with a description of a new species. Proc. Biol. Soc. Washington, 87: 395-403. . 1977. A review of the African gerbils, Taterillus (Rodentia, Cricetidae). Pp. 178-194 In Advances in Modern Theriology, Nauka, Moscow (in Russian with English summary). Robbins, L. W., and R. J. Baker. 1981. An assessment of the nature of chromosomal rearrangements in eighteen species of Peromyscus (Rodentia: Cricetidae). Cytogenet. Cell Genet., 31: 194-202. Sachs, L. 1952. Polyploid evolution and mammalian chromosomes. Heredity, 6: 357-364. Schlitter, D. A. 1973. A new species of gerbil from South West Africa with remarks on Gerbillus tytonis Bauer and Niethammer 1959 (Rodentia: Gerbillinae). Bull. S. Calif. Acad. Sci.,. 72: 13-18.
95 Schlitter, D. A., I. L. Rautenbach, and C. G. Coetzee. 1985. Karyotypes of southern African gerbils. Genus Gerbillurus Shortridoe. 1942 (Rodentia: Cricetidae). Ann. Carnegie Mus. Nat. Hist., In Press. Simpson, G. G. 1945. The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist., Vol. 85, xvi+350 pp. Smith, A. G., D. B. Hackel, and K. Schmidt-Nielson. 1966. Chromosomes of the sand rat (Psammomys obesus). Canad. J. Genet. Cytol., 8: 756. Sokal, R. R. and P. H. A. Sneath. 1963. Principles of numerical taxonomy. W. H. Freeman Co., San Francisco, 359 pp. Solary, A. J. and T. Ashley. 1977. Ultrostructure and behavior of the achiasmatic, telosynaptic XY pair of the sand rat (Psammomys obesus). Chromosoma, 62: 319-336. Stangl, F. B., Jr. and R. J. Baker. 1984. Evolutionary relationships in Peromyscus: Congruence in chromosomal, genie, and classical data sets. J. Mammal., 65: 643-654. Stevens, P. F. 1980. Evolutionary polarity of character states. Annu. Rev. Ecol. Syst., 11: 333-358. Todd, N. B. 1967. A theory of karyotypic fissioning, genetic potentation and eutherian evolution. Mammalian Chromosomal Newsletter, 8: 268-279. . 1970. Karyotypic fissioning and canid phylogeny. J. Theor. Biol., 26: 445-480. Tranier, M. 1974a. Dimorphisme chromosomique dans une population de Tatera du sud du Tchad (Rongeurs, Gerbillidae). Mammalia, 38: 224-233. . 1974b. Polymorphism chromosomique multiple chez des Taterillus du Niger (Rongeurs, Gerbillides). C. R. Acad. Sci. Paris, serie D., 278: 3347-3350. . 1976. Originalite du caryotype de Gerbillus nigeriae (Rongeurs, Gerbillides). Mammalia, 39: 703-704.
96 Tranier, M., B. Hubert, and F. Petter. 1974. Taterillus de I'ouest du Chad et du nord du Cameroun (Rongeurs, Gerbillides). Mammalia, 37: 637-641. Viegas-Pequignot, E., T. Benazzou, B. Dutrillaux, and F. Petter. 1982. Complex evolution of sex chromosomes in Gerbillidae (Rodentia). Cytogenet. Cell Genet., 34: 158-167. Viegas-Pequignot, E., T. Benazzou, M. Prod'Homme, and B. Dutrillaux. 1984. Characterisation of a very complex constitutive heterochromatin in two Gerbillus species (Rodentia). Chromosoma, 89: 42-47. Vorontsov, N. N., and K. V. Korobitsina. 1969. The comparative karyology of the highest gerbils (genera Meriones and Rhombomys: Gerbillinae, Rodentia). Pp. 111-116 rn N. N. Vorontsov (ed.) "The mammals (evolution, taxonomy, fauna)". Acad. Sci. USSR, Novosibirsk. (In Russian). Voroncov, N. N., and K. Korobicyna. 1970. (Materials on comparative karyology of gerbillinae). Citologija, 12: 152-157. (In Russian with English summary). Wahrman, J. and R. Goitein. 1972. Hybridisation in aature between two chromsome forms of spiny mice. Chromosomes Today, 3: 228-237. Wahrman, J. and P. Gourevitz. 1973. Extreme chromosome variability in a colonising rodent. Chromosomes Today, 4: 399-424. Wahrman, J. and A. Zahavi. 1955. Cytological contributions to the phylogeny and classification of the rodent genus Gerbillus. Nature (London), 175: 600-602. Wahrman, J., C. Richler, E. Neufeld, and A. Friedmann. 1983. The origin of multiple sex chromosomes in the gerbil Gerbillus gerbillus (Rodentia: Gerbillinae). Cytogenet. Cell Genet., 35: 161-180. Wassif, K. 1954. The bushy-tailed gerbil, Gerbillus calurus Thomas of South Sinai. J. Mamm., 33: 243-248.
97 7 — • ^556» Studies on gerbils of the subgenus Dipodillus recorded from Egypt. Ain Shams Sci. Bull., 1: 173-194. Wassif, K., R.G. Lutfy, and S. Wassif. 1969. Morphological, cytological and taxonomical studies of the rodent genera Gerbillus and Dipodillus from Egypt. Proc. Egypt. Acad. Sci., no. 22, pp. 77-97. 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. Yosida, T. H. 1981. Chromosome polymorphism of the large naked-soled gerbil, Tatera indica (Rodentia, Muridae). Japanese J. Genet., 56: 241-248. Zahavi, A. and J. Wahrman. 1957. The cytotaxonomy, ecology and evolution of the gerbils and jirds of Israel (Rodentia: Gerbillinae). Mammalia, 21: 341-380.
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
Somalia; 4 (M includes
Brachiones przewalski
No data
Desmodilliscus breweri No data Desmodillus auricularis
52
?
?
M
M
South Africa; 27
52
28
22
IM
mM
South Africa;this paper
?
Egypt; 57
Dipodillus maqhrebi
No data
Dipodillus simoni
60
Dipodillus zakariai
8-
48- ?
10
50
60
0
58
IM
sSM
Egypt; 58, 59
60
8-
50
?
?
Tun i s i a; 5
10
50
No data
99
100 Appendix A. Continued
Gerbillurus paeba
36
South Africa; 30
36
34
0
mSM sA
S. Africa, Namibia; 45
36
34
0
mSM sA
S. Africa, Namibia; this paper
Gerbillurus setzeri
60
18
40
ISM sA
Gerbillurus tytonis
36
34
0
SM
36
34
0
mSM SA
Namibia; 45
60
22
36
IM
S. Africa,Namibia; 45
60
12- 38- ISM sA
S. Africa, Namibia;
20
This paper
Gerbillurus vallinus
Gerbillus agag
No data
Gerbillus amoenus
52
Namibia; 45
7
Namibia; 2
sA
46
9-
42- 7
10
43
52
8
44
ISM sA
Egypt; 58, 59
40
38
0
ISM sSM
Egypt; 57
40
38
0
ISM mSM
Egypt,Israel; 21
40
38
0
ISM sSM
Egypt; 58, 59
40
38
0
7
40
38
0
7
Gerbillus aquilus
38
36
0
ISM sM
Gerbillus bottai
No data
Gerbillus campestris
56
7
7
SM
SM
Algeria; 25
56
13- 41-
7
7
Egypt; 57
IM
mM
Egypt; 58, 59
Gerbillus andersoni (=allenbyi)
58
15
43
8
48
7
Egypt; 57 (M includes sex chromosomes)
7 7
Tunisia; 6 Israel; 56 Pakistan, Iran; 21, 23
101 Appendix A. Continued
56,
10- 44-
57,5£1 12
Gerbillus cheesmani
Gerbillus dasyurus
mM
sA
Morocco; 21
48
56
10
44
IM
56
14
40
ISM sSM
Tunisia; 15
38
34
2
IM
Iran; 21, 23
38
34
2
mSM SM
60 6-8
52- 7
sSM
sSM
7
54 60
6
52
Morocco; 9
Iran; 12 (7:320) Sinai; 56 (M includes sex chromosomes)
IM
60 9-10 50- 7
7
Sinai; 21, 23
7
Egypt; 57
SA
Jordan, Palestine; th
51 60
8-
46- IM
12
50
24
48
Gerbillus dunni
74
Gerbillus famulus
No data
Gerbillus gerbillus
paper ISM mM
Somalia; 4
42,43 ?
?
Algeria; 25,26 (Y1,Y2)
42,43 38-
ISM Y1Y2
?
40 42
Israel; 56(M includes sex chromosomes)
32
ISM ?
42,43 32
Morocco; 21
ISM Yl=sM Y2=sSM Sinai, Egypt; 21, 23
42,43 34
6
42,43 34- ?
ISM 2SM
Egypt; 58, 59
ISM 2A
Egypt; 57
Tunisia; 15
36 42,43 36
6
ISM ?
42,43 32
8
lA
sSM,sSM Egypt; 12 (7:321)
102 Appendix A. Continued
Gerbillus gleadoni
50,51 20
28
ISM mA,mM Pakistan;21,23, 12 (7:322)
Gerbillus henleyi
Gerbillus hesperinus
Gerbillus hoogstraali
52
11- 39- ?
?
Egypt; 57(M includes sex chromosomes)
13
41
52
8
42
ISM sA
Morocco; 21
58
22
34
ISM M
Morocco; 21
58
20
36
IM
mM
Morocco; 20
72
6
64
ISM mM
Morocco; 20
72
6
64
ISM IM
Morocco; 21
Gerbillus jamesi
No data
Gerbillus latasti
74
20- 44 - ISM A 28
Gerbillus mackillingi
No data
Gerbillus mauritaniae
No data
Tun i s i a; 15
52
Gerbillus mesopotamiae No data Gerbillus muriculus
No data
Gerbillus nancilus
No data
Gerbillus nanus
54
?
52
10- 36 _ 9
Israel; 56(M includes
14
40
sex chromosomes)
52
8
42
IM
SA
Morocco;Iran; 21; 23
52
8
42
IM
SA
Tunisia; 15
52
10
40
ISM sA
Jordan; this paper
Gerbillus occiduus
40
38
0
mM
Morocco; 20
Gerbillus perpallidus
40
34
4
ISM sM
Egypt; 21
40
34
4
ISM sM
Egypt; 58, 59
Gerbillus poecilops
No data
?
ISM ISM
mM
Algeria; 26
103 Appendix A. Continued
Gerbillus pulvinatus
62
NF=84
7
7
Ethiopia; 13
Gerbillus pusillus
34
18
14
mA
SM
Somalia; 4
Gerbillus pyramidum
40
36
2
7
7
Algeria; 24, 25, 56
38
36
0
ISM SM
Egypt; 21, 57, 58, 59
40
36
2
IM
Tunisia; 15
IM
40
Senegal; 14
40-•66 variable
Sinai/Israel; 56, 61
Gerbillus riggenbachi
No data
Gerbillus rosalinda
No data
Gerbillus ruberrimus
No data
Gerbillus syrticus
No data
Gerbillus watersi
No data
Meriones chengi
No data
Meriones crassus
60
10
48
ISM mSM
60
12
46
ISM
60
12
48
ISM mM
Jordan; this paper
Meriones hurrianae
40
36
2
ISM SM
Iran; 35
Meriones libycxis
44
7
Egypt, Iran; 35 Iran; 1
25
(incl. erythrourcus) 44
30
12
IA
sSM
USSR; 53
44
30
12
IA
mSM
Transcaucasus; 18, 19
44
30
12
IA
mSM
Iran; 35, 12(5:226), 1
50
26
22
IM
SA
Volga;38,17,53,54
50
26
22
IM
variable var
50
26
22
IM
sSM
42
34
6
ISM mSM
42
34
6
ISM
42
34
6
ISM mSM
Meriones meridianus
Meriones persicus
7
Russia; 16
Mongolia; 36, 39 Iran; 29 Iran; 2 Transcaucasus; 53, 54
104 Appendix A. Continued
Meriones rex
No data
Meriones shawi
44
32
10
44
30
12
ISM mSM
44
30
12
ISM
7
40
36
2
IM
sSM
USSR; 53, 54
40
36
2
IM
sSM
Mongolia; 39
72
0
70
7
7
72
0
70
ISM
7
72
6-
54- ISM sSM
16
64
8-
51- ISM sSM
Armenia S> Azerbaijan
19
62
19, 53
72
4
66
Israel; 61
72
0-6 64- ISM mM
Meriones tamariscinus
Meriones tristrami
72
7
7
29 Egypt; 12 Jordan; this paper
29 Iran; 1, 2 Transcaucasus; 38,19
Jordan; this paper
70 Meriones vinogradovi
Meriones unguiculatus
44
32
10
7
7
No locality; 27
44
32
10
7
7
Iran; 35
44
32
10
IM
SM
44
32
10
ISM mSM
USSR; 53,54,38,39 (Domestic);35,12 (6:274), this paper
44
32
Meriones zarudayi
No data
Microdillus peeli
No data
Psammomys obesus
48
28
10
ISM sSM
Mongolia; 16, 53
18
ISM sM
(captive); 12(4:170) 46
48 48 Psammomys vexillaris
28
No data
18
IM
mM
Jordan; this paper
105 Appendix A. Continued
Rhombomys opimus
40
36
2
ISM SM
Mongolia; 53
Sekeetamys calurus
38
34
2
IM
sA
Egypt; 57, 58, 59
38
32- ?
?
?
Sinai; 56(M includes sex chromosomes)
36
Tatera afra
2
Sinai; this paper
38
34
44
NF=70-76 ? ?
S. Africa; 27
44
24
mM
S. Africa; this paper
20
ISM ?
ISM
Tatera boehmi
No data
Tatera brantsii
44
NF=70-76 M
M
S. Africa; 27
44
24
20
ISM
mM
S. Africa; this paper
Tatera guineae
50
16
32
ISM
A
Upper Volta; 34
Tatera hopkinsoni
48
16
30
IA
A
Upper Volta; 34
Tatera inclusa
No data
Tatera indica
72
44
72
NF=80
68
16
50
IM
Tatera kempi
36
22
14
ISM mSM
C. Afr. Rep.; 34
Tatera leucogastor
42
MF=72
M
South Africa; 27, 30
40
28
10
mSM ISM
South Africa; 11
40
28
10
ISM sSM
S. Africa, Namibia;
25 sA
?
India; 60
This paper Tatera nigricauda
40
32
6
ISM mSM
Ethiopia; 32
Tatera cf. nigrita
48
16
30
ISM mA
Upper Volta; 34
48
16
30
ISM mA
C. Afr. Rep., Chad; 47 (X polymorphic)
Tatera robusta
46
20
24
ISM mSM
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 Taterillus emini Taterillus gracilis
ISM sSM
C. Afr. Rep.; 10
(see T. harringtoni) 36,37 10
24
IM
SM,M
Senegal; 33(Aut. polymorphism in addition to XY1Y2 system)
36,37 8
26
36
IM ISM
mSM,M Upper Volta; 34 ?
Senegal; 51
see also T. pygarus Taterillus harringtoni 44
22
20
ISM
?
44
Ethiopia; 32 (=emini) 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).
