ZoologicalJournal ofthe Linnean Society, 65 :26 1-280. With 15 figures
March 1979
The chromosomes of the hystricomorphous
family Ctenodactylidae (Rodentia:
TSciuromorpha)and their bearing on the
relationships of the four living genera
WILMA GEORGE
Lady Margaret Hall and Department of Zoology, Oxford
Acceptedfor pubbcalion November 1977
Karyotype studies support the view that modern genera of the family Ctenodactylidae originated in
Africa. Karyotype differences between the genera are less obvious than morphological differences
but coincide in relating Matsoutiera to Felovia and deriving this line from the Pectinator-like ancestor
which, in turn, was closely related to a Ctenodactylus ancestor. 43%of the chromosomes are standard
throughout the family; 25% seem to be very susceptible to fragmentation, translocation and
inversion. These changeable chromosomes are the only ones that show differences in their G-band
patterns. The ctenodactylid karyotype resembles caviomorph karyotypes in its NF, predominantly
metacentric chromosomes and in its nucleolar organiser, or marker, chromosomes.
KEY WORDS :- Ctenodactylidae - karyotype - evolution - Rodentia.
CONTENTS
. . . . . . . . . . . . . . . . . .
Introduction
Materials and methods
. . . . . . . . . . . . . .
Results
. . . . . . . . . . . . . . . . . . . .
Ctenodactylus gundi
. . . . . . . . . . . . . .
Ctenodactylus vali
. . . . . . . . . . . . . . . .
Pectinator spekei
. . . . . . . . . . . . . . . .
Massoutiera mzabi
. . . . . . . . . . . . . . . .
Felovia vae . . . . . . . . . . . . . . . . . .
Discussion
. . . . . . . . . . . . . . . . . . .
Comparisons of karyotypes in the living genera
. . . . . .
Patterns of karyotype change
. . . . . . . . . . .
Relationships of the ctenodactylid genera
. . . . . . . .
Relationships of the family
. . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . . . . . .
References
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26 1
262
263
263
265
266
268
269
270
270
274
275
277
278
279
INTRODUCTION
The family Ctenodactylidae, the gundis, has proved difficult to assign to any of
the rodent suborders. Simpson ( 1945) put them with a query as Hystricomorpha
or Myomorpha or Myomorpha incertae sedis and Wood ( 1955), also with a query,
made them a superfamily, Ctenodactyloidea, of the Sciuromorpha. Since then,
the finds of fossils have led authors to consider the ctenodactylids as having had a
separate familial existence since the Eocene, at which time they seem to have
0024-4082/79/030261-20/$02.00
26 1
0 1979 The Linnean Society of London
262
W. GEORGE
resembled the sciuravids (Dawson, 1964; Shevyreva, 1972 a, b) and would seem,
therefore, to be properly placed in some sciuromorphous or protrogomorphous
group (Wood, 1965).
Within the family, the problem of the relationships between the genera has
received little attention, except from Jaeger (1971), and yet this could have a
bearing on the interpretation of the origins of the family in either Africa or Asia.
Should all modern genera be derived from Moroccan Miocene fossils (Black,
1972; Jaeger, Michaux & David, 1973) o r should they come from a n ancestral
Pectinator, an immigrant from Asia?
Whatever opinions there are about the relationships of the Ctenodactylidae,
they are based on morphological criteria, mainly on the structure of the teeth,
skull and embryonic membranes (Tullberg, 1899; Lange, 1938; Ellerman, 1940;
Landry, 1957; Luckett, 1971).
An extensive study of the four living genera and five species of ctenodactylids
has been undertaken recently (George, 1974). Karyotype analysis was part of this
study. Before this, only Matthey ( 1956a) had reported on ctenodactylid
chromosomes. He reported 2n=40 for Ctenodactylus gundi and concluded that the
chromosomes showed some resemblance to those of Dipodidae.
MATERIALS A N D METHODS
Animals were caught at various times between 1969 and 1972. Ctenodactylus
gundi (Rothmann) came from Tunisia and C. vali (Thomas) from desert areas of
Algeria. Pectinator spekei (Blyth) came from the Danakil desert of Ethiopia;
Massoutiera mrabi (Lataste) came from Algeria and Felovia vae (Lataste) from Mali.
Living specimens were brought to England and the karyotype studies were
carried out on blood obtained from these animals bred in the wild.
Identification of the specimens was checked against type-species in the British
Museum (Natural History).
Blood samples were taken from the orbital venous plexus by capillary tube
(Riley, 1960) under halothane anaesthesia. Between 1.0 ml and 2.0 ml of blood
was used and the technique of Hungerford (1965) was followed for culture and
preparation.
The technique was not very successful with the blood of the two Ctenodactylus
species and these were cultured according to a method devised and carried out by
Mr M. D. Burtenshaw of the Sir William Dunn School of Pathology, Oxford.
Some specimens were G-banded by the trypsin digestion method and Giemsa
staining of Seabright (1972).
In the analysis of karyotype patterns a modification of the method of Levan,
Fredga & Sandberg (1964) was used (George, Weir & Bedford, 1972). Short arm
to long arm values of 1.0 : 1.7 were classed as metacentric; 1.7 : 3.0 as submetacentric and 3.0 : 7.0 as subacrocentric. Even though the number of animals
was small the number of cells studied made it seem reasonable to construct
idiograms for making banding pattern diagrams and for calculating relative
chromosome lengths. Chromosome lengths were calculated as percentages of the
haploid female set. The standard deviations were calculated and the chromosomes
compared statistically by the least square difference test.
CTENODACTYLID C H R O M O S O M E S
263
RESULTS
Ctenodactylusgundi
Fifty mitotic plates were counted for each of three females and ten of each were
photographed and karyotyped. Idiograms were made from the average
measurements of these thirty karyotypes. The chromosomes of two of the females
were G-banded.
The diploid number of Ctenodactylu~gundi is 2n=40, previously reported by
Matthey (1956a)(Fig. 1).
The autosomes are all metacentric except for chromosome 2 and chromosome
5 which are submetacentric. Chromosomes 16 and 1 7 are nearly submetacentric.
Chromosome 2 stands out as a distinctive feature of the set.
Chromosome 8, the marker chromosome, is nearly submetacentric and has a
big nucleolar organiser region in the proximal part of one of the arms (referred
to as the short arm by some authors and the long arm by others but here called
the long arm). The distal part of the long arm in this marker chromosome is
equal in size to the whole of the short arm and the part of the long arm next to
the centromere is very short.
Chromosome 1 is big, forming over 10%of the karyotype. In one individual,
chromosome 1 and chromosome 2 were consistently polymorphic throughout
all the cells examined. The explanation seems to be that a simple translocation
had occurred between the long arm of one of the number 1 chromosomes and
the long arm of one of the number 2 chromosomes. In spite of the problems in
gametogenesis that may follow this type of translocation, it seems to have been a
common type of change in the ctenodactylids. Polymorphic pairs of
chromosomes resulting from similar translocations are known in the Caviidae
(Cohen & Pinsky, 1966; George et al., 1972).
Figure 1. Karyotype of female Ctenodactylus gundi.
-
-
-
I
I
I
I
80
80
12
12
40
40
36
36
Ctenodactylus w a l l
Peclindor spekei
Masoutiera mzabi
Feloriia vat
-
-
I
-
-
-
-
-
sm sa
80
m
> 9%
Large
40
2(m+ sm+ sa)
+a+x
NF
Ctenodactylus gundr
2n
-
-
-
-
-
a
1
2
5
3
-
-
-
-
2
5
-
-
-
-
5
-
-
4
-
m
8
9
10
11
1
4
-
-
-
-
-
-
2
1
-
_
-
-
-
-
-
I
-
-
_
-
-
-
-
-
-
a
-
_
-
sm sa
m
sm sa a
a
sm sa
1
2
m
Micro
< 2%
Small
5.5-2.0%
Medium
9-5.5%
Autosomal pairs
- 8/9th
8th
718th
7/8th
Marker
- 7/8th
-
Table 1 . Comparison of the chromosomes of five species of Ctenodactylidae
-
Y
5.3%m 1.7%m
5.2%m 2.5%m
5 . l % m 0.9%sa
5.2%m 2.7%sa
5.l%m
X
Sex chromosomes
$
w
0
s
5
CTENODACTYLID CHROMOSOMES
265
From chromosome 3 to 19 there is an even gradation through medium and
small chromosomes to chromosome 19 which is 2.7% of the karyotype.
The X chromosome is a metacentric and the 9th in length. At 5.1% it is a
standard mammalian X chromosome (Ohno, Christian, Wachtel & KOO, 1964).
The NF is 80.
The characteristics of the karyotype are summarised in Table 1. It is a
symmetrical karyotype (Stebbins, 197 1 ; George 8c Weir, 1974).
The banding pattern is shown in Figs 3 and 14. Although the banding pattern
of C. gundi did not come out well in any of the preparations, it provided an
adequate picture for comparison with the other species.
Ctenodactylus uali
Mitotic plates from seven animals, four females and three males, were counted
and ten of each karyotyped. The chromosomes of two males and two females
were G-banded. Idiograms were constructed.
The diploid number of Ctenodactylus uali is 2n= 40 (Fig. 2).
The autosomes are all metacentric except for chromosome 9 and chromosome
1 7 , both of which are just submetacentric but differ hardly at all from the same
chromosomes of C. gundi which just fall into the metacentric group.
The most obvious difference from C. gundi is in chromosome 2 which is
considerably shorter and is metacentric. It forms 6.5%+0.5 of the haploid
complex compared with 7.8%+ 0.3 for C.gundi. This is a statistically significant
dif'ference, P<O.OOl. Chromosome 1 is also shorter than that of C. gundi
(9.9%+0.4 : 10.4%+0.6, P=0.002). Chromosomes 6, 15 and 17 are rather bigger
than in C. gundi.
Chromosome 8 has a nucleolar organiser region.
The X chromosome is metacentric, forms 5.2% of the total haploid set and is
8th to 9th longest. The Y chromosome is submetacentric to subacrocentric and
forms 2.7% of the set. It is the smallest chromosome (Fig. 11).
Figure 2. Karyotype of female Ctenodactylus vali.
15
266
W. GEORGE
The NF is 80 (Table 1).
The banding pattern is very similar to that of C . gundz, differing noticeably only
in chromosome 2 (Figs 3, 4). The order of the bands in the long arm of
chromosome 2 is reversed in C . vali.
Pectinator spekei
Only one male and one female were available for blood samples but each
yielded a good crop of metaphase plates from among which twenty of each sex
were photographed and karyotyped. Cells from the male were G-banded.
Figure 3. Gieinsa banded karyotype of female Ctenodactylus gundz.
Figu1-e4. G i e m a banded karyotype of fernale Ctenoductylus uali.
CTENODACTYLID CHROMOSOMES
267
The diploid number ofPectinator spekei is 2n=40 (Fig. 5 ) .
The chromosomes are very similar to those of Ctenodactylus gundi with
chromosomes 2 and 5 the only submetacentric among the metacentrics.
Chromosome 5 is longer than in C. gundi, 6.1%?0.3:5.4%?0.3, P<O.OOl.
Chromosome 19 is shorter, being a microchromosome, only 1.4% of the haploid
set and only half the size of its counterpart in C. gundi ( P < 0.00 1).
Marker chromosome 8 is present.
The X chromosome is the 10th longest, 5% and metacentric but the Y
chromosome is minute. It is so small, 0.9% of the haploid set, that it proved very
Figure 5. Karyotype of inale Pectinator spekei
Figure 6 . Gieirisa banded karyotype of male Pectinator spekei.
268
W. GEORGE
difficult to resolve on most photographs. But on those prepared specifically to
identify this chromosome it appeared to be subacrocentric.
The NF is 80 (Table 1 ) .
The banding patterns of chromosomes 1 , 5 and 19 were the only ones that
were different from C. gundi (Fig. 6). There are considerably narrower pale bands
in the middle of both the short and the long arms of Pectinator chromosome 1
compared with the equivalent chromosomes of the two Ctenodactylus species.
Chromosome 5 probably has an extra dark band in its long arm. Chromosome
19 of Pectinator appears to have lost the dark band from both its arms.
Massoutiera mrabi
Three females and one male provided 50 metaphase plates each and
karyotypes were made from ten photographs from each animal. One female
blood sample was G-banded.
The diploid number for Massoutiera rnrabi is 2n=36 (Fig. 7 ) .
Only chromosome 5 is submetacentric and resembles that chromosome in
Ctenodactylus and Pectinator. Chromosome 2 is just metacentric and significantly
shorter than chromosome 2 of Pectinator and Ctenodactylus g u n d i
(7.3%_+
0 . 4 : 8.0%_+0.4,P < O . O O l ) . I t is not as short as the C. uali chromosome 2.
Chromosomes 18 and 19 are absent. Chromosomes 13, 14 and 16 are longer
,
14,
than in the other two genera (13, 4 . 6 % + 0 . 2 : 3 . 9 % _ + 0 . 2P=O.Ol;
:3.4%+0.1,P<O.OOl).
4.3%?0.2 :3.8%?0.2;P=O.2; 16,4.1%_+0.3
The marker chromosome 8 is present.
The X chromosome is metacentric, 5.2% and 10th to 1 1 th longest.
The Y chromosome is twice the length of the Pectinator Y chromosome and, at
2.5%, about the same size as the Ctenodactylus Y but, unlike either of these, it is
metacentric. It is the smallest chromosome of the set (Fig. 12).
The Masoutiera mzabi karyotype is the most symmetrical of all the species.
The NF is 72 (Table 1 ) .
Figure 7 . Karyotype of female Marsoutiera mtabi.
CTENODACTYLID CHROMOSOMES
269
The banding pattern of the chromosomes is, again, very similar to Pectinator
and Ctenodactylus. Chromosome 1 resembles Pectinator and not Ctenodactylus.
Chromosome 5 resembles Pectinator more than it does Ctenodactylus.
Chromosome 13 differs from both Pectinator and Ctenodactylus in having a
distinctive dark band in the short arm (Fig. 9).
Felovia vae
Four males gave excellent mitotic plates for counting. Again, ten of each
individual were photographed and karyotyped. The chromosomes of one male
were G-banded.
The diploid number for Felovia vae is 2n= 36 (Fig. 8 ).
Chromosomes 2, 5 and 7 are subacrocentric showing an exaggeration of the
tendency in the other four species towards asymmetry in these chromosomes.
They do not, however, differ significantly in overall length from those of the
other species. Chromosome 1 resembles chromosome 1 of Pectinator and
M assoutiera.
Like Massoutiera, chromosomes 18 and 19 are missing and chromosomes 13, 14
and 16 are longer than in Pectinator and Ctenodactylus, again resembling
Massoutiera ( 1 3 , 4.5%+0.2 : 3.9%+ 0.2, P=O.Ol; 14, 4.3%+0.2 : 3.8%+0.2,
P=0.02; 16, 3.9%+0.2 :3.4%+0.1,P=0.02).
Marker chromosome 8 is present.
The X chromosome is metacentric, 5.3% and 10th longest in the series. The Y
chromosome is metacentric, like the Y chromosome of Massoutiera, but it is very
much smaller at 1.7% of the set and the smallest chromosome.
This is the least symmetrical of the karyotypes.
The NF is 72 (Table 1).
The banding pattern shows the same constancy as the other four species.
Chromosome 5 has only one dark band in the short arm but otherwise resembles
Pectinator and Massoutiera. Chromosome 13 resembles that of Massoutiera and
differs from Ctenodactylus and Pectinator (Fig. 10).
Figure 8 . Karyotype of male Felouia w e .
2 70
W. GEORGE
Figure 9. Gieiiiaa banded karyotype offeinale Massoutiera mzabi.
Figure 10. Gienisa banded karyotype of male Felouia uae
DISCUSSION
Details of the karyotypes of the five species might be expected to give an
indication of the relationships within the family while the characteristics
common to all of them, the family karyotype, can be compared with those of
other rodent families.
Comparisons ofkaryotypes in the living genera
The overall karyotype pattern of the five species is broadly similar. A
comparison was made of length and centromere position of all the
CTENODACTYLID CHROMOSOMES
27 1
chromosomes. Between each pair ot species, the differences in length of each
short arm and each long arm of corresponding chromosomes were measured.
The values were squared and summed to give an index of dissimilarity. The
resulting relationship is shown in Fig. 13. Ctenodactylus gun& and C. uali have the
closest resemblance but are probably sufficiently different to merit their separate
specific status (Petter, 1961; Ranck, 1968). C. gundi is very close in pattern to
Pectinator. Massoutiera and Felouia are more similar to one another thaq to either
of the other two genera but are closer to Pectinator than to Ctenodactylus.
The banding patterns are very similar in the five species (Fig. 14). C. gundi and
C. uali differ slightly in the banding arrangement of chromosome 2. They both
differ from the other three species in the pattern of chromosomes 1, 5 and 19.
Pectinator has no dark bands in chromosome 19 and probably none in the Y
Figiii-r I 1. Metaphasr plate of inale Clenodacfylus d t . Arrows show the acrocentric Y chromosome
die two niarkcr chromosomes lying together as they often do.
;iiitl
Figui-r 12. Metaphase plate of inale Marsoutiera mzabi. Arrow shows the metacentric Y chromosome.
W. GEORGE
472
Felovio
Pectinotor
spekei
100
vae
volt'
Massoutiera
mzobi
Figici-e 13. Dissimilarity diagram for five species of the Ctenodactylidae based o n differences in
di~~o~iiosoiiie
length and position of the centromere.
I
1A
2
4
5
6
7
8
9 10 II
12 13
14 15 16
17 18
19
X
kigure 14. Diagram of Gieiiisa band patterns in Ctenodactylusgundi.
chromosome and, in this respect, is unique. Massoutiera and Felovia dif'fer from
Pectinator and Ctenodactylus in having a dark band in the short arm of
chromosome 13. Felouia has a unique banding pattern in chromosome 5 . These
are small differences.
Both overall morphology and banding of the chromosomes would seem to
support the hypothesis that a n ancestral ctenodactylid had a karyotype which
contained nine of' the chromosome pairs today common to all five species and,
perhaps, a mixture of Pectinator and C. gundi chromosomes accounted for the
remainder. The ancestral population could have given rise to Massoutiera and
belovia and then, perhaps, itself differentiated into Pectinator and Ctenodactylus
species.
I t s e e m more reasonable to work from the higher chromosome number to the
lower because there is no evidence from the banding patterns that the small
chroniosoines, 18 and 19, could have been acquired from the Massoutiera-Felovia
line by aneuploidy. Since all the chromosomes are two-armed there are no
grounds for postulating fission. I t is also unlikely that the Y chromosome would
CTENODACTYLID CHROMOSOMES
273
I
I
I
/
\
P
I
0
/
13
14
1
IG
.-
I
7
jY
'odaciylus
gundi
19
Ctenodoctylus
vali
itiera
zabi
Felovia
YO8
Figure 15. One way in which the karyotypes of the five species of Ctenodactylidae could be related.
get progressively bigger during evolution whereas loss of redundant Y material
can easily be imagined.
Taking a hypothetical gundi ancestor with a karyotype resembling both
Pectinator and Ctenodactylus gundi, an equally hypothetical evolutionary diagram
can be constructed (Fig. 15).
The changes leading to both Ctenodactylus species involve several translocations
and a paracentric inversion. In this way, the strikingly long chromosome 1 of C.
gundi and the comparatively small metacentric chromosome 2 of C. uali can be
274
W. GEORGE
accounted for. The steps to Pectinator are rather less satisfactory. Chromosome 5
may have acquired a piece of chromosome 19 by translocation, but it is difficult
to account for the other bit of 19 and the bits of Y that are not apparently
represented in the karyotype. Either they have been distributed to several other
chromosomes by the translocation of very small bits or they may have been lost.
I t seems possible that much of the Y chromosome is redundant and, therefore,
the bits could be lost without upsetting the genic balance.
Further translocations, involving five chromosomes, could give an ancestral
karyotype for Massoutiera and Felovia. The Massoutiera karyotype would then be
completed by a pericentric inversion to give a metacentric chromosome 2 with
the translocation of bits of that chromosome to others. The Y chromosome
becomes metacentric but how is not clear. To achieve the Felovia karyotype, two
pericentric inversions are needed for chromosomes 5 and 7 and loss, or
translocation, of part of the long arm of the Y chromosome.
Patterns of karyotype change
One of the most interesting conclusions from this hypothesis is that a few
chromosomes seem to be much more liable to change than others or, perhaps, it
should be put the other way round: that many of the “family chromosomes” are
basic linkage groups that cannot easily be disrupted. Chromosomes 2, 5, 7 , 18,
19 and Y are involved in several changes while over 40%of the karyotype is stable
throughout the family.
Changes in the Y chromosome, probably involving loss of bits, supports the
view often expressed that most of the mammalian Y chromosome is redundant
(Wachtel, Ohno, Koo 8c Boyse, 1975; Ohno et al., 1976). The Y chromosome of
Pectinator comes into the group of very small mammalian Y chromosomes, like
some of the insectivores, marsupials, carnivores, artiodactyls (Ford, 1970) and
caviomorphs (George & Weir, 1974) and the Y chromosome of Felovia is also
small.
Where chromosomes have become significantly smaller during the proposed
evolutionary sequence in the ctenodactylids, it has frequently been very difficult
to see where the missing bits have gone to. For instance, chromosomes 18 and 19
have not transferred obviously to any other chromosomes of the
Massoutiera-Felovia line, nor has chromosome 2 in its conversion to a Massoutiera
chromosome 2. However, since it is assumed that, apart from the Y
chromosome, all parts of the genome are essential to life, the chromosomes have
been estimated as occupying the same total length in each species. Thus, there are
small differences in the lengths of several chromosomes, though the differences
are statistically significant only in those chromosomes shown in the diagram (Fig.
15).
Consequently, it must be supposed that when a chromosome is liable to
breakage, for whatever reason, the breaks are likely to be multiple or to occur
often. In this way, very small bits of breakable chromosomes could be
translocated to many other chromosomes in the complex. If all these
translocations have to be reciprocal translocations, then a considerable number
of chromosomes must be involved in small breaks and exchanges during the
evolutionary process. But as chromosomes 18 and 19 gradually decrease in size
to nothing they cannot be involved in reciprocal translocations. The only
alternative would seem to be loss of small bits. This seems unlikely.
CTENODACTYLID CHROMOSOMES
275
In summary, the most economical set of changes that can be postulated
requires only pericentric inversions and simple, small-scale translocations.
Relationsha$ of the ctenodactylid genera
The relationships between the karyotypes of the five species corresponds
reasonably well with other criteria. Pectinator spekei has the general appearance of
a small squirrel with a pointed face and short bushy tail. It lives in rocky deserts
where there are acacia trees and climbs the trees to feed on the leaves. Both
species of Ctenodactylus are rounder, blunter-faced, flatter-eared and have mere
wisps of tail. They live in similar rocky desert habitats but where there are few, if
any, trees. C. gundi is considerably bigger than either Pectinator or C . vali. The
morphological changes from an ancestor which may have had a tail and squirreltype head like Pectinator seem considerably greater than the simple karyotypic
changes that have occurred.
Felovia vae has a head like Pectinator but a short fan tail, shorter than that of
Pectinator, longer than that of Ctenodactylus. Although the habitat of at least some
Felovia extends into an area where there are a few trees, Felovia does not climb
trees and most of its habitat is treeless. Massoutiera mzabi has a considerable
resemblance to Ctenodactylus, having an even blunter nose, rounder eyes and
Hatter ears. But it has a tail that is about the same size as that of Felovia and it uses
its tail as a “balancing” organ even though it lives where there are no trees
(George, 1974).
As in other cases that have been looked at in detail, there is no direct
correlation between morphological changes and karyotype changes. That a direct
correlation does not exist makes karyotypes all the more useful as independent
indicators of affinity.
Taking into account both morphology and karyotype, the evolutionary
pattern seems to go from an ancestor to a Pectinator-Mmsoutiera-Felovia line on the
one hand and a Ctenodactylus line on the other. On this supposition, there seems
to have been a split among the ancestral population early on and yet Pectinator
and Ctenodactylus gundi have karyotypes that are alike. It could be that the
karyotypes in these ancestral forms remained unspecialised and were correlated
with the ability to range over a wide habitat. Today, Pectinator and Ctenodactylus
gundz have the greatest range, living from extreme desert conditions to cooler
semi-arid areas with considerable plant coverage. Geographically, they both
have a wide continuous range. Massoutiera and Felovia have come to occupy some
of the more isolated habitats and, in some cases at least, the populations do not
extend over great distances. Felovia is known only from one colony in the Sahel
area of Mali (Lataste, 1886; George, 1974). Massoutiera is cut up into separate
populations (probably into several separate species) in the central Sahara
mountains. C. vali is the most desert adapted and it is not broken up into isolated
populations.
Some support for this hypothesis comes from a study of meiosis in C. vali and
Felouia. Not only does Felovia have fewer chromosomes but it also has fewer
chiasmata per chromosome.
If this is a correct assumption, that karyotype changes are related more to
population sizes than to the time for which a population has been separated
from its relatives, then the gundi story is in line with the findings of Koulischer
for artiodactyls (1973), Nadler et al. (1975) for ground squirrels, Carson, Clayton
276
W. GEORGE
& Stalker (1967) for Drosophila and Bush, Case, Wilson & Patton (1977) for
mammals in general, and does not support the view expressed by Wilson, Sarich
& Maxson ( 1974) that chromosome changes are positively correlated with time
and with gross anatomical changes.
Only small changes are found in the G-band patterns of the ctenodactylids.
25% of the chromosomes are affected but this accounts for only 11% change in
total band pattern.
This conservatism of G-band pattern is in line with the findings of Mascarello,
Stock & Pathak (1974)for an assorted group of rodents, and of Buckland & Evans
( 1978) for bovids. G-band patterns do not appear to give a clear indication of the
length of time for which groups have been separate. The amount of change
found between ctenodactylid genera is similar to that found between apes and
man (Vogel, Kopun 8c Rathenberg, 1976) but very much less than between rat
and mouse for which Nesbitt (1974)estimated a 40% G-band difference.
There is no general trend in chromosome number that can be correlated with
ecological factors. For example, chromosome number cannot be correlated with
increasing aridity. The two Ctenodactylus species are at the extremes. C. gundi
ranges as far north as the southeast corner of Morocco and mid-Tunisia where
the winters are cold and the rainfall approximately 150 mm. C. vali lives in the
most arid areas where the average rainfall is 40 mm. Both have 40 chromosomes.
Massoutiera mzabi, with 36 chromosomes, lives in areas that are almost as arid as
those occupied by C. vali, while Felovia vae, 2n=36, lives in areas where the
rainfall may be over 600 mm, though the temperature is always high. Pectinator
spekei, 2n= 40, occupies an intermediate climatic habitat.
Equally, there is no latitudinal cline. The two most southerly, Pectinator and
Felovia, have 2n=40 and 2n=36.
There is a very slight correlation between diploid number and the average
relative humidity, if the whole range of the species is taken into account, but the
tigures are not convincing.
There seems to be no single chromosome that can be correlated with any
geographical or ecological variation. Only chromosome 2 has any suggestion of
being correlated with climatic factors. Chromosome 2 is smaller and more
rnetacentric in Ctenodactylus uali and Masoutiera mzabi than in the other three
species and these two live in areas where the annual precipitation is lowest
(38 inin to 62 mm) and the index of aridity lowest (Koppen, 1931).
Very little can be said about the time sequence of ctenodactylid radiation.
Jaeger ( 197 1) suggested that the Felouia line is represented in the early Pleistocene
of' Morocco by the fossil genus Irhoudia and the Massoutiera line by Pellegrinia from
the early Pleistocene of Sicily. Thus these two lines would seem to have diverged
from one another some time in the Pliocene and the differences between them,
general shape and colour and minor modifications in the chromosomes,
accumulated over several million years.
The karyotypes do not solve the problem of ctenodactylid ancestry but they do
seem to show that all the modern genera are likely to have had a common
ancestor which was neither more nor less related karyotypically to Pectinator than
to Ctenodactylus. The Miocene Moroccan Africanomys of Jaeger et al. ( 1973) and of
Black ( 1972) seems a more likely candidate than the Tataromys-Syamys-Pectinator
group of Shevyreva (1972b).
Karyotypes support the Felovia-Massoutiera relationship suggested by Jaeger.
CTENODACTYLID C H R O M O S O M E S
21 7
They extend the relationship to include Pectinator, a nearer relative to this line
than to Ctenodactylus, and coincide exactly with relationships based on tooth
pattern (Ellerman, 1940).
Relationships ofthefami4
The diploid number 2n=36 to 2n=40 for the living genera of the
Ctenodactylidae is on the low side of the average for eutherian mammals which is
2n=48 (Matthey, 1973). I t is lower than the average for the myomorph rodents
where the average is, again, 2n=48 (Matthey 1952, 1956b), but falls well into the
range of the sciuromorphs where the average is 2n=38 (Nadler, 1964, 1966a, b;
Nadler & Hughes, 1966; Hoffmann 8c Nadler, 1968). Caviomorph rodents have a
wide range of diploid numbers from 2n= 20 to 2n= 88 and there is no convincing
peak in the distribution curve (George & Weir, 1974).
All ctenodactylid chromosomes have two arms and most are metacentric. This
gives NFs of 76 and 80 which are on the high side for mammals as a whole,
resembling gerbillines (Lay, Agerson 8c Nadler, 19751, but not reaching the high
values of some of the caviomorphs. Sciuromorphs have, in general, lower NFs
than most of the ctenodactylids.
Matthey ( 1956a)considered the karyotypes of Ctenodactylusgundiand the dipodid
Allactaga to be very similar on account of the big chromosome 1 and the mainly
metacentric character of the karyotype. Recent work has confirmed both the
presence of the big chromosomes and the metacentric karyotype in species of
Dipus (Malygina, 1973). But a big chromosome 1 is not confined to these families.
Many of the sciuromorphs and caviomorphs among the rodents have big first
chromosomes. I t is not easy to decide from the banding patterns of some of these
chromosomes whether any could be homologous. The G-banding of the
ctenodactylid chromosome 1 bears some sort of resemblance to chromosome 1
of some Spermophilus species (Nadler et al., 1975) but it is not identical and,
therefore, probably not significant. No chromosomes can be equated with those
of other rodents with certainty on the basis of banding patterns, except the X
chromosome, which appears to be identical with the X chromosomes of a
chinchillid and a ctenomyid (George, unpublished) and probably with that of
many other rodents. Chromosomes 16 and 19 of the ctenodactylids have G bands that can be homologised with those of similar small chromosomes in
Ctenomys talarum and Lagidiumperuanum, but chromosome 19 could be considered
to be just as much like the Rattus chromosome 20. Several other
be equated with
chroinosomes-3,
4, 5 , 6, 9, 10, 11, and 15-could
chromosomes in the Lagidium complex and 4, 5 and 9 also resemble
chrornosonies of Spermophilus. In general, the patterns of the ctenodactylids d o
not look like those of sciurids, murids or cricetids that have been investigated but
bear a general resemblance to a chinchillid.
Ctenodactylids resemble caviomorph rodents in several ways. They have predominantly inetacentric chromosomes. They have a standard metacentric o r submetacentric X chromosome and, often, a very small Y chromosome (Fredga,
1966; George & Weir, 1974).
The most outstanding feature of the ctenodactylid karyotype is the marker
chromosome 8 , with a nucleolar organiser region in the long arm. The organiser
region is close to the centromere; the rest of the arm, beyond the organiser
region, is as long as the other arm of the chromosome. Permanent metacentric
W. GEORGE
278
or submetacentric chromosomes of this type are found occasionally in
insectivores (Borgaonkar, 1969; Gropp, 1969) and in the giraffe (Koulischer,
1973) but are only widespread family features in the Carnivora (Wurster &
Benirschke, 1968; Wurster, 1969) and in the Caviomorpha (George 8c Weir,
1974).
In the caviomorDh rodents the marker chromosome is a rewlar
feature of all
”
but the erithizontids, caviids and dasyproctids. There are two distinct marker
chromosomes: the octodontid and the chinchillid. The chinchillid marker is
always big with the nucleolar organiser region at the distal end of the
chromosome arm. The octodontid marker is usually a medium to small
chromosome ranked no higher than 8th in the karyotype and usually lower. The
nucleolar organiser region is proximal, giving a very short bit of arm near the
centromere and a long piece beyond the organiser region.
The ctenodactylid marker chromosome is very like the octodontid marker
chromosome in every way except its overall size which is considerably greater
than in most octodontids and their relatives.
The G-banding patterns of these marker chromosomes do not show enough
detail to be more than suggestive. But the chinchillid marker has more, and more
distinct, bands than either the octodontid or the ctenodactylid. Both Ctenomys
talarum and the ctenodactylids have undifferentiated heavily staining arms in
their marker chromosomes.
The ctenodactylids are now generally supposed to have had a common origin
with the protrogomorph sciuravids (Dawson, 1964; Shevyreva, 1972a; Wood,
1975) and to have no bearing on the difficult problem of hystricognathous
rodents. This may be so. The ctenodactylid marker may be an entirely
independent event. The fact that one chromosome of a pair sometimes has a
similar nucleolar organiser region in Tamiasciurus (Arrighi, 1974) and Gulea
(George et al., 1972)would support the view that this type of chromosome comes
and goes and is not unknown among the sciuromorphs.
But however much the skeletal and developmental characters of the
ctenodactylids are rationalised away from the hystricognathous rodents (Lavocat,
1974; Wood, 1975)there still remain a considerable number of features that are
remarkably similar in the two groups. The multi-serial enamel, the lateral
nipples, the vaginal closure membrane, the comparatively long gestation period,
the sacculus urethralis (Tullberg, 1899), the hystricomorphous skull and even the
comb toes are characteristic of many of the caviomorphs and rare in
combination in other rodents.
hystricognathous-hystricomorphous
Perhaps
the
incipiently
Reithraparamyinae (Wood, 1974)of the Eocene New and Old Worlds were, after
all, the progenitors of some of the odd African rodents and had, among their
many other incipient characters, an incipient tendency to make big nucleolar
organiser regions on one pair of chromosomes. Or, are New and Old World
“hystricomorphs” more directly related ?
The presence of‘ a marker chromosome of the octodontid type in all living
genera of Ctenodactylidae adds one more provocative feature to the
hystricognath- hystricomorph tangle.
I
ACKNOWLEDGEMENTS
I am indebted to Dr Barbara Weir for a great deal of help: for looking after
living animals and for taking blood samples. Dr Ted Evans and Mr Mike
CTENODACTYLID CHROMOSOMES
279
Burtenshaw solved the problems of preparing Ctenodactylus chromosomes and Dr
Martin Bobrow’s department gave me invaluable help. George Crowther caught
the animals.
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