Reig (1979) - Barros - Useche - et al - The chromosomes of spiny rats proechimys

Genetica
THE CHROMOSOMES
OF SPINY RATS,
VENEZUELA
(RODENTIA,
ECHIMYIDAE)
PROECHIMYS
A. REIG’ ,M A. BARROS’ , M. USECHE’ , M. AGUILERA’
TRINITATIS,
FROM
Vol.
TRINIDAD
51,2:
AND
153-158,
1979
EASTERN
& 0 .J. LINARES’ *
i Departamento de EstudiosAmbientales,Universidad Simon Bolivar, Apartado 80.659, Caracas108, Venezuela
* Departamento de Biologia, Facultad de Ciencias,Universidadde Los Andes, Apartado 3 14, Merida, Venezuela
Received
February
13,1979fAccepted
July
I, 1979
A detailed description of the karyotype of Proechimys trinitatis, (2n = 62, FN = SO),basedon specimens from Trinidad, is given. It differs from the
karyotype of Proechimys guyannensis (2n = 40)
which is interpreted as an indication of the need of
giving full speciesstatus to P. trinitatis. It alsodiffers
from the karyotype of P. urichi, a montane form
living in Eastern Venezuela, and it is remarkably different from the karyotypes of membersof the superspeciesP. guairae from north-western and north-central Venezuela. Specimensfrom a sampleof Cachipo,
in the lowlands of MonagasState, proved to have a
karyotype identical to that of the studied specimens
of P. trinitatis from Trinidad. This is interpreted asan
indication that P. trinitatis is also representedon the
continent. Differences in size and in cranial characters
of the Venezuelan specimenssuggestthat the Cachipo
samplemight be separatedas a distinct subspeciesof
P. trinitatis.
ability is interpopulational (Reig et al., 1979). Therefore, when karyotypic differencesare large enoughas
to imply postzygotic reproductive isolation by a high
level of gametic aneuploidy in the F, hybrids (Capanna et al., 1977; Reig et al., 1979) these differences
make a good tool for speciesrecognition, even when
this recognition is hard to make on morphological
grounds. Consequently, chromosome investigations
may contribute to the understandingof the confusing
systematics of this genus, and help to gain further
knowledge on the role played by karyotypic rearrangements in the speciationprocess,a subject which is becoming a point of primary attention in modem theory
of speciation(White, 1978).
We now report the karyotype of Proechimys trinitatis (Allen & Chapman) 1893, the type speciesof
Proechimys (Allen, 1899), but which hasbeenalleged
(Ellerman, 1940) not to be separableat the species
level from the earlier proposedProechimysguyannensis(E. Geoffroy) 1803.
Introduction
Material
Spiny rats of the genusProechimyshave proven to be
highly variable in their karyotypes (Reig et al., 1970;
Patton & Gardner, 1972; Reig & Useche, 1976) and
very difficult to classify on conventional morphological characters(Thomas, 1928; Martin, 1970). In this
genus, the principal component of karyotypic vari* Present address:
Departamento
de Arqueologia
y Etnografia,
Instituto
de Investigaciones,
Facultad de Ciencias Econbmicas
y Sociales, Universidad
Central de Venezuela,
Caracas.
and methods
Four specimens
of Proechimys trinitatis were obtained
by O.J. Linaresand F.V. Clulow in Turure Forest and
in Chaguaramas
(Trinidad). Two additional specimens
were provided by C.O.R. Everard of the Caribbean
Epidemiology Centre (CAREC) at Port-of-Spain. The
specimenswere transported to Merida, Venezuela,
where three males were successfully processedfor
chromosomepreparation, following the routine bonemarrow technique (Patton, 1967). Moreover, three
specimensfrom Cachipo, NE Monagas State, Vene-
153
zuela, were provided by Gloria de VillafaAe. Later,
four other specimens from the same locality were obtained by O.A. Reig and M. Aguilera. Two females
and one male from Cachipo were processed following
the same procedure. Voucher specimens of the Trinidadian sample were deposited in the collection of
mammals of the University of Los Andes, Merida.
Those from Venezuela were incorporated to the collection of mammals of the Simon Bolivar University,
Caracas. The Trinidadian specimens were identified as
P. trinitatis by the senior author after comparisons
with the type and additional specimens at the American Museum of Natural History and the British Museum (Natural History).
Karyotypes were constructed from enlarged prints
of metaphase photographs. An idiogram was calculated after measuring ten selected metaphases of the
Trinidadian specimens. The mean length of each chromosome was expressed as its mean percentage of the
total length of the haploid autosomal complement
plus one X chromosome (TCL). Nomenclature of
chromosomes according to the position of the centromere follows current conventions (Levan et al.,
1964). The fundamental number (FN) represents the
number of measurable arms of the chromosomes of
the autosomal set.
The chromosomes were assorted into four groups
as in previous publications (Patton & Gardner, 1972;
Reig & Useche, 1976). Group A comprises large (>
7% TCL) autosomes, whatever the centromeric index.
Group B comprises medium-sized (4-7% TCL) and
small (< 4% TCL) metacentric and submetacentric
autosomes. Group C comprises medium-sized and
12
Fig. 1. Karyotypes
of Proechimys
man, 1893). Above:
0, Cachipo,
below: d, Turure forest, Trinidad.
phases, Giemsa stain. Cf. text.
1.54
trinitatis
(Allen & ChapMonagas State, Venezuela;
From bone marrow
meta-
t
Fig. 2. Idiogram
of froechim.vs
trinitatis
(Allen & Chapman,
1893). Length expressed
as % total length of female haploid
complement,
indicated
in scale at left. Cf. table 1 and text.
small telocentric and subtelocentric autosomes. The
fourth group includes the gonosomes.
Results
Seventy-eight metaphases from bone-marrow
cells
from six specimens were analysed. In all of them 62
chromosomes were counted and the FN was 80.
Karyotypes of the three Trinidadian and the three
Venezuelan specimens proved to be indistinguishable
as regards relative size and centromeric indexes of the
different chromosome pairs.
Table
There is one pair of metacentrics and one pair of
submetacentrics in Group A (Figs 1 & 2, Table 1).
Group B is made up of six pairs of metacentrics, three
of which are medium-sized and are separated by a
sharp size gap from the remaining three smaller ones.
No secondary constriction is visible in any of these
six pairs. Twenty-two
autosomes belong to Group C.
Pair C-l is a medium-sized T-chromosome bearing a
clear achromatic region in the middle. Pair C-2 is a
medium-sized subtelocentric. With the exception of
pair C-4, which is small and subtelocentric, all remaining Group C autosomes are small telocentrics, gradually decreasing in size. Pair C-6 is distinguished by a
1
Mean values and their standard deviation
(SD) of total length, arm lengths and arm ratio (I)
of the chromosomes
of Proechimys
trinitatis.
Length expressed
as % total length of female
haploid complement.
Calculated
from 10 metaphases
of three individuals
from Trinidad.
Chromosomes
C,
C4
CS
C6
C,
C8
C9
C 10
C,,
Cl2
C 19
C 14
C IS
C 16
C 17
C I8
C 19
C 2”
C,,
C 21
X
Y
Total
Mean
length
SD
10.15
7.43
6.82
6.40
5.45
3.18
2.50
1.76
6.02
4.97
3.15
3.27
2.76
2.44
2.31
2.18
2.07
1.95
1.87
1.78
1.73
1.69
1.62
1.57
1.53
1.48
1.45
1.42
1.37
1.27
0.86
0.68
0.29
0.43
0.23
0.54
0.36
0.23
0.51
0.39
0.28
0.36
0.25
0.13
0.11
0.10
0.11
0.09
0.11
0.13
0.12
0.13
0.12
0.12
0.12
0.12
0.13
0.11
0.13
0.15
5.39
5.30
4.03
3.56
3.04
1.80
1.44
0.98
-
0.53
0.69
0.29
0.31
0.22
0.31
0.19
0.13
-
4.20
247
-
5.84
1.80
Long arm
Mean
SD
Short
Mean
arm
Arm
ratio
SD
(r)
4.16
2.13
2.79
2.84
2.41
1.38
1.06
0.78
-
0.31
0.25
0.27
0.19
0.14
0.25
0.21
0.11
-
1.13
2.49
1.44
1.25
1.26
1.30
1.36
1.26
0.35
-
0.77
-
0.09
-
0.78
0.80
-
0.17
-
0.;2
m
.$a
-
0.37
-
0.90
3.25
0.46
2.56
0.48
1.28
0.30
-
-
-
-
-
m
1.55
secondary constriction, visible in most of the cells
studied, The X-chromosome
is a medium-sized
(5.85% TCL) metacentric, and the Y is a very small
telocentric.
Comparisons and discussion
The karyotype of Proechimys trinitatis is quite different from that of P. guyannensis, as redefined by Petter (1978) after discovery of the type specimen in
Paris. The karyotype of guyannensis is made up of
40 chromosomes, as previously described for P. cherriei (Reig & Useche, 1976), which is considered as a
junior synonym of P guyannensis (Petter, op. cit.).
The karyotype of guyannensis shows three large submetacentrics and one telocentric in Group A; four
medium-sized and small autosomes in Group B, pair
B-l bearing a secondary constriction, and ten pairs of
medium-sized to small telocentrics in Group C. The
X-chromosome is a medium-sized (6.08% TCL) subtelocentric, and the Y is a small telocentric (Reig,
Tranier & Barros, 1979). Additionaly, P. guyannensis is clearly different from P. trinitatis in morphology, the former being much smaller and exhibiting distinctive cranial and dental features (Petter, op.
cit.). Therefore, there is no room for doubting that
trinitatis and guyannensis must be considered as two
distinct biological species. Ellerman (1940) was certainly wrong in proposing that trinitatis was merely a
subspecies ofguyannensis.
The karyotype of P. urichi (Reig & Useche, 1976)
which inhabits the mountains of Monagas State, in
eastern Venezuela, is very similar to that of P. trinitatis. It consists also of 62 chromosomes, and the
X-chromosome is also metacentric, a feature of rare
occurrence among species of Proechimys. However,
there are important differences between the karyotypes of these two species. In urichi, the autosomes
of Group A are significantly smaller, while Group B
includes more, and Group C fewer autosomes. Additionally, pair C-l is subtelocentric and does not show
an achromatic marker. Karyometric comparisons suggest that at least four pericentric inversions and two
translocations account for these differences. Due to
the fact that hybrids for several pericentric inversions
and translocations usually lead to Fz sterility by
zygotic unbalance (Hamerton, 1966; White, 1973)
there are good reasons to infer that P. urichi is poten156
tially isolated from P. trinitatis by postzygotic isolating mechanisms, and therefore, to maintain that
the two taxa deserve full species status.
Another 2n = 62 karyotype has been described for
an unnamed new species which inhabits the Barinas
and Portuguesa states, Venezuela (Reig & Useche,
1976). In a more recent paper, the species was referred to as Barina’s species (Reig et al., 1979). It also
shows a metacentric X and a telocentric C-l autosome with an achromatic region. However, it differs
from trinitatis in having significantly larger Group A
autosomes, and in showing only three pairs of small
metacentrics in Group B, and twenty-five pairs of
Group C autosomes. These differences must be the
result of at least five deletions/duplications and three
pericentric inversions, which also suggest that these
two karyomorphs, which are sharply allopatric, might
prove to show fertility reduction or complete sterility
of possible F, hybrids. Moreover, it is probable that
the similarities between the two karyotypes are a
matter of convergence, and that the two species are
only distantly related. They strikingly differ in cranial
morphology (Reig, unpublished observations). Furthermore, Barina’s species belongs to the superspecies
P guairae (Reig et al., 1979), in which a transformation series was found in a Rassenkreis of chromosomal forms going from 2n=42 (the allospecies P. POliopus) to 2n=62 (Barina’s allospecies). This superspecies represents a geographically and genetically
(Benado et al., 1979) cohesive taxonomic group,
which seems to have evolved independently from
the set of Proechim-ys populations of eastern Venezuela and Trinidad, to which P. trinitatis belongs.
Thus, everything seems to indicate that P. trinitatis is a species well differentiated from P. guyannensis
and the allospecies of the P. guairue superspecies, and
that it also differs specifically from the more closely
related P. urichi. The distinction of P. trinitatis is
even far greater when we extend the comparisons to
other chromosomally known species of the genus of
northern South America and Middle America, like P.
brevicauda (2n=24), P. canicollis (2n=24), P. ‘longicaudatus’ (2n=28), P. cuvieri (?n=28), P. amphichoricus (3n=26), P. centralis (= P ‘semispinosus’)
(2n=30), P. hendei (2n=32), and the form from Balta,
Peru, referred to asP. ‘guyannensis’(2n=40)
(Patton &
Gardner, 1972; Reig & Useche, 1976; Aguilera et al.,
1978; Reig, Tranier & Barros, 1979).
The karyotype identity of the specimens from
Cachipo, in the lowland forests of NE Monagas, and
those of Trinidad poses the problem whether P. trinitatis is alsopresent in the Venezuelan portion of the
continent. The overall chromosomal multiformity
among species of Proechinzys inclines the present
authors to assumethat in spiny rats chromosomal
identity indicates absenceof speciesdifferentiation,
and therefore, that the Cachipo samplehasto be referred to asP. trinitatis. It cannot be excluded, however, though it doesnot seemto be probable, that the
Cachipo sampleis specifically distinct from trinitatis
on other grounds. We have found that the specimens
from Cachipo are smallerand darker than thosefrom
Trinidad, and that they also differ in minor cranial
details. The samplesare not large enough,however, to
allow a thorough comparative study, but it is probable that the differences found merely representgeographic differentiation within one and the samespecies, which might eventually prove convenient to formalize through subspecies
recognition.
In any case, the P. trinitatis from Trinidad, the
Cachipo population and P. urichi are likely to represent a tightly connected group of forms. This aggregate of closely related speciesand subspeciesmay be
conveniently grouped in a superspecies
of its own inhabiting Trinidad and eastern Venezuela. This superspeciesshould be named,by priority, Proechimys [trinitatis]. But the situation is further complicated by
the fact that easternVenezuela is not only inhabited
by the Cachipo trinitatis-like
form and the karyotypitally related P. urichi, but also by at least two other
chromosomalforms. Some of us are presently studying a population with In=58 chromosomesfrom Rio
Casanay, Sucre State, and another one with 2n=52
chromosomeswhich wasfound in Cueva de1Agua, La
CaraqueAa,NE Anzoategui State. The relationshipsof
those karyomorphs are not yet clearly established,
but they seemto indicate an extensive diversification
among the spiny rats of NE Venezuela, which may be
as intriguing and interesting asthe one found in north
western and north central Venezuela (Reig et al.,
1979).
We are greatly indebted to F.V. Clulow, G. de Villafafie, A. Chang and M.V. de Limongi for field assistance and gifts of specimens.Dr. C.O.R. Everard is
heartily acknowledgedfor gifts of specimensand field
assistancein Trinidad. We are alsoindebted to M. Benado for critical readingof the manuscript. This work
was supported by a grant of the Venezuelan Council
of Scientific and Technological Research(CONICIT
Sl-0630).
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