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Chromosomal evolution in Malagasy lemurs XII. Chromosomal banding study of Avahi laniger occidentalis (Syn Lichanotus laniger occidentalis) and cytogenetic data in favour of its classification in a species apartЧAvahi occidentalis

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American Journal of Primatology 21:307-316 (1990)
Chromosomal Evolution in Malagasy Lemurs: XII.
Chromosomal Banding Study of Avahi laniger
occidentalis (Syn: Lichanotus laniger occidentalis) and
Cytogenetic Data in Favour of Its Classification in a
Species Apart-Avahi occidentalis
Y. RUMPLER,' S. WARTER,' C. RABARIVOLA: J.J. PETTER? AND B. DUTRILLAUX3
'Facult6 de Medecine, Institut d'Embryologie de Strasbourg, Strasbourg, 'Pare Zoologique de
Vincennes, Museum National &Histoire Naturelle, and 31nstitut Curie, U R A No 118, CNRS,
Paris, France; 'Laboratoire d'Anthropologie, Universite de Tananarive,
Tananariue, Madagascar
A cytogenetical study of the western form of Avahi (Avahi laniger occidentalis) shows that its karyotype differs from that of A. laniger laniger by
at least 3 chromosomal rearrangements. Meiotic chromosomal pairing of
hypothetical hybrids has been constructed. Its configuration, a tetravalent
with an inversion loop, is likely to strongly reduce fertility, especially in
the male. This leads us to propose that the two forms correspond to two
distinct species, separated by a gametic barrier: Avahi laniger and a species apart, Avahi occidentalis.
Key words: chromosome, evolution, lemur
INTRODUCTION
Among Indriidae, a family of Malagasy Prosimians, the genus Avahi is represented by a single species, Avahi laniger. Moreover, this species is distributed in
two distinct areas and representatives of these areas can be distinguished by a few
morphological characters. This led taxonomists to propose a subdivision into two
subspecies: A. laniger laniger and A. laniger occidentalis [Hill, 1953; Petter et al.,
19771.
A cytogenetical study having been undertaken for A. laniger laniger only
[Rumpler et al., 19831, it seemed interesting to study the chromosomes of the
second subspecies, to determine eventual chromosomal differences between the
two subspecies.
MATERIALS AND METHODS
One adult male and three female Avahi were caught in the Ampijoro forest, in
the northwest of Madagascar, and three males and two females in the Ranomafana
forest, in the southeast.
In view of the strict conservation measures regarding these species, the cap-
Received for publication November 28, 1989; revision accepted April 3, 1990.
Address reprint requests to Professor Dr. Y. Rumpler, Faculte de MBdecine, Institut d'Embryologie, 11,
rue Humann, 67085 Strasbourg Cedex, France.
0 1990 Wiley-Liss, Inc.
308 / Rumpler et al.
tured individuals were immediately released at the place of capture as soon as a
skin biopsy was performed. The samples were sent by air to the Institut Pasteur of
Madagascar in Tananarive where fibroblast cultures were initiated until the skin
samples could be brought to the Institut d'Embryologie of Strasbourg. The following banding techniques were applied: R-bands (RHG), C-bands (CBG), and NOR
staining [ISCN, 19781. Chromosome comparisons were performed on R-banded
chromosomes of comparable condensation.
RESULTS
The karyotype of the 4 animals from Ampijoro contain 70 chromosomes (Fig.
1). All but two pairs of autosomes (Nos. 1and 2) are acrocentric. X chromosome is
submetacentric, and Y is a small acrocentric chromosome. C-banding does not
reveal heterochromatic peculiarities, except for two small chromosomes almost
entirely composed of heterochromatin (Fig. 2).
The karyotypes of the 5 animals from Ranomafana contain 70 chromosomes
and are identical with those previously reported for the Auahi from Andasibe
[Rumpler et al., 19831 (Fig. 3).
DISCUSSION
The chromosome number is the same in both forms of Avahi but their karyotypes differ by the morphology of 2 metacentric chromosomes: chromosomes 1and
2 of A. 1. laniger are not found in A . 1. occidentalis (Fig. 3). The comparison of the
two karyotypes with the previously reconstructed hypothetical ancestral karyotype of all the lemuriforms (LEM) [Rumpler et al., 19831 (Fig. 4) shows that the two
Auahi have undergone five rearrangements in common (Fig. 5): two of them are
shared with the other Indriidae and three are common only to both Avahi. The
rearrangements common to all Indriidae are shifts, changing the position of the
kinetokores of LEM5 and LEM8 which have previously been described [Rumpler et
al., 19881. The three others are two fissions and one complex rearrangement: one
fission splits the derived chromosome of LEM8 (der8) into two chromosomes, a
microchromosome and chromosome 14 of A . 1. laniger, corresponding to a microchromosome and chromosome 13 of A . 1. occidentalis. Der8 was the result of a
pericentric inversion which was undergone earlier, giving rise to a small submetacentric still present in Propithecus and Indri [Rumpler et al., 19881. The second
fission splits the ancestral chromosome LEM16 into chromosomes 16 and 17 of A.
1. occidentalis and A . 1. laniger, respectively, and one microchromosome. The third
rearrangement seems to be a shift involving probably the ancestral chromosome
LEM14 and gives rise to a n acrocentric chromosome: der(14) which leads to a part
of chromosomes 2 and 1 of, respectively, A . 1. occidentalis and A. 1. laniger.
From the bifurcation following this common trunk emerge two branches: the
first, leading to A. 1. occidentalis, is characterized by a Robertsonian translocation
between LEMl and the der(l4) which gives rise to its chromosome 1; the second,
leading to A. 1. laniger, bears two rearrangements, a Robertsonian translocation
between the der(l4) and a microchromosome of LEM which gives rise to its chromosome 2 and a pericentric inversion of chromosome LEMl which gives rise to its
chromosome 1. The breakpoints are located on LEMl directly on the top of the
centromere and under the dark proximal R-band, so that this R-band, which remains juxtacentromeric on the long arms of ALOl (ALOlq) constitutes the major
part of the short arms of ALAl (ALAlp).
The phylogenic scheme is in accord with the chromosome numbers of both
Auahi and the ancestral karyotype LEM except for one excess pair of microchro-
Cytogenetics and Taxonomy of Avahi laniger I 309
2
3
4
5
7
8
9
10
12
13
14
15
18
19
20
22
23
24
25
26
27
28
29
31
32
33
34
11
16
21
X
Fig. 1. R-banded karyotype of Auahi occzdentalis
310 / Rumpler et al.
Fig. 2. C-banded metaphase showing the darkly stained juxtacentromeric heterochromatin of all chromosomes
of Auahi. Arrows show the two mainly heterochromatic minute chromosomes.
mosomes in both Avahi. It is difficult to determine the origin of these small chromosomes.
Taxonomic Considerations
The chromosomal differences which exist between the two Avahi allow us to
propose a revision of the taxonomy of this genus. It is likely that these chromosomal differences would bring about eventual sterility of hybrids through disturbance of meiosis. The meiotic configuration in hybrids would have a complex figure: a quadrivalent with an inversion loop (Figs. 3,6). Previous studies on lemurs
[Ratomponirina et al., 1982, 1988; Warter and Rumpler, 19851 and mice IGropp
and Winking, 19811showed fertility in hybrids presenting trivalents in addition to
normal bivalents, even if their number rose t o 3 or 5, whereas hybrids carrying a
unique multivalent involving 4 or more chromosomes are most often sterile. According to these results, the two Avahi should be put into two distinct species: one
for the eastern form and another for the western form.
These considerations require some remarks on the systematics of the genus
Auahi. This nomenclature was established by Jourdan [ 18341 to differentiate this
Cykogenetics and Taxonomy of Avahi laniger 1 311
AOC
ALA
2
3
7
8
11
12
13
16
17
18
21
22
23
24
25
26
27
28
29
30
21
32
33
4
5
10
14
15
20
x x
Fig. 3. Half R-banded karyotypes of Auuhi occidentuZis (left) and Avuhi Zuniger (right)showing the homology
of most chromosomes. ALA = Auuhi Zanlger; AOC = Avahi occidentulis.
312 / Rumpler et al.
1
2
3
4
5
6
7
8
9
10
13
14
15
18
19
20
11
16
17
21
22
25
26
24
27
28
XY
J
29
30
31
32
Fig. 4. R-banded reconstructed ancestral karyotype of all the lemuriforms (LEM) except Daubentonicc.
Cytogenetics and Taxonomy of Avahi laniger / 313
ALA
b
(14) + rnin -2
1 + der (
ALA 2q
AOC l p
ALA 17 + rnin
AOC 16 + min
p 8-i
p +2;
der ( 8 )
PVE 10, PDI 10,IIN 12
PVE 8 , PDI 9,IIN 1 1
LEM
Fig. 5. Chromosomal phylogeny of the two species of Auahi from the ancestral karyotype LEM. Numbers
preceding the arrows indicate the chromosome numbers of LEM (Fig. 2); the numbers following the arrows
indicate those of the two species ofAuahi. Species names: ALA = Auahi laniger; AOC = Avahi occidentalis; PVE
= Propithecus uerreawci; PDI = Propithecus diaderna; IIN = Indri indri. Squares = Robertsonian translocations; circles = pericentric inversions; double arrows = fissions; half dark circles = chromosomal shifts.
woolly-haired and long-tailed animal clearly from the silk-haired, tail-less genus
Indri.
Its description was based on a skull and skin reputedly from the “Maki a
bourres,” described by Sonnerat [1782]. The type locality was “Pays des Betanimenes,” in other words the coast of the Antongil Bay at the northeast of the island.
Therefore, based on its eastern location, it corresponds to the form subsequently
considered as the subspecies Auahi laniger laniger [Gmelin, 17881. Other names
314 / Rumpler et al.
Fig. 6 . Schema of the presumed meiotic picture of a hypothetical hybrid ALA X AOC, showing the monobrachial homologies of ALA1, AOC1, ALAP, and a undeterminate microchromosome of AOC.
were also attributed by different authors and are now synonyms: Mycrorhynchus,
Jourdan “341 (which, already used for a Coleoptera, is Nomen nudum), Habrocebus Wagner [1840], Semnocebus Lesson [ 18401, Iropocus Gloger [18411, Lichanotus Illiger [1811]. (Some authors, following Eliott [ 19131, considered the latter
name as having priority over Avahi, but it had been proposed by Illiger [18111 to
replace the name of the genus Lemur, which had been used earlier by Gmelin
[1788] for the two genera Indri and Avahi. Jourdan [1834] was the first to separate
these two forms.)
Following Hill [1953], we can consider that the species Auahi Zaniger from the
east of Madagascar corresponds to the form called Lemur Zaniger Gmelin [17881,
Lemur brunneus Link [ 17951, Indrz longicaudatus E. Geoffroy [17961, Habrocebus
lanatus Wagner [1840], Lichanotus laniger Illiger [1811], Avahis Zaniger Lesson
[ 18401, Lichanotus avahi Van der Hoeven 118441, Avahis laniger orientalis Lorenz
[1898] (Lorenz wanted to distinguish this form from the western form which he had
just described). The Malagasy people from the eastern coast call it “Avahi“ or
“Vahi,” imitating its loud nocturnal call. The western form, called Auahi Zaniger
occidentalis Lorenz [1898], was described on the basis of a skull and a skin collected
by Voeltzkow in 1892, in northwestern Madagascar, a t Ambundube, near Betsako
to the north of Bombetoka Bay. Its Malagasy name is “Fotsife.”
There is little difference between the two forms, so that certain authors have
hesitated to consider them as subspecies [Tattersall, 19821. They are very similar
in body size (about 460 mm head to tail), and tail-length (about 360 mm). Their fur
is rather woolly, being slightly thicker in the eastern form.
The only clearly visible difference is in the colour of the fur. In the eastern
form it is more rufous, especially at the side of the head, the extremities, and the
tail, with grey hairs with yellow-brown tints a t the extremity, on the upper parts
of the body. The lower parts of the body are ash-coloured, with whitening on the
inner thighs. In the western form the fur is paler with the upper parts and the tail
covered in grey hair, with yellow-green tints at the extremity, whitening at the
face, and brown-yellow hands and feet. The lower body regions are cream-coloured,
like the inner thighs.
The eastern form has long since disappeared from the collection of the Paris
Museum, and this appears to be the case too for the western type specimen, which
was in Vienna Museum. Provisionally, the two forms can be considered to be
represented by two neotypes in the collection in Paris Museum. The eastern form
Cytogenetics and Taxonomy of Avahi laniger i 315
is represented by a male specimen from the Farafangana forest (general catalog
1882 No. 1487, coll. Lanz) and the western form by a male specimen from Ampijoroa in t h e Ankarafantsika (general catalog 1964 No. 71, coll. Blanchot).
The geographic ranges of the two forms are currently widely separated, but it
is likely that they were previously more or less in contact.
The chromosomal differences between the two forms justify modifying their
status by naming the eastern form Avahi laniger [Gmelin, 17881 and the western
form Avahi occidentalis [Lorenz, 18981.
CONCLUSIONS
The cytogenetical study of Avahi laniger occidentalis shows that its karyotype
differs from that of Avahi laniger laniger previously described.
Meiotic chromosomal pairing of hypothetical hybrids would give rise to a tetravalent with a n inversion loop likely to strongly reduce fertility, allowing us to
propose the classification of A. laniger occidentalis in a species apart: Avahi occidental is.
ACKNOWLEDGMENTS
We thank Mr. M. Hauwy and G. Cadiou for their technical assistance, Mrs. M.
Lavaux for her secretarial assistance, Mr. J. Anderson for correcting the English
version of the manuscript, and Mr. J. Devidts for his advice about taxonomy. We
are grateful to the Direction des Eaux et For6ts de Madagascar who has given
permits for the work, to Mr. M. Rabemazava (Ampijoro station) and Dr. C. Koehl
(Strasbourg) who helped us to capture the Avahi, and to the Institut Pasteur of
Madagascar for initiating the fibroblast cultures.
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species, xii, data, lemur, evolution, avahi, lichanotus, apartчavahi, malagasy, bandings, syn, cytogenetic, stud, laniger, classification, favours, occidental, chromosome
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