Biol. 3 Linn. SOC.,1. p p 77-84. With 1 plate
ApriZ 1969
Speciation in Madagascan Lemurs
J. J. PETTER
Laboratoire d’Ecologie du Museum de Paris, Brunoy
Nous nous sommes efforcts depuis 1957, date de nos premibres recherches h Madagascar] de
prtciser les caractbres systtmatiques des difftrentes espbces de Ltmuriens.
Sans minimiser l’importance des critbres morphologiques, nous nous sommes jusqu’h
maintenant appliquts, par des ttudes tco-tthologiques de mieux connahre les difftrentes formes
existantes et de prtciser leurs caractbres distinctifs. Les etudes ont t t t mentes sur le terrain au
cours de plusieurs missions et en captivitt dans la station de recherche de Tananarive et au
Laboratoire de Brunoy, en France.
C‘est ainsi que nos ttudes nous ont amen6 A revenir, par exemple, pour les Ltmurs, h la
classification de Schwarz groupant en une seule espbce toute une strie de formes de Lemur et
A les considtrer comme des sous-espbces de I’espbce Lemur m c a c o .
Les recherches sur les chromosomes faites par plusieurs chercheurs ces demibres anntes soulevent cependant quelques probltmes car on a trouvt des formules chromosomiques difftrentes
pour des animaux fort semblables h beaucoup de points de w e . Nous avons chercht tous les
cas d’hybrides connus et tent6 nous-mCmes, et avec R. Albignac chercheur de l’O.R.S.T.0.M.
B Tananarive de rtaliser toutes les hybridations possibles en captivitt.
C’est un aperqu de ces recherches en cours que nous avons voulu exposer, ainsi que quelques
observations nouvelles sur les hybrides obtenus.
L’tvolution des espbces le plus souvent sociales et territoriales posent des problbmes t r h inttressants et Madagascar nous offre encore Ace point de vue un champ d’ttude priviltgi6 qu’il faut
utiliser avant qu’il ne soit trop tard A cause des destructions de plus en plus rapides du milieu
forestier. Nous avons ainsi pu faire quelques observations dans la nature, notamment sur la
variabilitt au sein des groupes, qui nous permettent 21 faire quelques hypotheses sur les
mtcanismes de I’tvolution des LCmuriens h Madagascar. I1 semble que le territorialisme de la
plupart des Ltmuriens favorise la formation d’homozygotes ce qui a peut-&re pour consequence
d’acctltrer la sptciation. Beaucoup de questions concemant de nombreuses espbces restent
cependant encore sans rtponse et il faut se garder de trop vouloir dtduire des observations
fragmentaires que nous possbdons. Des etudes plus pousskes sur le terrain et particulibrement
dans certaines regions qui servent de limites 2I des sous-espbces nous paraissent inttressantes A
encourager dans l’avenir pour avoir une idte plus prtcise de l’tvolution du groupe.
CONTENTS
Introduction
.
Lemur hybridization experiments .
.
Hybridization in other genera
.
Variation within subspecies.
.
Eco-ethological influences on distribution
Territorial behaviour and inbreeding
Conclusions
.
References
.
.
.
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INTRODUCTION
When we study the lemur group in the Madagascan forests we are immediately
struck by the large variety of different forms which live in a relatively small area.
Whether in the eastern or western forest of Madagascar, we find everywhere a wide
range of subspecies of Lemur, Propithem and other species, which differ from each
other in minor physical features, especially the colour of their fur.
78
J. J. PETTER
For a long time now, classificationof all these varieties has posed taxonomic problems,
owing to the scarcity of specimens, the multiplicity of names which have been given to
them, and the lack of precision in their geographical location (a larger number of the
lemur skins in the old collections have for locality only Madagascar).
It was in 1875, when Grandidier published the Histoire nuturelle et Politique de
Muduguscur that the first important studies of lemurs began. Even so, for a long time,
museum collections remained very poor. The Anglo-Franco-American expedition
which ended in 1931,most of whose mammal collection is in London, provided the
first opportunity for serious studies. Schwarz (1936)was able, as a result, to begin the
revision of the lemur group, and put forward interesting theories on its evolution.
Hill (1953)in his book on the Strepsirhini adopted Schwarz’s major ideas. In our
work on the Madagascan lemurs in 1957,we have again taken up the taxonomic work of
Schwarz and have attempted to complete this as well as studying the ecology of several
species. During these observations, mainly carried out in the field, and later during
several other visits to Madagascar, we realized how difficult it is to obtain reliable
documentation on the accurate geographical distribution of the different species.
As these animals are disappearing, it is now forbidden to catch lemur specimens
for a collection, except for a special study, and the classification of the subspecies as
well as their precise locality entails long detailed study, which must be undertaken by
research workers properly trained beforehand in the recognition of the skins. A recent
Madagascan law for the protection of fauna forbids people to have lemurs as pets and
leads to the seizure of numerous animals which are subsequently housed at the
Biological Centre of O.R.S.T.O.M. in Tananarive. This law has helped to improve
our knowledge of the species by allowing the comparative study of captive animals.
Unfortunately, in this case as well, the exact origin of the animals is often unknown.
For these reasons, if we now know (more or less) the geographical distribution
of the different species, the limits of their habitat are in most cases not yet very precisely
defined.
LEMUR HYBRIDIZATION EXPERIMENTS
Chu & Bender (1962)undertook a detailed study of the chromosome formula of
Madagascan lemurs. They were able to determine that the chromosome number (272)
of the genus Lemur varies according to the species from 44 to 60.These studies are,
however, still very incomplete and the chromosome formulae of numerous subspecies
are still to be determined.
The results already obtained, however, allow us to record some interesting facts
among the Lemur genus.
Subsequent to the findings of Schwarz we have been able to segregate many species
into subspecies :
Lemur wariegatus (or Vurecia wuriegutu) with two subspecies:
L. w. wuriegutur Kerr, 1792 (46chromosomes)
L. w. ruba Gray, 1870 (46chromosomes)
SPECIATION
IN MADAGASCAN
LEMURS
79
Lemur macaco with at least seven subspecies:
L. m. macaco LinnC, 1766 (44chromosomes)
L. m. albifrons (E. Geoffroy), 1796 (60chromosomes)
L. m. fulvus (E.Geoffroy) 1812 (eastern form 48 chromosomes
western form 60 chromosomes)
L. m. collaris (E.Geoffroy), 1812 (48 and 54 chromosomes)
L . m. rufus (Audebert), 1800 (60 chromosomes)
L. rn.Jlavijrons (Gray), 1867 ( ? chromosomes)
L. m. sunfordi (Archbold), 1932 ( ? chromosomes)
Lemur mongox with two subspecies:
L. m. mongox Linnt, 1766 (60 chromosomes)
L. m. coronatus Gray, 1842 ( ? chromosomes)
Lemur catta Linnt, 1758 (56 chromosomes)
Lemur rubriventer I. Geoffroy, 1850 ( 1 chromosomes)
In Lemur macaco the chromosomes of two subspecies, rare in captivity, have not
yet been studied. The same applies to Lemur mongox mongox and Lemur rubriventer.
This division into species and subspecies was generally made intuitively by observation of the characteristics of the cranium and of the skins.
We have ourselves completed this study by observation of living animals. There is a
very great likeness between the different subspecies of Lemur macuco. These lemurs
are the same size; we cannot differentiate between them by study of their crania, their
behaviour is similar, and their cries are very alike. Furthermore, they all have a sexual
dichromatism. From the point of view of serum proteins and haemoglobins, there is
nothing to differentiate them (Goodman, 1962; Buettner Janusch, 1964). However,
they identify themselves distinctly by the colour of their fur and they have different
living areas.
In published works there are numerous references to cross-breeding between the
different forms of Lemur macaco which Gray reviewed in 1954. Later authors (for
example Moog, 1959) give other cases. These observations were made in various
zoological gardens.
Apart from certain observations which are entirely reliable, many others leave a
degree of doubt due to the difficulty of determining the exact identification of the subspecies.
This lack of experimental data led us, with R. Albignac, a zoologist living at the
Research Institute (O.R.S.T.O.M.) in Tananarive, to try a whole series of breeding
experiments. Three years ago Albignac reorganized the breeding installations of
Tananarive and it was therefore possible to carry out true experimental work.
The attempts which turned out to be successful were the following crosses:
In 1965
Male L. m. fulvus x female L. m. rufus+F1 female
The hybrid female is very similar to the mother but its colour is generally darker and
greyer ;the supraorbital spots are lighter.
J. J. PETTER
80
In 1966
Male L . m. fulvus x female L . m. albifLons+F1 male
The hybrid male is very similar to a male L . m. albt@vns, but its head-cap is smaller and
a darker shade of white.
Male L. m. fulvus x female L . m. rufw (the same as in 1965)+F1 male
The hybrid male is very similar to a male L. m. rufw but its head is lighter.
In 1967
Two second-generation hybrids were obtained by crossing :
(1st male hybrid of L. m. fulvus x L . m. albifions) x female L . m. albifrons
(female hybrid of L. m. f u l m x L . m. rufus) x male L . m. fulvus
This same year there were also the following hybrids :
Male L . m. macaco x female L . m. collaris+F1 female
This hybrid has yellow tinged rufous fur. Its head is entirely greyish like its mother ;
but it has rufous side-whiskers and white ears like its father.
Male L. m. macaco x female L . m. rufus-. F1 female
Above the eye, the hybrid’s fur is grey, unlike its mother’s white supraorbital spots.
It has rufous side-whiskers and white ears like its father.
These interesting experiments will be pursued with other subspecies and as soon
as possible we shall obtain the chromosome formulae for the hybrids.
An interesting hybridization of female L . rubriventer x male L . m.filvus, was obtained
in 1966 in the small zoological park of Asson in the Pyrenees by the St Pie brothers,
who are in touch with our laboratory. Unfortunately, the young hybrid died a week
after birth.
L . rubriwenter and L. macaco are quite different in skull characteristics: the former
has a well-developed palatine sinus which forms a big lump in the eye socket, This
Lemur, which is the same size as L . macaco, has uniform chocolate-brown fur (a shade
not found in other Lemur) and a black tail. Its distribution overlaps that of various
subspecies of Lemur maeaco.
This cross-breeding between two ‘species’ prompts us to try crossing Lemur catta
with Lemur macaco, despite the poor chances of success anticipated. For this purpose
Albignac proposes to settle several couples in cages in Tananarive.
HYBRIDIZATION IN OTHER GENERA
In 1960 we succeeded in cross-breeding two subspecies of Cheirogaleus major:
male C. m. crossleyi Grandidier, 1870 (north-east form) x female C. m. major Geoffroy,
1812 (centre-east and south-east form).
Cheirogaleus major is a small nocturnal lemur and the two subspecies are easily
recognizable when alive. The first one is smaller in size, has a redder fur with more
marked circumocular spots, and a more pointed muzzle than the second. The two
hybrids born were male and looked like their father.
Despite several efforts we have not yet succeeded in cross-breeding two subspecies
of Microcebus murinus but we still believe this to be possible. Twice a female M. m.
SPECIATION IN
MADAGASCAN
LEMURS
81
rufus (Geoffroy, 1928) (eastern form) has been killed by a male M. m.murinus (Miller,
1777) (western form), which is a little larger in size. The first female stayed three weeks
with the male and was beginning a gestation when she died of her wounds. T h e second
female died after three days with the male.
In 1956 and 1957, during our first stay in Madagascar, a couple of Propithecus
verreauxi kept alive in captivity by Professor R. Paulian and ourselves, as a result of
very careful treatment, reproduced twice. The cross was here a male P. o. coronatus
Milne Edwards, 1871 x female P . v . deckeni Peters, 1870. The former is white with a
black head cap, the second is entirely white. The hybrid males had a brownish head,
cap and fur tinged brown-red. They unfortunately died shortly after our departure.
One was 18 months old, the other six months old. (See Plate 1.)
Last year Albignac obtained reproduction between a P . o. coquereli Milne Edwards,
1867, white with large brown-red spots on the breast and anterior part of the limbs,
and a P. v . verreauxi Grandidier, 1867, all white except for a black head cap. The
hybrid has a white body except for the breast and the top of the limbs which were light
brown. The head had no trace of a black cap. This one died a year after birth.
These two subspecies of Propithecus have the same number of chromosomes 2n = 48.
They are the only Propithecus whose chromosome numbers are known.
A lot of experimental cross-breeding has still to be carried out, but we are hopeful
that this will be done in the near future.
VARIATION WITHIN SUBSPECIES
The interest of these experimental crosses is in showing that they are possible and
that they could probably occur in nature. They show, too, the very relative value of
lemur classification into species and subspecies. Observing Lemur or Propithecus in
their natural habitat also provokes critical consideration of accepted taxonomy.
It is in fact strange to observe the variation of specimens which can be found in the
distribution area of a given subspecies. We have established this with the subspecies
L. m. altifrons, for example, where we noticed on living animals, captured to the north
and south of the Baie d’Antongi1, variation in the size of the white spot on the forehead.
We saw it, too, in L. mongox coronatus living in the north of Madagascar, which presented variations in the shade of the body fur, according to the population area. The
same phenomenon was pointed out for L. macaco collaris in the south-east,
Jolly (1966) in her study in the south of Madagascar, also verified the same tendencies
in Propithecus verreauxi verreauxi Grandidier 1867, where some populations are
dimorphic containing a proportion of melanistic individuals.
Similar facts were pointed out in 1953 for P. o. coronatus by R. Paulian who was
struck by the external variability of the different populations of Propithem between the
Betsiboka river Maintirano, and the Bongola, in the west of Madagascar.
There is, in addition to this variability between the lemur populations, individual
variability within the troop which seems very strong. When we are able to get near
them, it is for instance always possible to recognize the individuals of a Lemur group.
Likewise in an Hapalemur group, even though they are all the same homogenous colour,
with binoculars we can clearly make out the difference of physiognomy between
individuals.
6
82
J. 3. PETTER
ECO-ETHOLOGICAL INFLUENCES ON DISTRIBUTION
When we consider the geographical distribution of the different types of Madagascan
lemur, we wonder why some are very localized in geographical subspecies (Lemur
macaco for example), while others, on the contrary, like Lemur rubtiventer, have a very
wide distribution. This lemur is found throughout the east, north and south of Madagascar and we believe that ecological and geographical considerations help us to understand this phenomenon. Unlike the subspeciesof Lemur macaco, L . rubriventer likes high
ground. While most of the rivers are very wide in their lower reaches and there create
almost insurmountable barriers for the Lemur macaco, they are easily crossed higher up
by Lemur rubtiventer.
It seems that similar considerationscould explain the very wide distribution (without
apparent division into subspecies) of Hapalemur griseus (Link, 1795), a species which
can be found throughout Madagascar, except in the extreme south, and which lives as
well on the sea coast as on high ground. Additional characteristics, such as its ‘aquatic’
tendencies and its preference for bamboo groves, which, no doubt, provide a very
effectiveprotection against its natural enemies, have probably allowed this species to
develop over such a vast and exceptional distribution.
We have recently had the opportunity of examining in detail this Hapalemur as well
as H.sirnus Gray, 1870, a very similar species. H. sirnus lives isolated in the Phrugmites
reeds and in the papyrus swamps of Lac Alaotra. It is partly ‘aquatic’(in that it swims
voluntarily and when pursued) which is unique among the lemurs, and which one could
compare with that of the African talapoin monkeys. Its ‘aquatic’ behaviour, which is
still more highly developed than that of H . griseus, could have led it (by contrast with
the former) to a strictly localized geographical distribution as lake and marshy habitats
receded in Madagascar.
The speciation of lemurs in Madagascar seems therefore to be explained by a wellmarked subdivision of the country due to the mountainous topography and numerous
rivers, but eco-ethological influences could also have played a part.
TERRITORIAL BEHAVIOUR AND INBREEDING
Another factor, the territorial behaviour of the lemurs, should also be considered if
we wish to understand better their evolution.
The field studies which we made during several visits to Madagascar, as well as the
work of other research workers such as A. Jolly and the current studies of R. Martin,
confirm that most lemurs have well-defined territorial habits. We ourselves observed
among the subspecies of L. macaco and Propithecus verreauxi many examples of the
defence of territory. Lemurs in addition, without exception, mark their home ranges
(they nearly all have special glands for this purpose) and loudly signal their presence by
their cries.
We also established that where there is a large concentration of animals (this is
rare today but must have been the rule in the past), the family groups (Propithecus)or
the larger groups (Lemur macaco) stay faithful to a home range whose area seems proportional to the apparent richness of vegetation. The different territories of the neighbouring groups are contiguous in areas where the population is dense.
SPECIATION
IN MADAGASCAN
LEMURS
83
As soon as a home range, occupied by a population, is large in relation to the possibilities of individual movements, the animals normally choose their mates among their
geographical neighbours and this process repeats itself throughout the generations.
This attachment to a territory results, therefore, in a certain consanguinity, and crossing
between individual neighbours belonging to neighbouring groups tends to be done
between ‘best enemies’.
Inbreeding and the separation of occupied areas by river barriers prevents panmixia.
These habits are therefore completely favourable, from a genetic point of view, for the
preservation of mutations, and favour the appearance of homozygotes.
All members of consanguinous families are likely to display some of the same
characteristics. This resemblance of a particular characteristic of different members of
the same group is easily noticeable among the Propithecus of the west and south. A.
Jolly notes for example among Propithems oerreauxi oerreauxi certain characteristics
such as the boundary of the head cap or small spots on the face which were similar
among different members of the same troup.
CONCLUSIONS
We often tend to think that speciation is more active in a tropical climate. For one
thing, heat certainly has a tendency to increase the frequency of mutations, but other
factors could also have an influence in Madagascar. One notices, for example, a strong
tendency towards melanization among the Propithecus in the south and south-east
where radioactivity is strongest from the thorianite deposits.
As a consequence of territorial attachment, inbreeding results in homozygosity,
which being more exposed to selection by the environment, makes such selection more
efficient for or against recessive genes and could thus accelerate evolution.
The ravages resulting from human action naturally upset all evolutionary processes
of this group which, for so long, developed without interference. The Madagascan
climate has remained stable and there was no important biological invasion for millions
of years. One could imagine that, before man arrived, the physical and biological conditions of the habitat tended to increase the fitness of the population and therefore its
numbers. This is confirmed by the fact that, only a short time ago, in many regions the
lemur populations were quite considerable. We could still see this ten years ago in
Propithecus, Lepilemur and Lemur of the Ankarafantsika Reserve.
Some precise observations, and some others not so precise, allow us to elaborate a
hypothesis. We must not, however, imagine that we know everything about the ecoethology of lemurs. For instance, for numerous species the territorial instinct seems less
strong during certain periods of the year. Several times we observed gatherings of
neighbouring groups during short periods, and this for various species. If some species
are home-abiding, it is not the case for all species, and the case of L. rubriventer still
poses many problems. This is not a widely spread species, always timid, and we never
found large populations. It seems that in the lemurs and Propithecus whose size is
large enough to protect them from predators, the colour represents a neutral element
not submitted to environmental pressure. It is not the same for smaller lemurs, which
all have dark brownish coloration. It may be for this reason that in Hapalemur,
84
J. J. PBTTER
for example, no chromatic variability appeared by selection pressure from predators.
Many mysteries remain relating to various other species which cannot be easily
observed, as for example, Propithem diadenra, Lemur variegatus, Microcebus murinus,
Phaner furcifer and L e p i h u r mustelinus. A more detailed eco-ethological study of
these species would perhaps allow us to understand better the evolution of all the
lemur group.
REFERENCES
BUETTNER
JANUSCH,
J. & BUBTTNER
JANUSCH, V., 1964. Hemoglobins of primates. In J. Buettner Janusch
(ed.) Evolutionary andgenetic biology of primates. 2 : 75-91. New York and London.
C m , E. H. Y.& BENDER,
M. A., 1962. Cytogenetics of the primates and primate evolution. Ann. N. Y.
Acad. Sci. 102: 253-266.
GOODMAN,
M., 1962. Immunochemistry of the primates and primate evolution. Ann. N . Y. Acad. Sn'.
102: 219-234.
GRANDIDIER,
A., 1875. Histoire Physique Naturelle et Politique de Madagascar VI. MammyJres. Pans.
GRAY,A. P., 1954. Mammalian Hybrids. (A check list with Bibliography.) C.A.B. England.
HILL,W. C. O., 1953. Primates: Comparative anatomy and taxonomy. I Strepsirhini. Edinburgh
University Press.
JOLLY, A., 1966. Lemur Behavior. Chicago and London: The University of Chicago Press.
MOOG,
G., 1959. Geburt eines bastardes Mohrenmaki x Schwartzkopfmaki im Zooloogischen Garten
Saarbrticken.2001.
Gart. 25: 99-104.
PETTER,J. J., 1962. Recherches sur 1'Ecologie et l'Ethologie des Ldmuriens malgaches. Mkm. Mus.
nut. Hist. nut. (Ser. A), 27: 1-146.
SCHWARZ,
E., 1931. A revision of the genera and species of Madagascar Lemuridae. Proc. Zool. SOC.
Lond. Pt. 1: 399428.
Scnwm, E., 1936. A propos du 'Lemur macaco' Linnaeus. Mammalia, T.I., 1: 25-26.
EXPLANATION OF PLATE
PLATE1
Hybridization of subspecies of Propithecus veneauJn'.
A. Male Propithecus vmeauxi coronatus.
B. Female Propithecus veneaum' deckeni, with hybrid young on her back.
C. The hybrid (a male) produced by crossing the male P.u. coronatus x female P. u. deckeni.