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Taxonomic status of the Macaques Macaca mulatta Zimm. and Macaca irus Cuvier (= M. fascicularis Raffles)
W. C. Osman Hill
Taxonomic
Royal College of Surgeons of England and Zstitutodi Antropologia, Unioersityof Turin, Zta!v Received
20 March
In preparing inevitable (1964)
Evidence adduced of natural intergradation of Macaca mulatta and M. irus at the area of contact between their respective ranges near the Thai-Burmese frontier, is interpreted as due to casual hybridization and does not warrant reduction of the crab-eating monkey to the status of a subspecies of the rhesus. Data from morphology, physiology and molecular biology militate against the latter conclusion.
1971
of the genus
a synopsis
series of monographs
that I would be impelled
Fooden
(Edinburgh
(now in the American the Thai-Burmese
the reducing
Museum
border.
of iv.
In discussing tail length,
in distinguishing
He makes
no mention
morphology
(except
regards
tail length,
for hf.
irus, while
that
taxa,
conditions Fooden
New York)
of whiskers,
tail thickness or other
barely
might
be regarded
both distinguishing
imperfections
of the two macaques
accepts and the respects.
pigmentation,
penile
of M. irus.
As
in captivity,
conclusions
taxonomists (e.g. Pocock, They also differ markedly
as warranting
admits,
chosen
the range of individual
receive
form a natural
sufficient
posteriorly
in
the conclusions are of relatively variation
collected
confirmation
and from current
it must be pointed
himself
defined
with the fact that the two forms
characters
differ in far more than the two criteria as Fooden
are stated to show some tawny
of the tail in material
that the rhesus and the crab-eater of Fooden’s
differ to a degree,
facial
in both
characteristic
but clearly
such as it is, combined technically
(cf. remarks by Sody, 1949, p. 134). further maintains that his conclusions
eating macaques
side of
male, Fooden
colour of the dorsum,
at root, features
on one female,
value when one considers
and the possible
In rebuttal
01
male
by A. S. Vernay
on the Thai
are transitional
All three specimens
perceptible
Nevertheless,
systematic
which indicate
collected Range
and a juvenile
intermediates
for the baculum)
sympatric,
interfertility
of a subspecies
none a mature
the range of the rhesus makes a southward
two females
length for M. mulatta.
drawn by Fooden. both
History,
village in the Dawna
the two forms, namely
the three
the young male. At its face value the evidence,
unreliable
to the status
irus
both his females fall near or within the range of individual variation the young male’s tail is, though short, still outside the maximum
tinge on the back,
are nowhere
macaque
of M. ins.
and claims
proportionate
of Natural
a mountain
these three specimens,
but two criteria
of my it was
of Fooden
of the crab-eating
on three specimens,
Here, apparently,
salient into the territory
volume
1953-1970)
on the pronouncements
of the relationship
111. mulatta on the basis of some observations in 1924 near B. Umphang,
Press,
(M. mulatta) .
monkey
advocates
in the seventh
University
to pass judgment
to the reassessment
(rtf. Gus) to the Rhesus Briefly,
Macaca for inclusion
on the Primates
with respect
Status of the Macaques
Mucaca mulatta Zimm. and Macaca irus Cuvier (= M. fascicularis Raffles)
within
under
field
from the known
studies on the OS penis. group.
out that the rhesus and crabadopted.
Morphologically
to have induced
earlier
the)reliable
1926; Miller, 1933) to place them in separate subgenera. voice, reproductive physiology and in respect of behaviour,
in other physiological and psychological attributes, and more especially serologically. First, conclusions drawn from relative interfertility must be interpreted realistically. The three intermediates
in question
are not known to be representatives
Journal of HunuwzEcohion
(1972) 1,49-51
of a whole local
50
W.
population members bands
(even
of different
crosses have occurred.
genera)
1953, p. 4). A closely Malay
normally bance
the result of chance
commonly
of different
do.
although
Peninsula,
has been
where
between
It appears
of the ecological
situation
between
the rhesus
them has occurred
in captivity
could be quoted from other mammalian reported
irus and M.
M.
between
a genus, but even intergeneric
us to infer that, for example,
breeding
situation
hybridization
temporarily, to join up, as monkey We know that captive animals often
species within
Many similar exampIes
related
interbreeding.
has occurred
merely
This would not entitle
and the drill are conspecific (see Gray,
HILL
of the two species that happen,
not only members
hybridize;
Lumpur,
OSMAN
and are, in all probability, of bands
groups.
C.
by Bernstein
(1966)
in Kuala
nemestrina are sympatric
without
that, in an area where there has been much distur-
by human
predation
and other activity,
hybridization
these two species.
A lower mammalian
parallel
would
be the fact that,
where
their
ranges
meet,
the
European
brown hare (Lepus europaeus) and the mountain hare (Lepus timidus) have been Yet no zoologist would consider referring them to the same species known to interbreed. because,
for the most part,
among other factors, I am not convinced, any different labelled
(i.e.
that
subspecies)
the rhesus-crab-eater
intermediates
rhesus
each with its own geographical
and
(1963)
may be of diverse
and this,
remarks,
orders
the genetic
of magnitude,
can fall into
crab-eaters
are best
variants.
resolves intself on the degree of the genetic
As Dobzhansky
preference
gene-flow.
and, for the sake of clearness
species,
The basic problem two populations.
each has its own ecological
prevents
therefore,
category,
as separate
in nature
normally
differences
differences
differing
between between
in respect
the races
of few or
many genes. The extreme situation is expressed where races are developing reproductive isolation and are thus being transformed into species, a stage already reached in the case under
consideration,
intermediates.
the gaps between exceptional
save for the casual
Again,
quoting
interbreeding
Dobzhansky
or hybrid
genotypes,
increasing
by Fooden’s
In view of their genetic
or decreasing
implications,
found in 16 macaques
a father Java
or joined
with time.
Such
the serological Wiener
three and
by a few a hybrid
based on reactions
differences established between (1962) tabulates the blood group
from saliva and serum.
All four M.
proved to belong to group B, whilst seven out of eight “Java
and his offspring,
monkey
of genotypes
material.
M. mulatta and M. irus deserve special emphasis. mulatta examined
by Fooden’s
clusters
them may be small or large, wholly discontinuous
cluster is well illustrated
factors
represented
(lot. cit., p. 350),
were of group A;
a single offspring
whose saliva gave a group B reaction,
was group 0.
mated with a mother
monkeys”, A male
of group AB,
produced offspring AB. Since Wiener’s records, eight more M. irus and thirty-two more M. mulatta have been Wiener et al., 1964) with the results in Table 1 tested (Moor- Jankowski et al., 1964; which sufficiently emphasize the genetic apartness of the two species. A further criterion suggesting innate biochemical differences between the two macaques at the moIecular Ievel relates to the infectibility with the malaria1 parasite Phmodium
knowlesi.
This parasite
is a common
mild reactions.
Artificial
West,
& Macdonald,
Manwell
infestation
infestant
in Malaya
of M. Gus, producing,
in M. mulatta induces
a 99.9 % mortality
at most, (Russell,
1963).
In conclusion it should be emphasized that the primary purpose of taxonomy is to provide US with labels wherewith to recognize our material clearly and distinctly and that over-enthusiastic lumping leads to nought but confusion. In the present instance such lumping would undoubtedly result in consternation among those who have based
TAXONOMIC
STATUS
OF
THE
Summary of findings on the human-type blood factors A-B-H and on the Lewis substance in Macaca mulatra and Macaca irus
Table 1
Human type blood factors \ / 0 A B AB
Species Maurca irus present series previous series? .Uacaca mulatta present series previous series1 previous series?
their
researches
Secretion of appropriate blood group substances and of Lewis substance in saliva Lewis Blood group substance substances ww Present Absent Present Absent
Totals
0 1
3 7
4 1
1 3
8 12
8 ND
0 ND
8 12
0 0 0
0 0 0
32 14 4
0 0 0
32 14 4
24 14 ND
8 :D
32 i&
ND = not done; t Wiener, and Wiener et al., 1964.
or are basing
51
MACAQUES
on these commonly
1943;
used monkeys,
total lack of justification
on the grounds
discussed above.
I am indebted
Moor-Jankowski
for providing
to Dr J.
and to Dr MC. Wilson Warren Ga., for supplying
of the Laboratories
the data relative
to Plasmodium
$ Moor-Jankowski
quite
0 0 0 0 ND et al.,
1964
aside from its
me with the data in the table
of Parasite
Chemotherapy,
Chamblee,
spp.
References Bernstein, I. S. (1966). Naturally occurring primate hybrid. Science 154, 1559-1560. Cuvier, F. (1818). Du macaque de Buffon, M&oires da Ma&m nationale d’histoire naturelle Paris 4, 109-120. Dobzhansky, T. (1963). Genetic entities in hominid evolution. In (S. L. Washburn, Ed.), ClassiJcation and Human Evolution. Chicago: Aldine Publ. Co. Fooden, .J. (1964). Rhesus and crab-eating macaques: intergradation in Thailand. Science 143, 363-364. Gray, A. P. (1953). Mammalian Hybrids; Farnham Royal; Commonwealth Agricultural Bureaux. Hill, W. & 0. (1953-1970). Primates, Vols. l-8. Edinburgh: Edinburgh University Press. Miller, G. S. (1933). The groups and names of macaques. In (C. G. Hartman, & W. L. Straus, Eds), The Anatomy of the Rhesus monkey (Macacamulatta). London: Ball&e, Tindall & Cox. Moor-Jankowski, J., Wiener, A. S. & Rogers, C. M. (1964). H uman blood-group factors in non-human Primates. Nature, London 202,663. Pocock, 11. I. (1926). The external characters of the catarrhine monkeys and apes. Proceedings of the Zoological Society London, for 1925, 1479-1579. Raffles, T. S. (1821). Descriptive catalogue of a zoological collection made on account of the Hon. East India Company in the Island of Sumatra and its vicinity; with additional notices illustrative of the natural history of those countries (1820). Transactions of the Linnean SocietyLondon 13, 246. Russell, P. F., West, L. S., Manwell, R. D. & Macdonald, G. (1963). Practical Malariolopy, 2nd. ed. London: Oxford University Press. Sody, H. J. V. (1949). The geographical races of Macaca irus in Notes on some Primates, Camivora and the babirusa from the Indo-Malayan and Indo-Australian regions. Treubia 20, 121-190. Wiener, ,4. S. (1943). Blood Groups and Transfwions, 3rd ed. : Springfield, Ill.: C. C. Thomas. Reprinted by Hafner Publ. Co., 1962, New York City. Wiener, A. S., Moor-Jankowski, J. & Gordon, E. B. (1964). Blood groups of apes and monkeys: V. Studies on the human blood group factors A, B, H and Le. in Old and New World monkeys. American Journal of Physical Anthropology 22, 175-187.
Taxonomic
Royal College of Surgeons of England and Zstitutodi Antropologia, Unioersityof Turin, Zta!v Received
20 March
In preparing inevitable (1964)
Evidence adduced of natural intergradation of Macaca mulatta and M. irus at the area of contact between their respective ranges near the Thai-Burmese frontier, is interpreted as due to casual hybridization and does not warrant reduction of the crab-eating monkey to the status of a subspecies of the rhesus. Data from morphology, physiology and molecular biology militate against the latter conclusion.
1971
of the genus
a synopsis
series of monographs
that I would be impelled
Fooden
(Edinburgh
(now in the American the Thai-Burmese
the reducing
Museum
border.
of iv.
In discussing tail length,
in distinguishing
He makes
no mention
morphology
(except
regards
tail length,
for hf.
irus, while
that
taxa,
conditions Fooden
New York)
of whiskers,
tail thickness or other
barely
might
be regarded
both distinguishing
imperfections
of the two macaques
accepts and the respects.
pigmentation,
penile
of M. irus.
As
in captivity,
conclusions
taxonomists (e.g. Pocock, They also differ markedly
as warranting
admits,
chosen
the range of individual
receive
form a natural
sufficient
posteriorly
in
the conclusions are of relatively variation
collected
confirmation
and from current
it must be pointed
himself
defined
with the fact that the two forms
characters
differ in far more than the two criteria as Fooden
are stated to show some tawny
of the tail in material
that the rhesus and the crab-eater of Fooden’s
differ to a degree,
facial
in both
characteristic
but clearly
such as it is, combined technically
(cf. remarks by Sody, 1949, p. 134). further maintains that his conclusions
eating macaques
side of
male, Fooden
colour of the dorsum,
at root, features
on one female,
value when one considers
and the possible
In rebuttal
01
male
by A. S. Vernay
on the Thai
are transitional
All three specimens
perceptible
Nevertheless,
systematic
which indicate
collected Range
and a juvenile
intermediates
for the baculum)
sympatric,
interfertility
of a subspecies
none a mature
the range of the rhesus makes a southward
two females
length for M. mulatta.
drawn by Fooden. both
History,
village in the Dawna
the two forms, namely
the three
the young male. At its face value the evidence,
unreliable
to the status
irus
both his females fall near or within the range of individual variation the young male’s tail is, though short, still outside the maximum
tinge on the back,
are nowhere
macaque
of M. ins.
and claims
proportionate
of Natural
a mountain
these three specimens,
but two criteria
of my it was
of Fooden
of the crab-eating
on three specimens,
Here, apparently,
salient into the territory
volume
1953-1970)
on the pronouncements
of the relationship
111. mulatta on the basis of some observations in 1924 near B. Umphang,
Press,
(M. mulatta) .
monkey
advocates
in the seventh
University
to pass judgment
to the reassessment
(rtf. Gus) to the Rhesus Briefly,
Macaca for inclusion
on the Primates
with respect
Status of the Macaques
Mucaca mulatta Zimm. and Macaca irus Cuvier (= M. fascicularis Raffles)
within
under
field
from the known
studies on the OS penis. group.
out that the rhesus and crabadopted.
Morphologically
to have induced
earlier
the)reliable
1926; Miller, 1933) to place them in separate subgenera. voice, reproductive physiology and in respect of behaviour,
in other physiological and psychological attributes, and more especially serologically. First, conclusions drawn from relative interfertility must be interpreted realistically. The three intermediates
in question
are not known to be representatives
Journal of HunuwzEcohion
(1972) 1,49-51
of a whole local
50
W.
population members bands
(even
of different
crosses have occurred.
genera)
1953, p. 4). A closely Malay
normally bance
the result of chance
commonly
of different
do.
although
Peninsula,
has been
where
between
It appears
of the ecological
situation
between
the rhesus
them has occurred
in captivity
could be quoted from other mammalian reported
irus and M.
M.
between
a genus, but even intergeneric
us to infer that, for example,
breeding
situation
hybridization
temporarily, to join up, as monkey We know that captive animals often
species within
Many similar exampIes
related
interbreeding.
has occurred
merely
This would not entitle
and the drill are conspecific (see Gray,
HILL
of the two species that happen,
not only members
hybridize;
Lumpur,
OSMAN
and are, in all probability, of bands
groups.
C.
by Bernstein
(1966)
in Kuala
nemestrina are sympatric
without
that, in an area where there has been much distur-
by human
predation
and other activity,
hybridization
these two species.
A lower mammalian
parallel
would
be the fact that,
where
their
ranges
meet,
the
European
brown hare (Lepus europaeus) and the mountain hare (Lepus timidus) have been Yet no zoologist would consider referring them to the same species known to interbreed. because,
for the most part,
among other factors, I am not convinced, any different labelled
(i.e.
that
subspecies)
the rhesus-crab-eater
intermediates
rhesus
each with its own geographical
and
(1963)
may be of diverse
and this,
remarks,
orders
the genetic
of magnitude,
can fall into
crab-eaters
are best
variants.
resolves intself on the degree of the genetic
As Dobzhansky
preference
gene-flow.
and, for the sake of clearness
species,
The basic problem two populations.
each has its own ecological
prevents
therefore,
category,
as separate
in nature
normally
differences
differences
differing
between between
in respect
the races
of few or
many genes. The extreme situation is expressed where races are developing reproductive isolation and are thus being transformed into species, a stage already reached in the case under
consideration,
intermediates.
the gaps between exceptional
save for the casual
Again,
quoting
interbreeding
Dobzhansky
or hybrid
genotypes,
increasing
by Fooden’s
In view of their genetic
or decreasing
implications,
found in 16 macaques
a father Java
or joined
with time.
Such
the serological Wiener
three and
by a few a hybrid
based on reactions
differences established between (1962) tabulates the blood group
from saliva and serum.
All four M.
proved to belong to group B, whilst seven out of eight “Java
and his offspring,
monkey
of genotypes
material.
M. mulatta and M. irus deserve special emphasis. mulatta examined
by Fooden’s
clusters
them may be small or large, wholly discontinuous
cluster is well illustrated
factors
represented
(lot. cit., p. 350),
were of group A;
a single offspring
whose saliva gave a group B reaction,
was group 0.
mated with a mother
monkeys”, A male
of group AB,
produced offspring AB. Since Wiener’s records, eight more M. irus and thirty-two more M. mulatta have been Wiener et al., 1964) with the results in Table 1 tested (Moor- Jankowski et al., 1964; which sufficiently emphasize the genetic apartness of the two species. A further criterion suggesting innate biochemical differences between the two macaques at the moIecular Ievel relates to the infectibility with the malaria1 parasite Phmodium
knowlesi.
This parasite
is a common
mild reactions.
Artificial
West,
& Macdonald,
Manwell
infestation
infestant
in Malaya
of M. Gus, producing,
in M. mulatta induces
a 99.9 % mortality
at most, (Russell,
1963).
In conclusion it should be emphasized that the primary purpose of taxonomy is to provide US with labels wherewith to recognize our material clearly and distinctly and that over-enthusiastic lumping leads to nought but confusion. In the present instance such lumping would undoubtedly result in consternation among those who have based
TAXONOMIC
STATUS
OF
THE
Summary of findings on the human-type blood factors A-B-H and on the Lewis substance in Macaca mulatra and Macaca irus
Table 1
Human type blood factors \ / 0 A B AB
Species Maurca irus present series previous series? .Uacaca mulatta present series previous series1 previous series?
their
researches
Secretion of appropriate blood group substances and of Lewis substance in saliva Lewis Blood group substance substances ww Present Absent Present Absent
Totals
0 1
3 7
4 1
1 3
8 12
8 ND
0 ND
8 12
0 0 0
0 0 0
32 14 4
0 0 0
32 14 4
24 14 ND
8 :D
32 i&
ND = not done; t Wiener, and Wiener et al., 1964.
or are basing
51
MACAQUES
on these commonly
1943;
used monkeys,
total lack of justification
on the grounds
discussed above.
I am indebted
Moor-Jankowski
for providing
to Dr J.
and to Dr MC. Wilson Warren Ga., for supplying
of the Laboratories
the data relative
to Plasmodium
$ Moor-Jankowski
quite
0 0 0 0 ND et al.,
1964
aside from its
me with the data in the table
of Parasite
Chemotherapy,
Chamblee,
spp.
References Bernstein, I. S. (1966). Naturally occurring primate hybrid. Science 154, 1559-1560. Cuvier, F. (1818). Du macaque de Buffon, M&oires da Ma&m nationale d’histoire naturelle Paris 4, 109-120. Dobzhansky, T. (1963). Genetic entities in hominid evolution. In (S. L. Washburn, Ed.), ClassiJcation and Human Evolution. Chicago: Aldine Publ. Co. Fooden, .J. (1964). Rhesus and crab-eating macaques: intergradation in Thailand. Science 143, 363-364. Gray, A. P. (1953). Mammalian Hybrids; Farnham Royal; Commonwealth Agricultural Bureaux. Hill, W. & 0. (1953-1970). Primates, Vols. l-8. Edinburgh: Edinburgh University Press. Miller, G. S. (1933). The groups and names of macaques. In (C. G. Hartman, & W. L. Straus, Eds), The Anatomy of the Rhesus monkey (Macacamulatta). London: Ball&e, Tindall & Cox. Moor-Jankowski, J., Wiener, A. S. & Rogers, C. M. (1964). H uman blood-group factors in non-human Primates. Nature, London 202,663. Pocock, 11. I. (1926). The external characters of the catarrhine monkeys and apes. Proceedings of the Zoological Society London, for 1925, 1479-1579. Raffles, T. S. (1821). Descriptive catalogue of a zoological collection made on account of the Hon. East India Company in the Island of Sumatra and its vicinity; with additional notices illustrative of the natural history of those countries (1820). Transactions of the Linnean SocietyLondon 13, 246. Russell, P. F., West, L. S., Manwell, R. D. & Macdonald, G. (1963). Practical Malariolopy, 2nd. ed. London: Oxford University Press. Sody, H. J. V. (1949). The geographical races of Macaca irus in Notes on some Primates, Camivora and the babirusa from the Indo-Malayan and Indo-Australian regions. Treubia 20, 121-190. Wiener, ,4. S. (1943). Blood Groups and Transfwions, 3rd ed. : Springfield, Ill.: C. C. Thomas. Reprinted by Hafner Publ. Co., 1962, New York City. Wiener, A. S., Moor-Jankowski, J. & Gordon, E. B. (1964). Blood groups of apes and monkeys: V. Studies on the human blood group factors A, B, H and Le. in Old and New World monkeys. American Journal of Physical Anthropology 22, 175-187.