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Blood groups of bonnet macaques (Macaca radiata) with a brief introduction to seroprimatology.

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Blood Groups of Bonnet Macaques (Macaca radiata),
with a Brief Introduction to Seroprimatology
W. W. SOCHA, J. MOOR-JANKOWSKI, A. S. WIENER,
D. R. RISSER AND H. 'PLONSXI
Primate Blood Group Reference Laboratory and W o r l d Health Organization
Collaborating Center f o r Primate Hematology, Laboratory f o r Experimental
Medicine and Surgery in Primates ( L E M S I P ) o f t h e N e w York University
School of Medicine, and t h e Department of Anthropology, University of
California, Davis, California
KEY W O R D S Macaques . Bonnet macaques . Crab-eating
macaques . Primates . Blood groups . Seroprimatology.
ABSTRACT
The human-type A-B-0 blood groups of 52 bonnet macaques
( M a c a c a radiata) were determined. Application of method of population genetics indicated the gene frequences to be 0 = 0.173, A = 0.480 and B = 0.347.
Cross testing of sera and red cells of the bonnet macaques revealed two bloodtype-specific isoagglutinins, one of them strong enough for use as a blood typing
reagent. No blood group polymorphism was revealed by testing bonnet macaque
red cells with isoantisera produced in rhesus monkeys ( M . mulatta) and in crabeating macaques ( M . fascicularis). The rhesus and crab-eating macaque isoantisera reacted either with all or with none of the bonnet macaque red cells
tested.
The present report is the continuation
of our studies on what we have defined as
the human-type (Wiener, Moor-Jankowski,
Gordon and Shell, '66), and simian-type
blood groups of apes and monkeys (MoorJankowski and Wiener, '65). This work
began with our early discovery of human
blood factor M in the rhesus monkey
(Landsteiner and Wiener, '37) and has resulted in about 150 publications providing
an over-view of the presence and distribution of both human-type and simian-type
blood groups in various species of apes and
monkeys, most recently summarized in
1972 (Moor-Jankowski and Wiener).
The importance of this body of information for anthropology lies mainly in the recognition of the presence in simians of blood
groups homologous (Wiener et al., '72),
i.e., human-type, and analogous, i.e., simian-type, to the human blood groups. In the
course of our work, it became apparent
that some of the simian-type blood groups
detected by the isoimmune sera prepared
by us in one species had homologues in
other primate species in which these
antisera detected polymorphic blood group
kM.
I.
PHYS. AhTHROP., 45: 485-492.
differences, viz, chimpanzee C-E-F system
in orangutans and gorillas (Moor-Jankowski et al., '73b) and rhesus monkey isoantisera showing polymorphisms in crabeating macaques (Moor-Jankowski et al.,
'67). On the other hand, there also exist
isoantisera produced in one species which
react with all or none of the red cells of
other primate species tested as shown in
the present article.
The observed cross reactions of blood
grouping sera with red cells of various
primate species have been developed into
a new taxonomic approach to the study of
nonhuman primates, as outlined in two
recent papers (Moor-Jankowski et al., '73a;
Moor-Jankowski et al., '74). Moreover,
already in 1964 (Moor-Jankowski and
Wiener, '65) we observed statistically significant differences between the distributions of blood groups in two population
groups of baboons of different origins. Further studies have enabled us to extend this
observation to differences i n blood group
distribution among populations of chimpanzees (Moor-Jankowski et al., '66), to
larger series of baboons (Wiener and Moor-
485
486
SOCHA, MOOR-JANKOWSKI, WIENER, RISSER AND PLONSKI
TABLE 1
Results of A-B-H grouping of a series of 52 bonnet macaques (Macaca radiata)
Reactions given by
Serum 1
Saliva
Typical results
A and H
B and H
A, B and H
Atypical results a
A and H
A, B and H
A, B and H
A, B and H
Incompletely tested
Not done
Not done
Not done
Presumed
blood group
Number of
animals
Anti-B
Anti-A
None
A
B
AB
18
12
15
Anti-B, weak anti-A
Anti-A, anti-B
Anti-B
Weak anti-A
A
AB
AB
AB
1
1
Anti-B
None
Anti-B and weak
A
AB
A
1
1
1
1
1
anti-A,
~
1 As determined after absorption with human group 0 red cells. (Before absorption titers for human group 0 red cells ranged from less than 1 up to 8 units by saline agglutination method.)
2 Not conforming with Landsteiner's rule.
The saliva samples were tested by the
quantitative inhibition technique for the
presence of the A-B-H blood group substances. The serum samples were tested
for anti-A and anti-B agglutinins after preliminary absorption with human group 0
red cells. The red cells were tested for
simian-type agglutinogens by using our isoand cross-immune sera prepared in rhesus
monkeys and in stump-tailed macaques
(Wiener et al., '73). The red cells and
sera of the bonnet macaques were crossmatched against one another.
All the tests performed in our Primate
Blood Grouping Reference Laboratory were
carried out by the same methods as used
MATERIALS AND METHODS
for typing of human beings for clinical and
All the animals studied were maintained forensic purposes, which have to guaranby the California Primate Research Center tee precise, reproducible results. Thus, only
at the University of California, Davis, Cali- specific reagents were used, the high pofornia. Eight of the animals tested were tency of which was confirmed by titration
wild-caught, while all the remaining ani- against control red cells of known types
mals were born since establishment of the routinely included in every experiment. DeColony at the Primate Center. The animals tails of methodology have been described
tested therefore did not constitute a pan- elsewhere (Socha et al., '72a; Erskine, '73).
mictic population. The blood and saliva
RESULTS
samples were collected under the supervision of one of us (D.R.R.) and shipped by
The results of tests for human-type
air mail to the Primate Blood Group Refer- A-B-0 blood groups are shown in table 1.
ence Laboratory at the Laboratory for Ex- With only relatively few exceptions, Landperimental Medicine and Surgery in Pri- steiner's modified rule holds i n bonnet mamates, New York. The saliva specimens caques, namely, those and only those aghad been inactivated by boiling for twenty glutinins (anti-A or anti-B) are present
minutes immediately after collection, be- in the serum for which the corresponding
fore being shipped.
group-specific substances are absent from
Jankowski, '69) and to gibbons (MoorJankowski and Wiener, '67), thus estabishing a new discipline of seroprimatology
(Moor-Jankowski and Wiener, '67), analogous to the discipline of seroanthropology,
viz the study of the distribution of blood
groups in various human populations, as
initiated by the Hirszfelds (Hirszfeld and
Hirszfeld, '19), and expanded in modern
times by Mourant ('75) and by Ruffik
(Bernard and Ruffik, '66).
The present paper reports on the results
of the extension of our blood grouping tests
to a series of bonnet macaques (Macaca
radiata).
487
BLOOD GROUPS OF BONNET MACAQUES (MACACA RADIATA)
TABLE 2
Results of cross absorption experiments with red cells of bonnet and rhesus macaques using
antisera prepared in. rhesus monkeys and crab-eating macaques
Antisera
Anti-Grli
(Rh-216)
Anti-Crli
( Rh-4 )
Anti-Brh
(Rh-2)
Java monkey (J-1)
( anti-rhesus )
Titers for
M . radiata
M . mulatta
64
M . radiata
M . mulatta
Absorbed with
red cells of
M. radiata
Absorbed with
red cells of
M. mulatta
0
0
0
256
64
4
0
4
0
M . radiata
M . mulatta
12
6
0
0
0
0
M . radiata
16
128
M . mulatta
1
Unabsorbed
10
2
0
0
128
4
Species specific.
the saliva. As in other species of Old World
monkeys (Moor-Jankowski and Wiener,
'72), the red cells of bonnet macaques
failed to agglutinate with anti-A or a n t i 3
or anti-H reagents. The human-type A-B-0
blood groups were readily determined for
the great majority of the animals; 18 monkeys were clearly group A, 12 were group
B and 15 were group AB, but no group 0
animals were encountered. In four animals,
the sera contained agglutinins in addition
to those expected by Landsteiner's rule, as,
for instance, a monkey with A and H in
the saliva and weak anti-A as well as
anti-B in the serum (see table 1, atypical
results). These additional agglutinins did
not react as auto-antibodies in bonnet macaques, but solely against human group A
red cells. A similar situation had been encountered by us in baboons (Moor-Jankowski et al., '65) and is explained by the
different chemical nature of the group A
substance on red cells and in secretions.
Therefore, the blood groups of these animals were determined on the basis of the
blood group substances present in their saliva, and confirmed by the strong reciprocal
agglutinins present in their sera, while
weak additional agglutinins were discounted. Sera but not saliva had been received
for three of the monkeys; the A-B-0 blood
groups of those monkeys were inferred by
applying Landsteiner's rule and discounting any very weak agglutination reactions.
The gene frequency analysis was based
solely on the results for 45 animals for
which complete, entirely typical reactions
were obtained. From the observed fre-
quencies of blood groups: 0 = 0.0, A 5
0.4000, B = 0.2667, AB = 0.333, by using
the method of direct count, the gene frequencies prove to be A = 0.5667 and B =
0.4333, if one assumes gene 0 to be absent
from this species.
If from these estimated gene frequencies
one calculates the expected frequencies of
the blood groups and tests for goodness of
fit, one obtains xZtr,= 4.64 so that P <
0.05.
The fit between expected and observed
blood group frequencies is much closer if
one postulates the existence of gene 0 in
bonnet macaques.' I n that case, the estimated gene frequencies using formulae of
Wiener and Moor-Jankowski ('69) become
0 = 0.173, A = 0.480, B = 0.347 and test
of goodness of fit gives x z c l , = 1.47 so that
P > 0.20.
By using the method of maximum likelihood, one of the referees who kindly reviewed this article obtained the following
estimates of the gene frequencies: 0 =
0.1067, A = 0.5075 and B = 0.3859; and
the chi-square resulting is 1.29 which is
not much less than the value of 1.47 resulting when the gene frequencies are estimated by the use of our own formulae.
Tests for simian-type blood agglutinogens were carried out with blood typing
sera prepared in rhesus monkeys and
crab-eating macaques (Wiener et al., '73).
Positive reactions were obtained with a
number of these reagents indicating the
1 The calculations presented here have the limitation that the population studied i s not a panmictic
one.
685
MRA-379
390
399
430
442
481
482
588
596
645
657
Rh-2
Rh-3
Rh-6
Negative control
( M . mulatta)
Rhesus monkeys
11.
12.
9.
10.
7.
8.
6.
1.
2.
3.
4.
5.
( M . radiata)
Bonnet macaques
Ked cells or
-
+++
+++
++
++
-
++
++
++
-
++
++
++
+++
+
++
++
++
++
++
++
++
(Rh-4)
(Rh-3)
(Rh-2)
+++
+++
+++
+++
+++
-+it
-t+ +
+++
+++
+++
+i+
+++
A n ti-Crh
Anti-Frh
Ant i-Brh
++++
-
-
-
-
(Rh-6)
Anti-Drh
Reactions with antiserum
++
-
++
I
I
-
-
-
-
(Rh-212)
Anti-Erh
3-+
-
++
++
+++
+++
+++
+++
+++
+++
+++
+++
++++
++
+++
+++
(Rh-2 16)
Anti-Grh
Reactions ( b y antiglobulin method) of rhesus monkey blood typing sera with red cells of bonnet macaques including serum of
one bonnet macaque (MRA-8) having a natural isoantibody
TABLE 3
5
F
12
E
”
3F
2
E
M
8
5z
2
+d
+++
-t4--t
+++ $
-
::
+++
-
++
+
-
-
MRA-8
ld
0
3:
B
*
5
v,
BLOOD GROUPS OF BONNET MACAQUES (MACACA RADIATA)
presence on red cells of bonnet macaques
of agglutinogens homologous to those present in rhesus monkeys. That the reactions
were indeed type-specific and not due to
non-specific heteroagglutinins, was established by absorption experiments since,
as shown in table 2, the antibodies anti-Brh,
anti-@ and anti-Grh could be absorbed by
positively reacting red cells from either
bonnet macaques or rhesus monkeys. Of interest was the reaction of a serum from
crab-eating macaques (J-l),immunized
with the red cells of a rhesus monkey. This
antiserum cross-reacted, although to a
lower titer, with the red cells of bonnet macaques. As shown in table 2, antiserum J-1
could be fractionated by absorption with
red cells of M . radiata indicating the presence in the serum of antibodies of at
least two specificities, one shared by both
M. mulatta and M . radiata and the other
peculiar exclusively to M . mulatta.
The red cells of the bonnet macaques
were tested with the rhesus blood typing
antisera in order to determine whether the
latter could be used also for demonstrating
individual differences in the blood of bonnet macaques. As shown in table 3, no
polymorphism could be demonstrated since
the rhesus reagents either agglutinated the
red cells of all the bonnet macaques or
none of them.
When the sera and red cells of the bonnet macaques were cross tested no reactions occurred except in four cases, in
which weak agglutination reactions occurred with the sera from some of the animals. In general, the specificities of these
weak agglutinations differed from one another and the reactions were poorly reproducible. The clearest reactions were given
by the serum of the female MRA-8 (cf.
table 3 ) ; though weak, the reactions were
distinct by the antiglobulin method. The
findings were reproducible, though with
difficulty, so that the serum could be used
for reliable typing of bonnet macaques,
provided that the tests were read blind and
done more than once.
In order to determine the presence or
absence in the sera of heteroagglutinins
for the human red cells, a series of unabsorbed sera from bonnet macaques were
tested against human group 0 red cells by
the saline agglutination methods. I n every
case some agglutination occurred, though
489
in some the agglutination was very weak
while in other cases the agglutination was
quite avid, with titers ranging up to eight
units.
DISCUSSION
The present investigation extends to another species of Old World monkeys our observations on human-type and simian-type
blood groups of non-human primates, reviewed in the introduction to this paper.
As in other Old World monkey species, the
red cells of bonnet macaques do not react
with anti-A, anti-B or anti-H reagents;
nevertheless, their human-type A-B-0 blood
groups could be determined by inhibition
tests on the saliva and by tests on the sera
for anti-A and anti-B agglutinins. The distribution of the human-type A-B-0 blood
groups in bonnet macaques is similar to
that observed by us for crab-eating macaques (Wiener et al., '74) but different
from that of rhesus monkeys, all of which
we have found to react as group B.
While many of the blood typing reagents
produced in rhesus monkey cross react with
red cells of bonnet macaques, they proved
to be of no value for blood typing the latter because those isoimmune rhesus sera
which agglutinated bonnet macaque red
cells reacted with red cells of all bonnet
macaques tested, and were therefore useless for demonstrating polymorphism.
These results show that when testing
across specific lines, there is no essential
difference between agglutinogens responsible for species-specific differences and
those which give rise to type-specific diff erences. * For example, hum an-type blood
group B may be considered a species-specific characteristic of rhesus monkey, but
it is a type-specific characteristic in crabeating and bonnet macaques as well as in
man. In contrast, simian-type blood factors, type-specific in rhesus monkeys, are
apparently species-specific characteristics
of bonnet macaque red cells. That typespecific differences ( polymorphisms) exist
among the red cells of bonnet macaques
was demonstrated by naturally occurring
isoagglutinins found in four animals. Of
these MRA-8, whose serum gave the most
distinct reactions, proved to be a female of
2For a thorough discussion and definition of the
concept of immunological species specificity as introduced first by Uhlenhuth ('01). the readers are referred to the paper of Moor-Jankowski et al. ('73a).
490
SOCHA, MOOR-JANKOWSKI, WIENER, RISSER AND PLONSKI
breeding age. It is significant that she had
had seven pregnancies, in three of which
the infants died within a few months of
birth. This supports the idea that the antibodies resulted from feto-maternal isoimmunization, as observed in marmosets
(Gengozian et al., ’66) and in baboons
(Volkova et al., ’66), and more recently in
rhesus monkeys (Sullivan et al., ’72). For
a detailed review and discussion of materno-fetal isoimmunization in primate animals the readers are referred to our recent
paper on the subject (Wiener et al., ’75).
In our studies we have not used the
rhesus monkey antisera described on the
one hand by Edwards and on the other
hand by Duggleby and Stone (Stone, ’73;
Edwards, ’73). Both groups used antisera
diluted to one-unit titer while our work is
directed by the standards required for
human blood grouping. Edwards’ reagents
were not available to us, while those of
Duggleby and Stone were received in only
small aliquots. Most of them gave nonreproducible results in our hands and the
others detected the same specificities as
our earlier described standard reagents.
ACKNOWLEDGMENTS
This study was supported by U. S. Public
Health Service N.I.H. Grant GM-12074,
Contract RR-4 12184.
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