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Distribution of transferrin phenotypes in selected troops of Kenya baboons.

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Distribution of Transferrin Phenotypes in
Selected Troops of Kenya Baboons
JOHN BUETTNER-JANUSCH AND THOMAS J. OLIVIER
Departments o f Anatomy, Zoology, and Sociology-Anthropology,
Duke University, Durham, North Carolina 27706
ABSTRACT
The distribution of transfenin alleles in a group of common baboons,
Papio cynocephalus of East Africa, was determined after starch gel electrophoresis of
plasma and autoradiography of electrophoretograms. Three alleles, T f A ,T f B ,and T f C ,
were found, i n agreement with results previously reported. The frequencies of these
alleles are T f " = 0.276, T f B = 0.515, T f C= 0.209. The difference between the frequencies reported here and those reported by Buettner-Janusch (1963 Folia Primat., 1: 738 7 ) for the same species ( T f A= 0.205, T f " = 0.332, T f C:
1 8.463) is significant. Transferrin of P. cynocephalus contains four residues of sialic acid per molecule of
transferrin, as determined by electrophoresis and autoradiography o€ plasma treated
with neuraminidase.
Although there is a wealth of information available on genetic variation in Homo
sapiens, there are a limited number of genetic studies of socially or geographically
separated populations of nonhuman primates. We know little about the distribution and range of genetic variation in
natural populations of nonhuman primates
and even less about the influences of behavior on genetic variation. Despite the
paucity of data, we constantly make assumptions about kinds and degrees of genetic variation in the order Primates in
our attempts to elucidate evolutionary
processes.
The available data on genetic traits of
Anthropoidea come largely from studies of
serum proteins, hemoglobins, and other
erythrocytic proteins. We report here the
distribution of transferrin phenotypes for
selected groups of baboons, Papio cynocephalus. We compare these results with
those reported in an earlier study that provided evidence for effective genetic isolation between baboon troops (BuettnerJanusch, '63, '65). Serum transferrins of
nonhuman primates are excellent proteins
for genetic studies. The transferrin phenotypes can be determined easily from small
amounts of material. Surveys of transferrin
phenotypes among the nonhuman primates
indicate that many species of primates
are polymorphic at the transferrin locus
(Goodman et al., '65, '67; Barnicot et al.,
'67; Nute, '68). In those species for which
AM. J. PHYS.ANTHROP.,33: 303-306.
the inheritance of transferrin alleles has
been studied, the alleles are inherited in a
simple, nondominant, autosomal manner
(Goodman and Riopelle, '63; Nute and
Buettner-Janusch, '69; Nute et al., '69).
MATERIALS AND METHODS
Blood samples were obtained in Kenya
in 1962 from 67 Papio cynocephalus, common baboons of East Africa. These 67 animals were captured in four well-defined
trapping areas. The method of trapping has
been described (Maxim and Buettner-Janusch, '63). We assume that the animals
obtained in a single trapping area are members of a single troop (Maxim and Buettner-Janusch, '63; Buettner-Janusch, '65).
These animals and the animals used in the
previous study came from the large population of baboons in the Kibwezi-Darajani
area of southeast Kenya (Buettner-Janusch, '63).
Plasma and red cells were separated in
the usual manner. Plasmas were frozen,
packed in dry ice, and shipped by air to
the United States where they were stored
at -20°C. Starch-gel electrophoresis and
autoradiography of plasma labelled with
radioactive iron were carried out essentially as described previously (Nute and
Buettner-Janusch, '68, '69). Transferrin
bands were identified on the autoradiographs. The bands are named alphabetically in order of increasing mobility toward
the anode. This is a different system from
303
304
JOHN BUETTNER-JANUSCH AND THOMAS J. OLIVIER
that used earlier (Buettner-Janusch, '63).
The three bands reported in 1963 as bands
1, 2, and 3 are bands B, C, and A, respectively, in the present system. Selected
plasma samples were treated with neuraminidase (Coppenhaver and Buettner-Janusch, '70) in order to determine the number of sialic acid residues in baboon
transferrin and to establish that multiple
bands of heterozygotes do not result from
variation in number of sialic acid residues
present on a single transferrin (Chen and
Sutton, '67; Nute et al., '69).
Blood samples used as controls were obtained from the inbred colony of baboons
at the Southwest Foundation for Research
and Education, San Antonio, Texas. The
animals in this colony are descendants of
animals from the Kibwezi-Darajani area
and are homozygous for transferrin B
(Buettner-Janusch, '63).
RESULTS AND DISCUSSION
Three different transferrin bands were
found on autoradiographs made after electrophoresis of labelled plasmas on starch
gels (fig. 1). These three bands have been
designated A, B, and C. Band B has the
same mobility as band B found in plasmas
used as controls. We cannot distinguish
the three major bands from the three reported in the earlier study (Buettner-Janusch, '63). Barnicot and his colleagues
reported a similar transferrin polyrnorphism in East African baboons (Barnicot
et al., '65; Kitchin et al., '67). In addition
to the three major bands seen on auto-
I
Origin
-
AA
BB
CC
AB
AC
BC Human
Fig. 1 Relative electrophoretic mobilities of
transferrin phenotypes found in Papio cynocephalus. Human transferrin CC is shown as a reference.
radiographs, faint bands appeared in some
cases. The faint band moved either faster
or slower than the major band with which
it was associated. The samples in which
these faint bands were evident had been
stored for several years. The control samples had been freshly prepared and these
faint bands were not seen on autoradiographs. We believe that the faint bands are
artifacts that occur after prolonged storage
of plasma.
Treatment of five samples of plasma
with neuraminidase indicated that there
are four sialic acid residues per molecule
of baboon transferrin. After enzymatic digestion, plasma from two heterozygous
animals yielded two transferrin bands;
plasma from three homozygous animals,
including one from the control group,
yielded a single transferrin band. The sialic
acid content of transferrin of Papio cynocephalus is the same as that of P. geladn
and P . hamadryas (Coppenhaver and Buettner-Janusch, ' 7 0 ) .
We assume that the transferrins of
Papio cynocephalus are inherited as nondominant autosomal alleles. Thus, one
band seen on an autoradiograph designates one allele. This distribution of phenotypes in the sample of 67 Papio cynocephalus from four troops is presented in
table 1. The allele frequencies are: T f * =
0.276, Tf" = 0.515, TfC = 0.209. The observed frequencies of genotypes do not fit
the Hardy-Weinberg model; x* = 12.98, P
< 0.01.
In order to compare these data with results of the earlier study on Kibwezi-Darajani baboons, we reproduce in table 2 the
data from the previous study (BuettnerJanusch, '63). The f m t study was based
on a group of animals trapped in 1960;
the present one based on a group of animals trapped in 1962. The differences in
frequencies of alleles in these two sets of
data are significant (table 3 ) . Among the
baboons examined in 1960, there were
many more homozygotes than the HardyWeinberg model predicted; x2 = 264.4, P
< 0.01. Among those sampled in 1962,
there was an excess of heterozygotes. In
each of the troops sampled in 1960, only
two of the three transferrin alleles were
present. In the 1962 sample, all three al.
leles were present in each troop.
305
TRANSFERRINS OF BABOONS
TABLE I
Distribution of transferrin phenotypes of baboons from various
trapping areas (1962 sample)
Transfemn phenotype
Area
AA
BB
cc
AB
BC
AC
Total
Kitui Bridge
Kibwezi River
Kibwezi Springs-2
North Darajani
1
0
0
0
6
3
4
5
22
2
3
3
1
1
7
1
0
1
5
1
1
0
46
7
8
6
Total
1
16
6
28
9
7
67
0
0
TABLE 2
Distribution o f transferrin phenotypes of baboons f r o m selected troops (1960 sample)
Transferrin phenotype
Troop
AA
BB
cc
AB
BC
AC
Total
8
0
0
20
40
35
47
17
0
0
0
0
E
0
11
10
9
2
0
5
11
2
0
0
0
0
0
10
5
0
0
45
68
32
34
53
Total
32
68
99
16
2
15
232
A
B
C
D
1 Data
from Buettner-Janusch ('63).
TABLE 3
Frequencies of trunsferrin alleles i n t w o samples o f baboon populations
Allele
TfA
TP
Tf C
Number Frequency
Number Frequency
Number Frequency
Sample
1960
1962
95
37
0.205
0.276
x2 = 28.30
1 Calculated
154
69
0.332
0.515
D.F. = 2
215
28
0.463
0.209
Total
Number Frequency
464
134
1.000
1.000
P < 0.001
on basis of number of alleles.
There is no obvious explanation for these
data. We suggest that interpretations must
be sought in one or all of the following. It
is possible that the selective pressures were
not identical for the two groups of animals
sampled. This explanation is in keeping
with classical concepts of adaptation and
does not demand the modification of a general theory to fit phenomena occurring in
a particular species.
Alternatively, the observed frequencies
of transferrin alleles may be the result of
sampling error. The trapping procedures
used for obtaining the animals were essentially unchanged from 1960 to 1962. These
trapping methods may have led to the
biases seen in the allele frequencies in both
sets of data. It j s also possible that our
trapping areas did not define troops, although we consider this unlikely.
If we assume that the trapping procedure did not bias the sample, then sampling error may be a consequence of the
structure of baboon populations in the
Kibwezi-Darajani area. Many baboon
troops appear to be stable in composition,
relatively small, and with many more adult
females than males. The effective breeding
population may be further limited, for
mating may be restricted to two or three
males and may not be random in a troop
(DeVore and Washburn, '63; DeVore, '65;
Buettner-Janusch, '65; Rowell, '66). Random processes are believed to have their
greatest effect in small closed or semiclosed breeding isolates, and baboon troops
may often be such isolates. The distribution of transferrin alleles suggests that
there is effective genetic isolation between
neighboring troops of baboons (Buettner-
306
JOHN BUETTNER-JANUSCH AND THOMAS J. OLIVIER
Janusch, '65), and it seems plausible that
territoriality of a troop causes effective reproductive isolation. Thus, we can interpret
both the differences between the allele frequencies in the two samples and the deviations from the Hardy-Weinberg model in
each of the samples as results of random
processes such as genetic drift. Although
this interpretation does not completely explain the failure of the alleles at the transferrin locus to assort according to HardyWeinberg predictions, there is evidence
from behavioral studies (DeVore and
Washburn, '63; DeVore, '65; Buettner-Janusch, '65; Rowell, '66) to support in part
this interpretation of the observed results.
It should be pointed out that random
processes and natural selection are not mutually exclusive phenomena (Dobzhansky
and Pavlovsky, '57; Wright, '48). The frequencies of alleles possessing adaptive values may well be influenced by random
processes. The relative importance of these
processes in the genus Papio is unknown
and may be better understood with further studies of the population dynamics
and genetics of this group.
ACKNOWLEDGMENTS
We thank the Southwest Foundation for
Research and Education (SFRE) for supplying much of the material used in this
study. Our special thanks go to Dr. William R. Maples, resident manager of the
SFRE Darajani station in 1962, for obtaining the wild baboons; and to Dr. Robert
Hummer, Director, Animal Resources and
Facilities, SFRE, for his cooperation. The
work reported here was supported in part
by GM 06053 and GM 13222 of the United
States Public Health Service. The work was
carried out during the tenure of a National
Defense Education Act Fellowship (T.J.O.),
a National Science Foundation Senior Postdoctoral Fellowship and a United States
Public Health Service Research Career Development Award (J.B.-J.).
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