close

Вход

Забыли?

вход по аккаунту

?

Carbonic anhydrase heterozygosity and FST distributions in Kenyan baboon troops.

код для вставкиСкачать
Carbonic Anhydrase Heterozygosity and FSTDistributions
in Kenyan Baboon Troops
CAROLE OBER,' THOMAS J OLIVIER ' AND JOHN BUETTNER-JANUSCH
' Department ofAnthropology, Northwestern Uniuersrty, Euanston, Illinois 60201 and
'Department ofAnthropology, New York University, New York, N e u York 10003
K E Y WORDS Carbonic anhydrase
Microevolution Migration Pupio
-
. Heterozygous
advantage
.
ABSTRACT
An analysis of the distribution of carbonic anhydrase alleles in
troops of olive baboons, Pupio cynocephalus, is reported. In an earlier study
(Olivier, T. J., J. Buettner-Janusch and V. Buettner-Janusch, 1974, Am. J. Phys.
Anthrop., 41: 175-1901 the authors found a significant excess of heterozygotes
with a large amount of intertroop differentiation a t the CA ZZ locus. If balancing
selection is acting on the CA ZZ locus and maintaining a n excess of heterozygotes,
then the degree of local differentiation observed a t this locus is unexpected.
In this study the analyses of the CA Z and CA IZ data are extended and some
idiosyncratic features of baboon population structure are considered. Nonidealized forms of behavior, such as adult male migration and other age-specific
and sex-specific behaviors, may affect observed patterns of gene frequency distributions. The analysis reveals that the excess of heterozygotes a t the CA II
locus is localized in the females only and that the males are highly differentiated
among the troops. These findings suggest that a female-limited heterozygous
advantage exists a t the CA ZZ locus in this baboon population. A computer simulation model, RAMBLE, further suggests that recurrent male migration
between troops may explain the intertroop microdifferentiation found in primate
populations.
In an earlier study, we reported substantial
microspatial variations in gene frequencies of
neighboring troops of baboons (Olivier et al.,
'74). We described the distributions of carbonic anhydrase I and carbonic anhydrase I1
alleles in troops of olive baboons, Pupio
cynocephulus, from the Laikipia District of
Kenya (table 11. The troops studied were
grouped in two clusters in a relatively small
geographic area.
In our previous analyses, the entire sample
appeared to be in Hardy-Weinberg equilibrium a t the CA Z locus both before and after applying Wahlunds correction for subdivided
populations. Homogeneity tests of the CA Z
frequencies indicated the presence of statistically significant heterogeneities. We suggested t h a t migration and drift, acting approximately in accordance with Wright's island model (Wright, '31, '43,'651, were the
major forces affecting the distribution of
alleles at the CA Z locus.
AM. J. PHYS. ANTHROP. (1978)48: 95-100
The frequencies of the alleles at the CA ZZ
locus, however, were not as easily analyzed by
stochastic models. When Wahlund's version of
the Hardy-Weinberg model was applied to the
CA I I data, a significant excess of CA I1 heterozygotes was found. Considered alone, the
observed excess of heterozygotes could be
taken as evidence supporting a balanced polymorphism model for the CA ZZ locus. However,
if selection favoring heterozygotes is maintaining the polymorphism in this area of relatively small size, the gene frequencies should
be stable throughout the area, a t or near a n
equilibrium point (Cavalli-Sforza and Bodmer, '71). The equilibrium point will be determined by the fitnesses of the two homozygous
classes relative to that of the favored heterozygote.
Although we expected the gene frequencies
to be stable throughout the area, we found significant intertroop differentiation for the CA
95
96
C. OBER, T. J. OLIVIER AND J . BUETTNER-JANUSCH
TABLE 1
Frequencies of the common alleles at the CA I
and CA I1 loci
Frequency
Troop
CA la
CA
IP
A
B
C
D
E
F
G
H
I
J
0.76
0.91 '
0.91
0.82
0.93
0.77
0.85
0.94
0.87
0.88
0.78
0.97 '
0.90
0.82
0.88
0.72
0.48
0.57
0.77
0.79
p:- XniPi
0.86
0.79
0.0355
0.0995
In,
FsT=V/$-$
Homogeneity
X 2 (9d.f.)
32.96
P
< 0.001
Hardy Weinberg with Wahlund's correction
0.04
X2
P
> 0.95
' Frequencies
<
<
97.75
0.001
11.64
0.001
differ slightly from 1974 analysis. see text for
details.
ZZ frequencies. The level of gene frequency differentiation a t the CA 11 locus is considerably
greater than t h a t observed a t the CA I locus
(table 1). Such large genetic microdifferentiation is difficult to reconcile with the proposition that there is balancing selection acting
on the CA ZI locus; that is, how could the CA I1
polymorphism, one perhaps subject to heterozygous advantage or stabilizing selection,
show such large microspatial variations in
gene frequencies? Earlier (Olivier e t al., '74)
we discussed various conflicting propositions
to explain what we found, but we left the questions unresolved.
We have become increasingly aware of the
degrees to which primate social structures differ from the simple, idealized structures assumed in many population genetic models.
In these models (Wright, '31, '43; Crow and
Kimura, '70; Cavalli-Sforza and Bodmer, '71;
Li, '76; Kimura and Weiss, '64) breeding
population sizes are assumed to remain constant over time, and migration usually occurs
in a regular, idealized fashion. Migrants are
generally considered to represent a random
sample of each local population. However, in
many primate populations kinship-related
patterns of behavior, periodic troop fissioning,
and high levels of adult male-only migration
occur regularly and probably influence the ob-
served gene frequencies. Primate social behavior, potentially influential, is disregarded
in most population genetic models and may be
a major determinant of the patterns of gene
frequency differentiation observed in some
human and nonhuman primate groups. Therefore, we have extended the analysis of data on
baboon carbonic anhydrase in an attempt to
account for the age-specific and sex-specific
behaviors t h a t may influence the distribution
of alleles within baboon populations.
We present the results of a further analysis
of the carbonic anhydrase data emphasizing
the distributions of levels of heterozygosity
and gene frequency differentiation within the
adults of ten troops of olive baboons. In addition, we discuss a computer simulation
program, RAMBLE, that may be used to explain the observed distribution of gene frequency differentiation in this population.
MATERIALS AND METHODS
Population
Genetic data for the CA Iand CA 11 loci for
the adult males and adult females in ten
troops of baboons were analyzed. The criteria
used to assign ages to individual animals and
male and female gene frequencies for each
troop are reported in Olivier e t al. ('74).
We encountered difficulties in assessing the
troop membership of some animals while trapping troops B, E, and F. Several days after
Troop B was trapped, a group of animals was
trapped and bled a t another location. Many of
these animals showed signs of having been
bled previously and it was assumed that this
group may have been part of Troop B. Most of
the newly captured members of this group
were bled and designated a s Troop BQ
(Olivier, '72). In this paper, as in Olivier's ('72)
study, data from Troop BQ were eliminated
from the analysis because of the uncertainty
of their status. However, in Olivier et al. ('74)
BQ was considered a part of Troop B. Therefore, in this paper the gene frequencies for
Troop B are slightly different from those reported in Olivier et al. ('74).
Troops E and F, two distinct groups of
baboons with overlapping home ranges, were
trapped a t one site. Olivier ('72) treated these
as separate troops. In a later paper (Olivier et
al., '74) these groups were pooled and considered as a single troop (E, F) for the purpose
of analysis. Because we are interested in finer
levels of genetic structure within baboon
troops, we have separated the samples from
97
HETEROZYGOSITY AND FST DISTRIBUTIONS
groups E and F and treated them as separate
troops, as was done by Olivier ('72) and Steinberg et al. ('77).
Analysis
Heterozygosity levels (No. heterozygoted
N) for the C A IZ locus were calculated for each
age/sex class to determine whether the overall
excess of heterozygotes a t this locus was distributed evenly over all demographic groups.
To test for an excess of heterozygotes against
gene frequency-corrected expectations, proportions of genotypes expected in the adult
male and adult female segments of the population were calculated for each troop using agespecific and sex-specific gene frequencies. We
used a binomial probability function as in the
Hardy-Weinberg model and assumed that the
alleles within each age/sex class are combining randomly. Wahlund's correction for subdivision was applied to yield expected proportions of genotypes for the adult males and for
the adult females in the population.
To measure the degree to which the troops
were differentiated, Wright's FST statistic
(Wright, '65) was used as a standardized
measure of gene frequency differentiation.
These values are computed by the following
equation:
FST =
V
p(1- p)
- 7,
where V is the weighted variance of the frequency of one allele in a set of subpopulations
and
is the mean frequency of one allele
among the troops. The utility of this equation
in calculating standardized variances of gene
frequencies within subdivided populations
was first suggested by Wright 1'65); since
then i t has been used frequently as a measure
of genetic differentiation (Workman and Niswander, '70; Nee1 and Ward, '70; Lewontin
and Krakauer, '73). To determine whether all
agehex classes were equally differentiated,
we calculated FsT values for the total sample
and for the adult male and female components
of each troop.
A computer program, RAMBLE, was developed by one of us (T. J. 0.)
t o test whether
fluctuations in the composition of one portion
of each troop (such as the adult males) could
substantially affect FsT values for that portion of the population. In RAMBLE, 161 individuals with genotype counts identical to
those we observed in the adult males at the CA
I locus were assigned to ten model troops. FST
values were recalculated after each set of ex-
changes that might be conveniently taken as
occurring during one generation. For baboons,
this would be approximately five to seven
years (Olivier e t al., '74). In RAMBLE, unweighted means and variances of gene frequencies are used in calculating FST values because we are interested in demonstrating the
amount of fluctuation between consecutive
generations which is due to male migration
and subsequent changes in troop size.
Weighted variances should have no effect on
the overall degree of these fluctuations. The
aim of this part of our analysis was to examine
in isolation those fluctuations in FSTvalues
for adult males that could occur simply as a result of recurrent male migration. In a future
study we will examine the effects of various
demographic parameters, such as the number
of troops, migration rates, and population size
on the distribution of FsT values over time.
RESULTS
Heterozygosity
The observed proportions of females that
are heterozygotes exceed the proportion of
males that are heterozygotes in both the adult
and nonadult classes in nine out or ten troops.
The proportions of heterozygotes in the adult
males and females are shown in table 2. In
part, the higher heterozygosity in the females
is attributable to the higher frequency of the
rarer CA I1 allele in the females of each troop.
An excess of heterozygotes is present among
the adult females and no such excess is present in the adult males (table 3). The excess
heterozygosity found in our earlier analysis of
the CA IZ locus appears to be restricted to the
females in this population.
Gene frequency differentiation
FST values calculated for the CA I locus are
fairly homogeneous. They are 0.0355, 0.0484,
and 0.0362 for the total troops, the adult
females, and the adult males, respectively. At
the CA II locus the total troop FsT is equal to
0.0995; this value is greater than any FST obtained for the CA I locus. However, the value
for the adult females a t the CA 11 locus is
0.0829 while the adult males show an extremely high index of gene frequency differentiation, with FSTequal to 0.1942. It appears
that the gene frequency differentiation found
between troops a t the CA ZI locus is primarily
a function of the extremely high differentiation found between the adult males of the
different troops.
98
C. OBER. T. J. OLIVIER AND J. BUE'ITNER-JANUSCH
-
I
25
0
TIME
i
1
50
75
GENERATIONS
Fig. 1 Fluctuations in FSTvalues observed with the exchange of 100 migrants per generation as determined
by RAMBLE (see text for details). The horizontal lines represent observed FST values for the adult males.
TABLE 2
Adult male and adult female heterozygotes at the CA I I locus
Adult 1.3
Adult dd
Troop
Hetero
zygotes
(N)
A
6
B
0
C
D
0
1
1
4
7
7
5
2
33
E
F
G
H
I
J
Total
' Totals dlffer slightly
Total
(Nl
i%)
20
28
13
10
22
15
10
16
16
0.30
0.00
0.00
0.10
0.05
0.27
0.70
0.44
0.31
0.25
0.21
8
158
Total
(N)
Proportion
iX)
16
3
6
11
2
7
4
17
14
13
93 I
39
29
15
18
9
17
9
22
25
21
204 I
0.41
0.10
0.40
0.61
0.22
0.41
0.44
0.77
0.56
0.62
0.46
from 1974 analysis. see text for details.
TABLE 3
RAMBLE
Genotype counts for adult male and adult females
at the CA I I locus
Two runs of 100 generations each were conducted. In the first, 40 migrants were exchanged within the set of 10 troops per generation; in the second, 100 migrants were exchanged. In both runs, large fluctuations in
FSTvalues were observed. The mean FSTwith
40 migrants per generation was 0.0489, with a
range of 0.1134 to 0.0138 and a variance of
0.000749. Figure 1illustrates the fluctuations
observed with the exchange of 100 migrants
per unit time in the population of 161 adult
males. The mean Fsr here is 0.0537, with a
IE
Genotype
CA IIa/CA IIa
CA IIa/CA XIb
CA Ilb/CA IIb
P
I
Proporiion
Hetero
zygotes
(N)
Exp
Obs
Exp
Obs
Exp
Obs
ild
(Nl
(Nl
114.20
103
70.59
93
19.21
8
119.05
120
32.90
33
5.05
5
< 0.001
> 0.99
'Totals differ slightly from 1974 analysis, Bee text for details.
HETEROZYGOSITY AND FST DISTRIBUTIONS
range of 0.0099 to 0.0208, and a variance of
0.00121. This range fully encompasses the
range of variation found for the adult male
baboons between the CA 1 and CA II loci.
DISCUSSION
The localization of the excess heterozygotes
in the females and the extremely high index of
gene frequency differentiation in the adult
males lead us to suggest that a sex-limited
heterozygous advantage exists a t the CA Zl
locus among female baboons and that the
dynamics of the polymorphism among males
are radically different.
Although the hypothesis of sex-linked selection seems reasonable within a statistical
framework, a physiological model is more difficult to construct. If heterozygosity a t a particular locus confers a selective advantage to
females during gestation, but is selectively
neutral all other times, female-limited heterozygous advantage may result. The exact role
of carbonic anhydrase during pregnancy is
largely unknown, however, it has been suggested that in mammals maternal carbonic
anhydrase plays an important role during reproduction (Friedley and Rosen, '75), possibly
because fetal red cells have been found to have
little or no carbonic anhydrase activity (Meldrum and Roughton, '33; Berfenstam, '52,
cited in Kirschbaum and DeHaven, '68). Until
more is known about the physiology of maternal carbonic anhydrase activity, a mechanistic model for sex-limited balancing selection
a t the CA ZZ locus in our baboon sample can
only be speculative.
In the adult male portion of the population
construction of a specific model for the CA ZZ
polymorphism is even more difficult. While it
may be possible that variations in local selection pressures favoring one allele over the
other could account for the observed differentiation, the geographical area in which the
troops were trapped is so small that this explanation seems unreasonable. Alternatively, we
can argue that random drift, a s in Wright's
island model (Wright, '31, '43,'651, is responsible for our observations. However, with such a
model an extraordinary degree of isolation between troops would be required to produce the
differentiation we have found between adult
males a t the CA ZZ locus. Such isolation is difficult to reconcile with our findings at the CA
Z locus in the same groups and with recent behavioral reports on migration between baboon
troops (Rowell, '69; Packer, '75). Indeed, we
99
expected initially that the adult males would
be that least differentiated segment of the
population due to such relatively high intertroop mobility.
Behavioral observations of troops of cercopithecoid monkeys have indicated a wide
range in the numbers of males that migrate
between neighboring troops. While several
earlier studies described negligible migration
rates between baboon troops (DeVore, '65;
DeVore and Hall, '651, more recent studies reported high frequencies of intertroop male migration. During eight years of observations of
olive baboons, Packer ('75) recorded the exchange of adult males among seven troops. Of
the 39 recognizable males who reached pubert y during his study, each migrated out of its
natal troop. Approximately 252: of these were
reported to have transferred troops more than
once during the study. Rowell ('69) reported
intertroop movement for 23 out of 25 known
adult male olive baboons during five years of
observations. The length of association of any
one male with a particular troop varied from a
few days to several years. Lindburg ('68) reported that one-third of the original adult
male rhesus monkeys in India changed groups
during 20 months of Observations. Koford ('66)
described similar migration patterns for the
Cay0 Santiago rhesus monkeys where relatively large indices of gene frequency differentiation have been reported (Duggleby, '77, '78)
despite these large migration rates. Similar
findings have been reported for some South
American Indians where high levels of genetic
microdifferentiation between neighboring villages have been observed (Arends e t al., '67;
Chagnon, '74; Ward and Neel, '70).
If, in fact, adult male baboons are a n unstable adjunct to a more permanent core, then
Fs, values would fluctuate somewhat over
time simply as a result of the random redistribution of these males. Behavioral observations (Rowell, '69; Packer, '75) suggest
t h a t during one generation nearly 100%of the
adult male baboons change their troop affiliation a t least once. Under these conditions,
fluctuations in FSTvalues between consecutive generations in the adult males may be
similar to those observed in the computer
simulations program, RAMBLE. Therefore,
large amounts of microdifferentiation could
exist in the face of very high migration rates,
as in the Cay0 Santiago macaque colony (Duggleby, '77, '78b) and in some South American
Indian populations (Arends et al., '67; Chag-
100
C. OBER, T. J. OLIVIER AND J. BUE'ITNER-JANUSCH
non, '74; Ward and Neel, '70). The difference
in FSTvalues between the CA I and CA ZI loci
in the adult male baboons may be a result of
randomly fluctuating FsTvalues due to high
levels of male mobility.
The results of our analysis suggest that
processes controlling distributions of alleles
a t a single locus may vary among the different
demographic components of a baboon troop
and that the dynamics of a polymorphism
within a troop may not be described by a single
model. We suggest that gene frequency differentiation can exist in the face of high levels of
interpopulation mobility and, in fact, random
processes a t times may produce highly divergent FsT values for different independently
segregating alleles in a set of small populations. In general, we feel that baboons and
other primates have a complex internal genetic structure and this structure must be
accounted for if microevolution in these species is to be understood.
ACKNOWLEDGMENTS
The authors thank Mrs. Wren Olivier for
her extensive assistance in the collection of
the baboon blood samples on which this study
is based. We also thank Mr. Paul Zawa for assistance with calculations. This research was
supported in part by NSF Grant SOC 7517426.
LITERATURE CITED
Arends, T., G Brewer, N. Chagnon, M. L. Gallango, H.
Gershowitz, M. Layrisse, J. Neel, D. Shreffler, R. Tashian
and L. Weitkamp 1967 Intratribal genetic differentiation among the Yanomama Indians of Southern Venezuela. Proc. Nat. Acad. Sci. (U.S.A.1, 57: 1252-1259.
Cavalli-Sforza, L. L., and W. F. Bodmer 1971 The Genetics
of Human Populations. W. H. Freeman and Co., San
Francisco.
Chagnon, N. 1974 Tribal social organization and genetic
microdifferentiation. The Structure of Human Populations. G. A. Harrison and A. J. Boyce, eds. Clarendon
Press, Oxford, pp. 252-282.
Crow, J. F., and M. Kimura 1970 An Introduction to
Population Genetics Theory. Harper and Row, New York.
DeVore, I. 1965 Changes in the populations structure of
Nairobi Park baboons, 1959-1963. In: The Baboon in Medical Research. H. Vagtborg, ed. University of Texas Press,
Austin, Vol. I, pp. 17-28.
DeVore, I., and K. R. L. Hall 1965 Baboon ecology. In:
Primate Behavior. I. DeVore, ed. Holt, Rinehart and
Winston, New York, pp. 20-52.
Duggleby, C. 1976 Blood group antigens and the population genetics of Mucuea mulatta on Cay0 Santiago. 11. Ef-
fects of social group division. Yearbook of Physical Anthrop., Vol. 20.
1978 Blood group antigens and the population
genetics of Macaca mulatta on Cay0 Santiago. I. Genetic
differentiation of social groups. Am. J. Phys. Anthrop.,
48: 35-46.
Friedley, N. J., and N. S. Rosen 1975 Carbonic anhydrase
activity in the mammalian ovary, fallopian tube and
uterus: histochemical and biochemical. Biol. Reprod.,
12: 293.
Kimura, M., and K. Weiss 1964 The stepping stone model of
population structure and the decrease of genetic correlation with distance. Genetics, 49: 561-576.
Kirschbaum, T. H., and J. C. DeHaven 1968 Maternal and
fetal blood constituents. In: Biology of Gestation, N. S.
Assalie, ed. Academic Press, New York, Val. 11, pp.
143-179.
Koford, C. B. 1966 Population changes in rhesus monkeys: Cay0 Santiago 1960-1964. Tulane Studies in Zool.,
13: 1-7.
Lewontin, R., and J. Krakauer 1973 Distribution of gene
frequencies as a test of the theory of the selective neutrality of a polymorphism. Genetics, 71: 1-7.
Lewontin, R., and J. Krakauer 1973 Distribution of gene
frequencies as a test of the theory of the selective neutrality of a polymorphism. Genenetics, 71: 175-195.
Li, C. C. 1976 First Course in Population Genetics. Boxwood Press, Pacific Grove, California.
Lindburg, D. G. 1969 Rhesus monkeys: mating season
mobility of adult males. Science, 166: 1176-1178.
Neel, J., and R. Ward 1970 Village and tribal genetic distance among American Indians and the possible implications for human evolution. Proc. Nat. Acad. Sci., 65:
323- 3 30.
Olivier, T. J. 1972 Microevolution in Kenyan Baboons.
Unpublished Ph.D. Dissertation. Duke University, Durham, North Carolina.
Olivier, T. J., J. Buettner-Janusch and V. BuettnerJanusch 1974 Carbonic anhydrase isoenzymes in nine
troops of Kenyan baboons, Pupio cynocephalus (Linnaeus
1766). Am. J. Phys. Anthrop., 41: 175-190.
Packer, C. 1975 Male transfer in olive baboons. Nature,
255: 219-220.
Rowell, T. 1969 Long term changes in a population of
Ugandan baboons. Folia Primat., 11: 241-254.
Steinberg, A. G., T. J. Olivier and J. Buettner-Janusch 1977
Gm and Inv studies on baboons, Pupio cynocephulus:
analysis of serum samples from Kenya, Ethiopia and
South Africa. Am. J. Phys. Anthrop., 47: 21-30.
Ward, R., and J. Nee1 1970 Gene frequencies and
microdifferentiation among the Makitare Indians. IV. A
comparison of a genetic network with ethnohistory and
migration matrices; a new index of genetic isolation. Am.
J. Hum. Gen., 22: 538-561.
Workman, P. L., and J. D. Niswander 1970 Population
studies on southwest Indian tribes. 11. Local genetic differentiation in the Papago. Am. J. Hum. Genet., 22:
24-29.
Wright, S. 1931 Evolution in mendelian populations. Genetics, 16: 97-159.
1943 Isolation by distance. Genetics, 28: 114138.
1965 The interpretation of population structure
by F-statistic with special regard to systems of mating.
Evolution, 19: 395-420.
Документ
Категория
Без категории
Просмотров
2
Размер файла
496 Кб
Теги
distributions, baboons, carbonic, kenya, heterozygosity, anhydrase, fst, troops
1/--страниц
Пожаловаться на содержимое документа