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Blood-protein allele frequencies and phylogenetic relationships in Macaca A review.

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American Journal of Primatology 17209.241 (1989)
REVIEW ARTICLE
Blood-Protein Allele Frequencies and Phylogenetic
Relationships in Macaca: A Review
JACK FOODEN' AND SCOTT M. LANYON'
lDivision of Mammals and 2Division of Birds, Field Museum of Natural History, Chicago
Allele-frequency data have been assembled for 35 blood-protein loci in 17
of 19 recognized species of Macaca based on 29 published electrophoretic
studies; studies of inbred captive colonies have been excluded. Data for 22
polymorphic loci are tabulated in detail for 43 geographic populations of
these species. Calculated FsT values provide a measure of intergroup
genetic differentiation at various hierarchical levels-troop, locality,
province, country or island, species, species group; polymorphism indices
measure genetic variation. The greatest intraspecific genetic differentiation occurs a t the level of island populations within species. The pattern of
genetic variation among island populations appears to be relictual, suggesting that the reduced genetic variability of island populations of
macaques is a result of postisolation genetic drift rather than founder
effect. Interspecific relationships were investigated by means of a jackknifed Fitch-Margoliash algorithm, using Papio as outgroup. Phylogenetic
inferences based on blood-protein evidence are largely compatible with
inferences based on morphology and zoogeography. The reduced genetic
variability that frequently characterizes insular macaque populations
complicates phylogenetic interpretation of blood-protein evidence.
Key words: blood proteins, phylogenetics, electrophoresis,
genetic distance
INTRODUCTION
The primary goals of the present paper are 1) to assemble in an accessible form
the scattered published information concerning blood-protein allele frequencies in
Macaca, 2) to analyze the assembled protein data phylogenetically, and 3) t o
compare the resulting hypotheses of relationships with those derived from morphologic and zoogeographic analyses. Blood-protein information is available in 29
published reports that include data on 35 loci for 17 of 19 recognized species of
macaques (Tables I, 11; Appendix A); a total of 233 localized or unlocalized
populations have been sampled in these reports.
Although protein information has been analyzed in nine previous multilocus
studies, some of which employed overlapping data sets [Ishimoto, 1973; Weiss et
Received for publication September 8, 1988; revision accepted November 15, 1988.
Address reprint requests to Jack Fooden, Division of Mammals, Field Museum of Natural History,
Roosevelt Rd. at Lake Shore Dr., Chicago, IL 60605.
0 1989 Alan R. Liss, Inc.
TABLE I. Key to Species Abbreviations and Country or Island
Index Numbers (cf. Fig. l).*
Species grouplspecies
1. silenus-syluanus group"
M . silenus
M . nemestrina
M.
M.
M.
M.
maurus
tonkeana
ochreata
brunnescens"
M . hecki"
M . nigrescensc
M . nigra
M . syluanusd
2. fascicularis group
M. mulatta
M . fascicularis
M . cyclopis
M. fuscata
3. sinica group
M. sinica
M . radiata
M. assamensis
M . thibetanag
4. arctoides group
M . arctoides
Species
abbreviation
SIL
NEM
MAU
TON
OCH
BRU
HEC
NGS
NGA
-
MUL
FAS
CYC
FUS
SIN
RAD
ASS
ARC
Country
India:Keralab
India:Karnatakab
Thailand
Malaysia, W (2)
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
[NW Africa]
Pakistan,N (6)
India, N'
Bangladesh
China
Thailand,N
Vietnam,N or Cent.
Thailand,Cent. or S
Kampuchea
Vietnam,S
Malaysia,W (3)
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Philippines
China
Japan
Japan
Japan
Japan
Japan
Japan
Sri Lanka
India,S
India,NE
China$ central
India,NE
Thailand
Ma1avsia.W
*
,
Island
Index
No.
Sumatra
Mentawei Ids.
Sulawesi,SW (3)
Sulawesi,Cent.
Sulawesi,SE
Muna & Butung
Sulawesi,N
Sulawesi,NE
Sulawesi.NE
1
2
3
4
5
6
7
8
9
10
11
12
13
-
Sumatra (7)
Java (7)
Bali (8)
Lombok (4)
Sumbawa (7)
Timor
Mindanaof
Taiwan
Yaku
Kyushu (7)
Shikoku (3)
Awaji (2)
Shodo (2)
Honshu (19)
Sri Lanka (12)
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
-
41
42
43
*Parenthetical notation following name of country or island indicates No. o f subpopulations known to have been
sampled, where greater than one.
V f . Delson [19801, who allocates M . ayluanus to a separate monotypic species group.
bThese two large Indian states are treated here as geographically equivalent to countries.
'Cf. Groves [1980], who regards M. brunnescens, M . hecki, and M . nigrescens as subspecies, respectively, of M .
ochreata, M . tonkeana, and M . nigra.
dData on 48 specimens of this species reported by Schmitt et al. [19811 are not directly comparable with those
of other authors.
ePart of the Indian M . mulatta sample originated near the Nepal border [Darga, 19751; the geographic origin of
other specimens in this sample is unknown.
'Part of the Philippines M . fascicularis sample is known to have originated in Mindanao [Darga, 19751; the
island of origin of other Philippine specimens, here arbitrarily indicated as Mindanao, is unknown.
"Not sampled.
Blood Proteins in Mamca I 211
TABLE 11. Loci Included in Analysis, With Key to Abbreviations*
Abbreviation
ACP
ADA
AK
Alb
Alp
CA-I
CA-IC
CA-I1
CellEs
ChEs
Dia
EsD
G6PD
Gc
HbA
HbB
HP
IDH
LAP
LDHA
LDHB
MDH
PGD
PGM-I
PGM-I1
PHI
PI
TBPA
Tf
TO
Locus
Acid phosphatase, cell
Adenosine deaminase, cell
Adenylate kinase, cell
Albumin, plasma
Alkaline phosphatase, plasma"
Carbonic anhydrase-I, cell
Carbonic anhydrase-I control, cell
Carbonic anhydrase-11, cell
Cell esterase
Cholinesterase, plasma
NADH-dependent diaphorase, cell
Esterase D, cell"
Glucose-6-phosphate dehydrogenase, cell"
Group specific component, plasma
Hemoglobin-alpha, cell
Hemoglobin-beta, cell
Haptoglobin, plasma"
Isocitrate dehydrogenase, cell
Leucine aminopeptidase, plasma"
Lactate dehydrogenase A, cell"
Lactate dehydrogenase B, cell
Malate dehydrogenase, cell"
6-phosphogluconate dehydrogenase, cell
Phosphoglucomutase-I, cell
Phosphoglucomutase-11, cell
Phosphohexose isomerase, cell
Protease inhibitor, plasma
Thyroxine-binding prealbumin, plasma
Transferrin, plasma
Tetrazolium oxidase. cell"
*Excludes five plasma protein loci that are monomorphic in Mucuca and P@o: alpha-macroglobulin, amylase,
catalase, ceruloplasmin, and prealbumin [Kawamoto et al., 1982; Nozawa et al., 19821. Sample sizes vary by
locus and taxon; sample size data are available on request.
"Indicates that locus is essentially fixed in Mucuca and Pupio (frequency of major allele greater than 0.95 in all
species or partitioned countryhland subdivisions of species).
al., 1973; Darga et al., 1975; Nozawa et al., 1977; Shotake, 1979; Cronin et al.,
1980; Lucotte et al., 198413;Melnick and Kidd, 1985; Kawamoto et al., 19851, none
has considered all of the available data; the number of loci encompassed in these
studies varies from 3 to 33, the number of species varies from 3 to 14, and the
number of populations varies from 5 to 20. Furthermore, comparing the results
from these different studies has been complicated because the protein-based
phylogenies presented in these studies have been generated by a variety of
statistical procedures: minimum deviation method; unweighted pair-group
method; additive hypothesis method; maximum parsimony method; weighted pair
group method; phenetic cluster analysis; nearest neighbor algorithm; median
algorithm; Ward's algorithm; least squares analysis; principal components analysis; and Hennigian qualitative analysis. As a result of this analytical and
methodological variation, it was necessary to compile a single dataset encompassing the published allele frequencies for macaques. The dataset compiled for this
study enables us to consider phylogenetic, population genetic, and biogeographic
212 I Fooden and Lanyon
patterns in the present paper and should facilitate future work on interpretation
of macaque blood proteins.
MATERIALS AND METHODS
Data
Data for this analysis are derived from 29 electrophoretic studies of blood
proteins in Macaca and one study of blood proteins in Papio, which is used as an
outgroup. Details of these studies are summarized in Appendix A. These studies
present data on samples of one or more populations of 17 of 19 recognized species
of macaques (Table I). Thirty-five protein loci were investigated in these studies; of
these, 30 are included in the analysis (Table 111, and 5 monomorphic loci are
excluded. Copies of computer files in which our basic data are stored by author,
species, and locality are available upon request.
Authors of the 30 studies are affiliated with 5 laboratories or laboratory
groups. Members of each of these five groups have directly compared their results
with those of some or all of the other groups. These comparisons explicitly
postulate concordance between loci and alleles studied. However, as is true for all
electrophoretic studies, electrophoretic identity may not always be equivalent to
genetic identity [Richardson et al., 19861. Notes on concordance of alleles are
provided in Appendix A.
Results from different laboratory groups are generally similar, with minor
exceptions noted in Appendix A. In an unpublished Ph.D. dissertation, however,
one author [Bruce, 19771working outside of the five laboratory groups cited above,
has reported alleles and allele frequencies that are only partly concordant with
those reported by the five groups; although results reported in this dissertation
have been employed by Cronin et al. [1980; for criticism, see Melnick and Kidd,
19851, these divergent data are excluded from the present analysis. Also excluded
are data derived from transplanted colonies that are known to have been
genetically isolated from their parental stock for several generations; examples are
the Cay0 Santiago population of M . mulattu [Duggleby et al., 19861 and the
Alberta/Arashiyama population of M . fuscuta [Lucotte et al., 1984al.
Statistical Analysis
To examine genetic variation we calculated a simple index of polymorphism for
each of the 43 populations studied (Table I; Fig. 1). This index is calculated as the
number of alleles observed in a given population divided by the number of alleles
observed across all taxa for those same loci. Because of variation in sample sizes,
only those alleles present at frequencies of 0.07 or greater were considered to have
been observed; this value represents the smallest theoretically observable frequency in the population for which the fewest individuals were surveyed (Population No. 6, n = 7).
Rogers’s modified genetic distances (0)
[Wright, 19781 were calculated from
the Mucaca allele frequencies summarized in Tables I11 and IV. This measure
satisfies the triangle inequality, an important prerequisite for the generation of
trees as discussed by Farris [19811. Unrooted Fitch-Margoliash networks [Fitch
and Margoliash, 19671 were produced from the matrix of Rogers’s D values using
Felsenstein’s PHYLIP program [1985] and were rooted by designating Papio as the
outgroup. The Fitch-Margoliash analysis was selected because, although it assumes that evolution can be characterized as time-dependent divergence, it does
not assume equal rates of change in all lineages and, therefore, is not strictly
dependent upon the existence of a molecular clock. A cladistic analysis was not
Blood Proteins in Macaca I 213
performed because evolution of electrophoretic characters in macaques has proceeded primarily through shifts in allele frequency; because frequency differences
do not contribute to cladistic analyses, much of the phylogenetic information
contained in this dataset would be lost.
As discussed by Lanyon [19851 and Felsenstein [19851, tree-generating algorithms may produce topologies that are only marginally supported by the data.
Some three-taxon statements that appear in the resulting trees may owe their
existence more to the tendency for algorithms to produce dichotomously branching
structures than to any real biological pattern in the data. Consequently, a
jackknife manipulation of taxa was used in this study to identify those nodes in the
Fitch-Margoliash network that were unstable and presumably poorly supported by
the data [Lanyon 19851. In jackknifing, n ( n = number of ingroup taxa) pseudoreplicate datasets are produced, each lacking a different ingroup taxon; a FitchMargoliash network is produced for each pseudoreplicate dataset, and a consensus
of all n trees is calculated.
In many instances, our analyses required combining the information reported
for different troops or localities into some larger geographic or taxonomic unit. To
estimate allele frequencies for these more inclusive units, data from all relevant
individuals were combined and new frequencies calculated (weighted means). This
approach is in contrast to estimating frequencies by averaging the various
observed population frequencies. In the latter approach, all populations would
receive equal weight, regardless of the number of individuals sampled. Consequently, the relatively inaccurate frequency estimates for populations represented
by a few individuals could bias the results.
Most blood proteins are assumed to be selectively neutral based on the
observation that alleles from a single protein-coding locus generally are functionally equivalent [Kimura, 19831. In isolated cases, examples of selection operating
on alleles have been proposed [e.g., Hazout et al., 1984; Koehn & Hilbish, 19871,
but these instances appear t o be the exception, rather than the rule, and are not
consistent across taxa. Consequently, in this paper we assume that electrophoretic
characters are selectively neutral.
RESULTS
Allele-FrequencyVariation
Of 30 loci considered, 8 are essentially fixed, with the frequency of major
alleles greater than 0.95 in all species or partitioned country/island samples of
species (Table 11). Allele-frequency data for the 22 polymorphic loci are presented
in detail in Table I11 (localized samples) and Table IV (unlocalized samples).
One hundred seventy-two alleles have been identified at the 30 loci surveyed.
Ten of these alleles-CellEs:I, EsD:I (not studied in Papio), GGPD:B+, Hp:l,
MDH:l, PGD:A, PGM-19, PGM-II:I, PIC, and T0:I-occur in all macaque
species, but not in Papio. Although some of these ten alleles may be unique t o
Macaca and represent synapomorphies of the genus, five-Hp:l, MDH:I, PGD:A,
PGM-I:l, and PGM-119-are known also t o occur in Cercopithecus [Kawamoto et
al., 19821, and others may occur in other cercopithecine genera. (Unexpectedly, the
allele frequency data of Kawamoto et al. [19821 indicate that blood proteins in
Macaca and Cercopithecus are more similar than blood proteins in Macaca and
Papio.)
Genetic differentiation. Available data permit investigation of the degree of
genetic differentiation at various hierarchical levels from troops within localities
to species groups within Macaca. As illustrated in Figure 2, high degrees of
214 I Fooden and Lanyon
Fig. 1. Location of countries or islands where macaque populations have been sampled; for key to country or
island index numbers, see Table I. Within countries or islands, map symbols are positioned arbitrarily within
known ranges of indicated species.
2
1
4
3
5
L-r-;;g;;;;
Locus
Acp
Papio 1
A
c
2
3
5
4
N
32
0
100
0
0
32
100
2
2
_ - - _
0
3
6
0
0
_ - - _
0
0
=
A
B
c
8 9 10 1 1 12 13 14 15 16 17 18 19
U
N
H
U
C
S
A
99 100 100 100 100 100 100 100 - 98 100 0
0
0
0
0
0 0 0 - 2 0 1
0
0
0
0
0
O O - O O 7 64
50
19 17 35
16 47 219214 0 76 31 0
0
0 0 1 3 0
0
0
0
0
0
0
100 100 100 100 100 100 100 96 97 99 - 92 94 0
3 0 7 30
0
0
0
0
0
0
0 10 04
0
0
0
0
0
0
0
50 19 17 35 16 47 216214 0 76 31 0
7 64
100 100 100 100 100 100 100 99 100 - - - - 0
o----0
0
0
0
0
0
0
0
o----0
0
0
0
0
0
0
1
o - - - - 0
0
0
0
0
0
0
100 100 100 100 100 100 100 100
0
0 0 0 0 0 0
0
0
0
0
0
0
0
0
0
D
N = 502
8 11 50127
1
0 44 9 0 ADA
0 0 100 2
96
3
0 5691 0 0 0 0 4
4
8 I 1 11 0
N = 502
AK
1
98 _ - -
Alb
-
7
MUL
MAU TON OCH BRU HEC NGS NGA
6
7
8
9
10 11 12 13 14 15 16 17 18 19
NEM
SILa
and
allele
6
- - _ 0
0
0
7
64
100 - - 100 - 95 100
5 0
O - - 0 -
38
62
502
o _ -
D
O
D’
0
N = 502
0 3 2
0
0 0
- 0 0
0 0 11 0 32
- -
0 -
0
0
0
7
0
0
0
64
19
17
91 100 100
9
0
0
0
0
0
0
0
0
0
0
0
35
0
0
0
0
50
35
16
50
19
17
16
47 187
54 100 100
0
0
46
0
0
0
0
0
47
0
0
0
0 0
98 40 - 98 95 2 602 50 0 0 00
0 0 00 0 032 214 0 76 31 0
0
Blood Proteins in Macaca I 215
Table I11 (below). Allele Frequencies (%) at Polymorphic Loci in Macaque Species and
Papio; Where Locality Information is Available, Data for Macaque Species Have Been
Partitioned According to Country or Island of Origin.'
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43
FAS
20 21
22
23
24
25
FUS
CYC
26
27
28
29
30
31
32
33
34
35
36
37
SIN RAD ASS
38
39
40 41
ARC
42
43
~
91 96 9 4 0
0
98 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100
2 < l
0
0
0
0
0
0
0
0
0
0
0
0 < 1
0
-
0
0
_
_
_
_
0
0
0
0
0
0
0
0
0
0
0
0
0
0
_ _
- _
- _
-_
- -
0
0
0
100
0
0
0
0
119
-
-
-
-
-
0
0
0
0
0 223
96 89
4
9
0
1
0
1
0
0
109 222
-
100 - 100 0 0 -
o - o -
0
0 244 223 204 136 33 78
7
3
0
0
0
0
0
0
- 95 100 100 100 100 100 100
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0 33 223 204 135 33 78
7
- - 100 100 100 100 100 100
0
0
- 0
0
0
0
149113
-
0
100
0
118 121
29 538 80 87 96 880 131
19
0
0 100 100 100 100 100 100 100
53
100 100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0 < 1
47
0
0
0
0
0
0
0
0
0
0
19
21
67 126 538 80 87 96 880 I31
99 100 87 98 99 96 - - 1 0 1 3
2
1
0
0
0
0
0
0
4 - 0 - - -
0
0
0
0
0
0 - - 0
0
0
0
0
0 0
0
0
204 136 33 78
7
0
0
0 538 80 87 96 880 131
0
100 100 100 100 93 100 99 100 100 100 100 100 100
0
0
0
0
0
0
7
0
1 0 < 1
0
0
0
0 9 8 1 0 0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
0
200 136 33 78
7 79 68 126 538 80 87 96 880 131
19
28
64
0 171
0
- 35
- 0
10
0
0
3 6 - 6 5 9 0
o
-
o
18
0
13
5
-
-
-
-
-
-
-
-
-
o
-
- - - 0 0
0
0
16 - 100 100
8 4 0
0
o - o o
o - o o
o - o o
28
-
13
5
216 I Fooden and Lanyon
Table 111. (continued)
Locus
SIL"
and
allele
CA-I
Papio 1
A
98
A2
0
B
21
C
0
0
D
D2
0
0
D3
D4
0
N = 502
CA-IC X +
-
x-
-
N =
CA-I1 A
A2
-
B
c
G
0
-
2
ChEs
000 0 0 0 0
Dia
HbA'
HbB
5
4
-
0
0
834252100
0 3 0 0
6 0 0 0
0 0 0 0
0 0 0 0
0
0
0
0
8 0
29 0
71100
8 I1
72 I65 105 7
45 43 33 100
55 57 67 0
63 I65 105 7
- 0 0 0 0
- - 322517 0
- - 68 75 83 100
_ - - - -
0
0
1
0 2
0 - 2 ' 1 0 0 - 3
o - 4
0 - N = 502
0
1
4
5
6
3
0 - 11 55 48
0 0 0 0
N=
CellEs
MUL
MAU TON OCH BRU HEC NGS NGA
6
7
8
9
10 11 12 13 14 15 16 17 18 19
NEM
0
0
0
0
0 0 0 0
0 17 12 32 7
- - - 100 100
- 0 0
- 0 0
- 0 0
- 0 0
0 0 0 32 7
0
1 39 35
0
0 28 100 100 100 96 85 70
22 39 41 5 6 1 0 0 43
0 0 0 0 00
0
0
0
0
0
0
0 0 0 0 00
0
0
0
0
0
0 0 0 0 0 3 0
0
0
0
0
0
0 0 0 0 0 0 0
0
0
0
0
0
0 < 1 0 0 41230
77
19 15 44
0 29
0 0 0 0 00
0
3
9
0
0
0
0 0 0 0 0 71
50 19 I 7 35 16 53 219238 26 76 46 0
100 100 100 100 100 100 100 - 100 100 - 100 0
0
0 0 0 00
0
0
0
0 24 26 0 I5 0
71 50 19 17 35 I6 53
0
0
0
0 2 9 - - - 6 0 0
0
0
0
0 12
0
0 - - 05
0
1
95
95 100 100 100 88 100 71 - - - 40 0
0
0 - - 00
0
0
0
0
0
0
0 - - 00
0
0
0
4
66 50 19 17 35 16 53 186 0 0 0 5 0
100 100 100 100 100 100 100 100 100 - 100 100 0
0
0
0 0 0 0 0
0
0
0
0
0
0 0 0 0 0
0
0
0
0
0
0
0
o o o - o o 0
0
0
0
0
0
0 0 0 0 0
0
0
0
64
50 19 17 35 16 47 219214 0 76 31 0
100 - - 100 - 100 100 100
0 0
0
0 - 0 0-'0 - -
0 -
0
0
0
99 100 100 100 100
0
0
0
0
0
0
0
0
0 0 0
0
1
N = 502 0 0 10 0 32 7 64 50 19 17
100 - - 20 96 97 100 100 100 100 100
A
0
0
0 - - 8 0
2 3 0
0
0
C
0
0
0 - 0 0 0 0
0
0
D
0
0
0 - - 0 0 0 0
0
0
G
0
0
0 - - 0 2 0 0
0
0
Otherb
N = 502 0 0 10 25 32 7 64 50 19 17
N =
1
2
6
M'
P
N =
1
2
3
5
6
N =
0 n u o o o o
0 50 73 35 0 < I 0
100 50 27 65 100 100 100
0 0 0 0 0 0 0
0 0 0 0 0 0 0
0 0 0 0 0 0 0
502 n I I 95 160 103 7
0 - - 100 100 100 100
0
0 0 0 0
100 - - 0 0 0 0
0 -- 0 0 0 0
0 - - 0 0 0 0
502 0 0 85 160103
7
_-
0
6
91
1
2
0
71
1
0
98
1
0
71
0
2
90
8
0
0
50
11
0
89
0
0
50
0
0
0
0
97 100 100 - 100 100 0 0 0 0 0
0
0
0
-
0 76
10
81
9
0
-
31 0
29 46 250-
0 00 76 31 0
0
0
35
16
47
0
0
0
0
0
0
97 100 100
3
0
0
0
0
0
0
0
0
19 I 7 35
84 18 29
0
0
0
16 82
9
0
0 62
0
0
0
19 17 35
0
3
94
3
0
0
16
0
0
38
62
0 0 0 0 0 0
0
0 100 100 100 100 100 98
0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 2
0 0 0 0 0 0
53 219240 47 76 58 0
6 100 100 100 - 100 0 0 0 00
0 0 0 031
0 0 0 63
0O O O - O 0
53 219 26 47 0 58 0
32214
-
00-
0
0
16
0
0
0
0 -
0
0
3
0 0
35 16 47 219214
94 100 100
6 5
0 6 7 7 7
0
0
0 2 7 1 8
0
0
0
0 0
6
0
Blood Proteins in Mucaca I 217
Table 111. (continued)
FAS
20 21 22
23
24
26
25
27
28
29
CYC
30 31
98 - - 97 98 99 100 100 100 100 100
0
0
0
0
0
0
0
0
0
0 - - < l < l < l
0
0
0
0
0
I - 3
2 < 1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1 - 0
0
0
0
0
0
0
0
0
-
-
0
0
136
100
-
-
0
0
0
0
0
0
0
0
0 0 294 223 206 I36 33 78
- - 100 - 100 - - -
0
7
o - -
0
0
-
0
(
I36 0 0 2 6 1
0
38- 45 O--O
62- 55 O - - O
0
)
-
0
-
-
0
-
0
0
- -
-
-
74
62
- - -
-
-
38
-
0
- _ _ - - - - _ _ - -
1 7 0 0 4 9
0
- - - 95 100
- 0
0
_ - _
-
- - - - 0
0
0
0
0
0
0
0
0
97 100 100
0
0
0
0
0
5 < 1
3
0
0
0
0
0
33 217 190 136
0
0
0
0
80
0
0
8
0 1 2
33 78
0
32
33
34
35
36
37
38
0
0
0
0
0
0
0
0
0 1 6
0
17
0
0
0
0 3 5
0
22
86 100 100 100 100 100 100 100 96 100 100
0
0
0
0
0
0
0
0
4
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0 < 1
0
0
1 4
0
0
0
4
0
0
0
0
0
0
7 21
46
29 538 80 87 96 880 I31
19
100 100 100 100
99
0
1
0
131
100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
29 538 80 87 96 880
100 100 100 100 100 100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0 <1
0
0
0 <1
0
29 538 80 87 96 880 131
0
0 0 0
0
0
0
0
0
0
0
50
72 99 - 53 58 72 99 97 50
18 1 - 41 42 28
1
3 50
50
0 0 0
0
0
0
0
0
0
0
0
0
0 0
0 0 0
0
10 0 6
0
0
0
0
0 0
0 80
197113 0 296 222 210 I36 33 78
100 - - 100 100 100 97 100 100 100 100
0
0
0
0
0
0
0
0 - 0
0
0
0
0
0 - 0 0
0
0
0
0 - 0 0
0
0
0
0
0
0
0
3
0
0
0
0
0 - 0
7 80
197 0 0 296 222 212 136 33 78
0
100
0
0
0
0
I51
100
0
0
0
0
102
0
0
0
0
0
0
0
100 100 100 100 100 100 95
0
0
0
0
0
0
5
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
29 538 80 87 96 880 202
- 100 100 100 100 95 100
0
0
0
0
5
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0 538 80 87 96 880 202
- - 0 0
31-69 0 - -
0
-
0 - -
0 - 43
0
0
0
0
33 222
6
1
94 99
0
0
0
0
0
0
84 217
<1
0
0
0
0
0
0
0
0
0
201 136 33 78
7
1
0
0
0
0
99 100 100 100 100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
189 136 33 78
7
42
43
o - o o - o -
0
0
0
0
0
0
0
80 87 96 880 186
71
- - - - - - 100 100
I ) - - - - - 0
o
92
0
0
0
0
0
0 55
52
100 - - - - 8 6 O
o - - - 0 o
o - - - 0 - 100
o - - - 1 4 O
o - - - 0 o
0
0
50
4
93
3
0
0
47
0
40 41
0
0
46 538
0
0
21
1
99
0
0
0
48
0
39
100 99 82 100 54 99 33
0
0 - 30 0
0
0
0
0
0
0
0
o - o 0
0
0
0
0
0
0
0
0
0 0 0
0
0
6
0
0
0 6 7 1 0 0 1 0 0 - 7 0 0
0
0
0
0
0
0
0
0
o - o 1
0
1 1 2
0 4 6
1
0
0
0 0 -
- - - 100 100 100 100 100 100 100 100 100 100 100
- - - 0 0
0
0
0
0
0
0
0
0
0
_ - -
ARC
SIN RAD ASS
99
0
0
0
95 139
100 100
0
7
_ - - - _ -
o - - o
-
0
FUS
81
19
0
28
0 154
0
-
- 100
-
- -
0
0
- -
0145
98
- -
0
-
-
- -
-
0
-
2 0
-
0
-
0 0 2 2
100 - 94
0
-
o - o o - o 0 -
6
-
0 -
0
-
28
0
9
0
-
100
-
100
0 0 -
0
0 0 -
0 -
0 -
19
100
0
0
0
0
19
28
0
9 0
72 - 100 280 -
0
74
26
0
0
0
68
100
0
0
62
38
0
0
0
28
0
0
0
49
0 0 -
0 0 -
0 28
-
-
0
0
0
0 59 0
0
0
- 51 - 49 - 0 - 0 - 0 0 202
0
- 100 - 0 - 0 - 0 - 0 0 193
0
218 I Fooden and Lanyon
Table 111. (continued)
Locus
and
allele
SIL
Papio 1 2
NEM
3
4
5
6
7
8
9
10
100 - - 100 - 100 100 100 100 100
0-0 0 0
0
0
0
0-0 0 0
0
0
0
N = 502 0 0 9 0 32 7 67 50 19
LDHB
1
100 - - 100 - 100 100 100 100 100
0
0
2
0 - 0 0 0
0
0
0
3
0-0 0 0
0
N = 502 0 0 10 0 32 7 64 50 19
PGD
A
0 - - 99 98 92 100 100 98 87
B
0-0 0 0 0
0
0
0
1
3
c
0 - - 0 2 5 0
0
0
0
D
0 - - 0 0 0 0
0
E,FdlOO-0 0 0 0
0
0
0
0
0 1 0
0 -- 0 0 0 0
M
1 0 3 0
0
1
0
0
Othere
N = 502 0 0 73 162 104 7 71 50 19
0 81 68 90 - 100 100 100 100 100
PGM-I 1
0 0
0
0
0
0 1932102
0
0
0
0 o o o - o o
3
0
0
0
99 o o o - o o
4
0 0
0
0
0
1 0 0 0 5
N = 502 8 1 1 10 0 32 7 64 50 19
IDH
1
2
3
__
PGM-I1
PHI
PI
1
2
3,4d
6
7
0 - - 100 - 100 100 100
0 - -
loo--
0 - 0 - N = 502 0 0
100 88 100
1
2
0 0 0
0 1 2
4
5
0 0 0
0 0 0
9
0 0 0
17
0 0 0
18
0 0 0
Other'
N = 502 8 11
0 - A
0 - - 5
B
0 C
D
0 - - 1 2
N , P , Q d 100 - -
-
TBPAh
Othes
0 - N =
502 0 0
F
100 - F+
0 - F0 - S
S'
N
=
0 - 0 502 0
-
0
MUL
MAU TON OCH BRU HEC NGS NGA
0 0 0
0 0 0
0 0 0
0 0 0
10 0 32 7
81 99 100 100
0 0 0 0
0 0 0 0 0
1 9 0 0 0
0 0 0 0
0 0 0 0
0 0 0 0 1
0 1 0 0
21 34 32 7
0 1 0 0 0
1 6 6 0
83 83 94100
i l
0 0
0 0
0 0
0 0 0 0
74 222 32 7
91 100 98 90
0 0 1 0
0 0 0 0
9 0
1 0
0 0 0 1
67 182 127 7
11
12
0
90
10
50
50
82
18
38
62
84
16
0
0
0
0
0
0
0
0
0
0
0
64
74
50
96
0
0
0
0
0
0
0
3
1
0
0
64 50
0
1
0
99 100
0
0
0
0
0
0
0
0
0
0
0
0
8
8
0
0
0
0
0
0
19 17
92 100
0
5
0
0
3
0
19 17
0
0
3
0
97 100
0
0
0
13
14 15 16 17 18 19
100 100 100 100 < 1 1 - 14 21 0
0
0
01009983750
0
0
0
0 0 3 417 35 16 48 219214 0 76 31 0
100 100 100 100 100 100 - 100 100 0
0
0
0 0 0 0 0
0
0
0
0
0 0 0 017 35 16 47 219214 0 76 31 0
74 87 100 100 99 84 84 97 99 0
0
0
1 1 6 1 6 3 10
0
0
0
0
0 0 0 0 0 0
0 0 0 0 0 0
1
0
0
0
0
0
0 0 0 0 00
0 0 0 0 0 02 6
0
0
0 0 0 0 0 00 1 2
17 35 16 53 219238 25 76 46 0
100 100 100 98 100 100 - 97 96 0 20
0
0
0 0
0
3 20
0
0
0
0 0 0 00
0
0
2 0 0 0 00
0
0 0 0
0
17 35 16 47 219214 0 76 31 0
0
0
0
64 50 19 17
99 100 100 100
0 0 0 0 0
1 0 0 0 0
0
0
0
0
0 0 0 0 0
75 50 19 17
0
0
0
0
35 16
99 100
0
0
1 100 100 - 97 100 99
0 0 3 00
0 0 0 00
0 0 0 00
0 0 0 047 219214 0 76 31 0
98 92 93 - 96 96 0
0 0 - 3 2 -
0
0
0
o o - o o -
0
0
0
0
0
1
0 3 - 0 0 8 3 - 0 2 O O - O O -
0
0
0
0
1
35
0
1
99
0
0
0
0
0
0
0
16
0
-
0
0
-
1 0 1 - 1 0 47 216214 0 76 31 0
0
0 0 0 0 0 0
3
0
0 0 6 0 1 97 100 100100 94 100 99 0
0
0
35 16
100 100
0 0
0 0
0
0
0 0 0
35 16
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0 0 0 -
47 32314 25 76 46 0
100 83 88 88 80 83 0 0 0 0 0 0 0 0 0 0 0 17121220170 0 0 0 0 58 32342 39 76 44 0
Blood Proteins in Macaca / 219
Table 111. (continued)
FAS
20 21 22
23
24
- - -
73
27
0
33
100
0
0
33
86
89
10
< 1
222
100
0
0
223
89
_ - -
- - 0
- _
0
0
- - - - -
a
0
0
97 - 0 - 3 - < 1 - 0 - -
0
10
4
0
0
0
136 0 0 296
- 100
- - 0
0
0
- - - 0
0 0 0 33
0 - 0 - -
- _
_ - _ - -__
-_
-
-0 0
100
- 0
0
0
- 0
-
0
96301-
-
0-
-
0-
0059 0
266 31 <10<1188 0
99 0010195 0
-
0
-
-
33
99
4
0
1
0
0
0
0
117
1
66
32
1
0
<
0 356
- 83
- 0
- 0
- 17
- 0
0 343
25
65
35
0
198
100
0
0
204
100
0
0
11 < 1
0
0
0
0
0
0
0 < 1
218 212
98 98
0
0
2
2
0
0
< 1 < 1
221 187
FUS
CYC
26
27
28
29
30
31
15 56 100 8 6 9 8
2
85 44
0 14
0
0
0
0
0
7 21
136 33 78
100 100 100 100 100
0
0
0
0
0
0
0
0
0
0
7 21
136 33 78
100 100 100 100 100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
7 99
136 33 78
94 83 100 - 90
0
0
0
0 0
0
0
0 l
6 1 7
0 0
0
0
0 0 21
136 33 78
8
92
0
44
100
0
0
50
100
0
0
0
0
0
<
137
100
0
0
0
0
39
32
33
34
35
0
0
0
0
100 100 100 100
0
0
0
0
29 538 80 87
100 100 100 100
0
0
0
0
0
0
0
0
44 538 80 87
100 100 100 100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
28 538 80 87
100 100 100 100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
29 538
ARC
SIN RAD ASS
0
0
80
87
36
37
38
39
0
100
0
96
100
0
0
96
100
0
0
0
0
0
0
96
100
0
0
0
0
100
0
880
99
1
0
880
100
0
0
0
0
0
0
880
99
~
1
0
90
10
0
131
100
100
0
0
19
100
0
0
0
131
100
0
19
100
40
41
42 43
47 0
53 - 100
0 0
28
0
9
91 - 100
0 9 28 0
100 -
-
-
0
-
0 0 -
9 0
42 0 -
0
0
0 -
0
0
0
0
0
188
100
01
0
0
0
0
0
96 880 131
0
0
0
0 0 0 - 5 8 0 0 -
0
0 -
0 100 100 100 100 98
99 100 100 100 100 - 100 100
0
0100
0
0
0
0
2
0
0
0
0
0 0
0
0
0
0
0
0
0
0
0
0
0
0 1
0
0
0
0 0
0
0
0
0
0
0
0
0
0
0
0
0 0
0
0
0
0
0
0
0
0 21
39
29 538 80 87 96 880
223 204 136 33 78
99 100 99 97 100 100 67
92 100 87 100 100 100 97
0
0
0
0
0
0
1
0
0
1
3
0
0
0
2
0
0
0
0
0
0
0
8
0
0
0
0
0
<
1
1
0
0
0
0
0
3
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
3
0
0
0
0
0
<
1
0
0
0
1
7 51
64
29 538 80 87 96 880
223 204 136 33 78
l < l
0
0
0
0
1
0
0
0
0
0
0
<
1
7
80 72 22
0 79 64 95
1 <1
0
0
0 <I
19 27 78 100 21 36
4
90
99 95 100 100 100 100
0
0
0
0
0
0
0
2
0
5
0
0
0
~
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
7 127 139
66 538 80 87 96 880
291 222 136 33 78
90 96 100 100 52 - 9 5 7 3 0 0 0 0 0 0
0
0
0
0
0
0
0
0
0
0
0
0
0 0
0
0
0
0 0
0
0
0
0
0
0
0
5
27 100 100 100 100 100 100
10
4
0
0 48 0
0
0
0
0 0
0
0
0
0
0
0
0
0 131 206 149 538 80 87 96 880
274 259 136 33 78
0
73
74
0
0
0
26
19
68
0
0
0
32
I31
75
0
0
100
0
0
0
0
25
131
0
0
100
01
0
0
131
29
0
0
71
0
196
0
0
0
28
100
0
0
0
0
28
0 -
-
0 -
0 177
- 100
0
0
0
0
0
9
0
-
-
0
100 - 100 0 0 0
-
0 -
0
0
-
0 -
0
19
100
0
0
-
28
100
0
-
0 -
0
0
-
0 -
0
0
0 -
0
0
0
19
0
0
100
0
0
0
19
66
0 -
0
-
9
99
0
-
-
0 0 -
0
-
0 -
0
-
0 -
0
0 28
0
0 0 100 0 0
0
28
97
-
1 77 0
0 -
1 98 0 0 -
<1
-
0 249
0
- 100
-
0
0
-
0 -
0
34
0
3
-
0 -
0
0
-
171
28
0 -
0 0 241 0
220 I Fooden and Lanyon
Table 111. (continued)
Locus
and
allele
Tf
‘IL
Papio 1 2
NEM
3
4
5
6
O O O < l 2 0 B
0 0 0 1 1 4 7 C
0 0 0183035D
012 0 5<1<lE
0 0 0 123023F
0 0 0 0 1 0 F’
0 88 100 53 29 34 G
0 0 0 0 0 1 H’
CP, DP,
Dp’,Epd 100 0 0 0 0 0 0 0 0<1 3 0Other’
502 8 11 102209203 0
N=
MUL
MAU TON OCH BRU HEC NGS NGA
7
8
9
10 11 12 13 14 15 16 17 18 19
0
0
0
0
53
3
44
0
-
-
-
-
-
-
-
-
-
15
0
0
-
-
-
-
-
-
- - - - 0
4 2 8 2 3 5
0 26 4535 23 2830
0
7 22 12 20 7 13
0
1 2 1 0 9 14 3
91 14 4 9 9 19 15
0
0 3 0 3 013
9 26 16 11 28 24 17
0 < 1 1 1 5 3 3
0
- - - -
-
-
-
-
-
-
-
0
0
-
-
-
-
-
0
0
0
0
0
21
0
0 0
514 <1
0 0
2 1
18 21968855106 5967
population substructuring are not observed in macaques until individuals from
different countries or islands are compared. Variability between neighboring
troops (FST = 0.0368; SD = 0.07831, between localities within a province
(FST= 0.0605; SD = 0.1073), and between provinces within a country or island
(FST = 0.0816; SD = 0.0946) are low and show no statistically discernible differences. However, variances around these means are high as a result of obvious
outliers at all levels.
At the troop-within-locality level, 2 of 18 comparisons resulted in high FST
values. Kawamoto et al. [1981] reported allele frequencies for two troops of M.
fascicularis from West Sumatra (Gunung Meru A [n = 511 and B [n = 151).Samples
from these troops had significantly different allele frequency distributions for
three of the 11 loci that were surveyed (Fs,=0.2567). Shotake and Santiapillai
[1982], in their study of M . sinica, collected samples from three troops located
within several kilometers of one another in the Trincomalee area of Sri Lanka;
these troops exhibit different major alleles at 3 of the 11 surveyed loci
(FsT=0.2442). It seems unlikely that the observed differences were a result of
sampling error because significant fractions of these M. sinica populations were
sampled (17%, 40%, and 76%). The most parsimonious explanation is that these
two sets of adjacent troops have experienced reduced gene flow relative to other
sets of neighboring macaque troops. Excluding these two localities, FsT for
variation between troops within localities was calculated to be 0.01 (SD = 0.01).
At the level of localities within province, one of 14 comparisons of allele
frequencies is aberrant. The M . fascicularis allele frequency data [Kawamoto et
al., 19841 suggest that, in West Java, the Jatibarang troop has diverged from the
three troops sampled at Pangandaran more than is typical of troops inhabiting the
same province (FS~=0.4130).
This high FST value appears to be a result of
relatively lower genetic variability in the Jatibarang troop. For the five surveyed
loci that were polymorphic in West Java M. fascicularis, the Jatibarang macaques
exhibit only 6 of the 12 alleles found in the Pangandaran troops. With 26
individuals sampled for the Jatibarang troop and a total of 44 for Pangandaran, it
is unlikely that these differences could be due to sampling error. Genetic differentiation between these troops is perhaps not surprising because, although both
localities are located in West Java, they are separated by the main Javan
mountain chain. Elimination of West Java results in a revised estimate of FSTfor
localities within provinces of 0.0333 (SD = 0.0363).
Blood Proteins in Mucucu I 221
Table 111. (continued)
FAS
20 21 22
~
23
24
25
FUS
CYC
26
28
29
0 -
27
-
<I <1 -
-
0
0
- 100
30
31
32
33
34
35
36
SIN RAD ASS
37 38
39
40
ARC
41
42 43
~
4-25
2725
44- 50
5 - 0
4 - 0
5 - 0
6 - 0
3 - 0
1
13
66
3
3
4
2
7
2
2
24 15
59 60
5
2
< 1
1
0
l
8 1 3
0
0
0 1 -
o - - 9 8 - - 0
-
0
0
0
0
1
5
3
0
2 - 0
197 0 2 296 244 255 136
-
0 - 0
-
- - -
-
-
- - 0
0
0
0
0
0
0
0
0
0
0
0 1 3
0
0
0
0
0 22
90
0
0
0
0
0
0
2
0
0
1
0
0
0
0
O C l 2 7
2
0
1
1 100 100 100 100 100 92
0
0
0
0
0
0
0
0
0
0
0
5 3 4
< 1
0
0
0
0
0 4 1
0
0
0
0
0
0
0
0 151
6
168
0
0
0
0
29 538
0
0
80
0
0
87
0
0
5
63
0
2
29
0
1
0
0
0
0
2
~
96 880 239
1
I29
1
16
24
57
1
0
1
0
0
O
O
0
0
0
4
< 1
< l
< l
-
0 444 010051-
0
0
0 0
0
0
0
35 21 265 0
*For key to species abbreviations and country or island index nos., see Table I and Figure 1. Excludes loci a t
which frequency of major allele is greater than 0.95 in all species or partitioned countryiisland samples of
species. For geographically partitioned species (SIL, NEM, MUL, FAS, FUS, ARC), data for unlocalized samples,
omitted from this table, are presented in Table IV.
“Jolly and King [1985, p. 2061 report that a sample of 26 zoo specimens of M . szlenus is polymorphic for ChEs,
HbA, and Tf; the allele notation employed by these authors is not directly comparable with that of other authors
bAlleles B , E , and F
‘Table omits minor allele 4, which has a frequency of <.Ol in one sample of M . fusciculuris (Sumatra, Index
No. 24).
dAlleles restricted to Pupzo
“Alleles I , J , K , L, and S.
fAlleles 3, 7, 8, 10-16,19,and 20.
alleles C’, E, and F.
hFor allele frequency inPupio, cf. Shotake et al. [1977, p. 2281, Tanabe et al. [1977, p.3201, and Shotake [1981,
p. 2901.
’Alleles A, C’, D’, Dp’,G’, G - , and H .
At the level of province within country or island, FSTvalues were comparable
to those discussed above (mean FsT= 0.0816). However, once again one comparison
was aberrant. Nozawa et al. [19821surveyed two localities on the island of Shikoku
(Kochi prefecture), and one on the nearby islet Kashima (Ehime prefecture). The
latter population, although separated by only a few kilometers from Shikoku, is
genetically quite distinct, showing high frequencies for an otherwise uncommon
allele at CA-I. The resultant FST value of 0.3021 is considerably above that
observed for other between-province (or prefecture) comparisons. The remaining
13 comparisons of genetic differentiation between provinces within countries had
a mean FsT= 0.0605 (SD = 0.1073).
At the level of country or island within species, the degree of genetic
differentiation differs greatly for various species (mean FST = 0.2217; SD = 0.2107).
This result implies that the five species analyzed a t this level (M. silenus, M .
nemestrina, M . fuscata, M . rnulatta, and M . fascicularis) differ in the extent to
which they are subdivided. Two subspecies of M. fuscata were sampled and FSTwas
calculated to be 0.5413. If the Yaku island subspecies (population No. 32) is
eliminated from the analysis, the FST value for variation within the nominate
subspecies between islands drops to 0.1542. Only a single described subspecies is
known to have been sampled for M. silenus and M . rnulatta, and the resultant FST
values are 0.0352 and 0.0253 respectively. The two intermediate data points in
Figure 2 are for M. nernestrina and M . fascicularis, both of which have mainland
and island populations. If the data for these two species are subdivided into islands
within species and mainland countries within species, we would predict higher FST
-
222 I Fooden and Lanyon
Table IV. Allele Frequencies (%I at Polymorphic Loci (see Table 111) in Unlocalized
Samples of M . silenus (SIL),M . nernestrinu, (NEM), M. muluttu (MUL),M. fusciculuris,
(FAS),M. fuscutu (FUS), and M. arctoides (ARC).
Locus
and
ADA
A 1100 N=
1
0
1
2
3
4
N =
0
0
0 100
100
0
0
0
1 12
0
99
0
1
49
Species
and
SIL NEM MUL FAS FUS ARC allele
- 100 100 GC
0 14 29
0
allele
ACP
Locus
Species
3 100
97
0
0
0
0
0
44 31
38
0
62
0
4
SIL NEM MUL FAS FUS ARC
A 5 0 ~ 5 0 - N = l O
0
HbA"
1 5 0 2 5 0 -
N=
HbB
AK
N=
0
0
Alb
A - 100
B 0
N = 0 16
92
8
54
CA-I
0
A B -
30
63
c 5
D 2
D2 0
N = 0 152
100
(1
0
0
0
243
0
0
83 100 100
17
0
0
52 32
5
IDH
85
0
0
0
4
15
14 133
28
0
72
0
0
9
LDHB
- 100
0
0 137
-
89
0
7
0
x-
N=
0
100
1
-
0
-
0
6
94
66
46
0
54
104
0
CellEs
A A2 B N= 0
1 2 3 -
0
0
N=
ChEs
1
-
N=
Dia
0
A -
-
c -
N =
0
0
0
100
0
0
14
95
2
3
31
-
100 100
14218
0
0
0
12
88
53
70
0
30 100
31 29
0
0
- 100 100
0 14 50
-
0
A 0
0
-
-
1 -
N
-
-
PI
O
0
0 100
- 100
0
0 14 28
0
0
- 100 100
0 14 30
100
14
1 100
2 0
= 1
B D -
TBPA
s-
N=
Tf
0
F 0
B -
0
0
21
29
D 0
E F 7
0
F' G 100 43
0
H' Otherb 0
N= 1 7
c -
"Table omits one minor allele with frequency of 0.4% in M . fuscatu sample.
bAlleles A, D',G-, and H .
0
0
97
3
31
57
2
29 95
14
3
14 182
c -
N=
100 100
0 14 32
0
100 100
14 177
0
96 100
4
0
14 30
-
1 -
N=
-
0
1 50
2 50
N= 1
PHI
0
0
0
100 100
0
0
0
0
4
0 76
88 100
12
0
14250
-
N=
-
0
0
1 2 -
PGM-I1
CA-I1
0
0
0
N=
-
-
0
N=
PGM-I
CA-IC X +
_
0
1 -
PGD
-
-
1
N=
0
-
_
79
21
67
98 <1
2 100
43 175
3
46
9
1
7
4
20
2
0
0
7
0
7
78
0
0
0
0
0
2 97
6
0
0 41
11
2
0
0 <1 45
0
1
1
27 268 73
8
220
2
-
0
-
Blood Proteins in Macaca I 223
+
Troops within Locality
Localities within Province
Provinces within Countryllsland
lCountrles
Countries/lslands within Species
I
I
I
‘
Islands
Species within Species Group
Species Groups within Macaca
I
1
I
1
0
0.2
0.4
06
FST
Fig. 2. FSTvariation a t various hierarchical levels in Macaca; vertical line indicates mean, rectangle indicates
one standard deviation on either side of mean, and horizontal line indicates range. At the “CountriesiIslands
within Species” level, data for M . nemestrina and M . fascicularis have been further subdivided to show FST
differences between mainland countries within species and islands within species.
values for the former (due to the anticipated reduced gene flow between islands)
and lower for the latter. The resulting FSTvalues are as predicted (Fig. 2). Island
populations of these two species of macaques are more highly differentiated than
are mainland populations.
~
reported herein are consistent with species limits as currently
The F S values
described and support the use of species as the operational taxonomic units in the
phylogenetic analysis that follows.
Genetic Variability. Mainland and island populations differ substantially in
their genetic variability, as previously indicated by Goodman et al. [1965],
Ishimoto [19731, and Darga et al. [19751. Mainland forms exhibit 29% of macaque
alleles and island forms an average of 24% of the observed macaque alleles. When
an arcsin transformation is performed on these ratios and an approximate t-test of
the equality of two means conducted, the differences are observed to be significant
at the 0.01 level. Interestingly, the six lowest indices of variability are from
populations of the insular species M. fuscata (mean = 20.7%). However, the
insular species M . sinica exhibits a relatively high degree of genetic variation (28%
of macaque alleles), as reported by Shotake and Santiapillai [19821; this in fact is
the highest level of variation observed in any of the island forms.
The best opportunity to observe intraspecific variation in allele frequency is in
M . fascicularis, for which nine populations were surveyed for ten or more loci
(populations Nos. 21 and 22, surveyed for fewer loci, were omitted). Using the same
index of variability described above, we observed a striking geographic pattern of
variability. There is a significant decrease in genetic variability between Java and
Bali, where a 12% drop in number of alleles from west to east is observed. The four
populations to the west of the Java-Bali strait exhibit, on average, 47% of macaque
alleles and the five to the east 27% (P < 0.01).
FST statistics and indices of variability are simple summaries of the allele
distribution and frequency patterns. An examination of geographic patterns
Macaca
maurus
r-
tonkeana
l-
nigrescens
brunnescens
hecki
nigra
ochreata
fascicularis
cyclopis
mulatta
c
0.0
fuscata
0.2
0.1
Rogers’ D
Fig. 3. Fitch-Margoliash tree (BSD= 10.867)produced from distance analysis of macaque blood-protein data
using Papio as outgroup. Branch lengths correspond to Rogers’s modified Ds.
within polymorphic loci in M. fascicularis can provide additional information
about macaque evolution. Only two loci, Acp and CA-11, provide even weak
evidence of a simple unidirectional cline (Table 111). In Acp, frequency of allele A
varies slightly, from a low in the northernmost mainland population (frequency of
91%), through intermediate values in populations Nos. 21 and 23 (96% and 98%
respectively), to fixation in the remaining populations. CA-I1 alleles A and B also
could be interpreted as a clinal distribution in frequency, but data are available for
only three localities; of six possible random permutations of data for three
localities, 33% would simulate a cline. In contrast to these questionable examples
of clines, the remaining polymorphic loci exhibit no consistent pattern of geographic variation in allele frequency. For example, allele 2 a t the HbA locus occurs
at relatively high frequencies in three isolated portions of the range of M .
fascicularis (Table 111).
Phylogenetic relationships. The Fitch-Margoliash analysis resulted in a
network that was rooted using Pupio as the outgroup (see Fig. 3; %SD = 10.867).
This and subsequent analyses exclude M. silenus because few loci were surveyed in
this species. A jackknife manipulation of taxa identified four unstable regions of
the topology; these are reduced to polychotomies in Figure 4 to emphasize the
remaining nodes that are strongly supported by the allele frequency data. This
analysis subdivides Macaca into three major units that contain eight, four, and
three species; the first unit consists exclusively of non-Sulawesi species, and the
latter two units consist exclusively of Sulawesi species. Although the relationships
between these lineages are not resolved, M . nemestrina was identified as the sister
taxon to all other non-Sulawesi members of the genus.
Blood Proteins in Macaca / 225
Papio
Macaca
maurus
tonkeana
nigrescens
brunnescens
hecki
nigra
ochreata
nemestrina
fascicularis
cyclopis
mulatta
fuscata
arctoides
sinica
radiata
assamensis
Fig. 4. Jackknife strict-consensus trees derived from 16 pseudoreplicate Fitch-Margoliash analyses of macaque
blood-protein data using Pupio as outgroup. Branch lengths do not correspond to genetic distances. Polychotomies identify portions of the phylogeny that conflict between pseudoreplicate Fitch-Margoliash trees.
One limitation of this analysis is that 4 of the 22 polymorphic loci observed in
Macaca were not included because they were not surveyed in the outgroup taxon.
In an attempt to include the additional information represented by these characters, we re-analyzed each major group separately using M. nemestrina as the
outgroup taxon (Fig. 5). Since Sulawesi species are generally considered to
represent a monophyletic assemblage, we elected to treat them as such in this
analysis (Fig. 5b). Although the electrophoretic data do not provide strong
evidence for the monophyly of the seven Sulawesi species, the results are not
inconsistent with this hypothesis, and the unjackknifed Fitch-Margoliash tree
places all seven species on a single lineage (Fig. 3). The jackknife analysis of the
non-Sulawesi group, with M. nemestrina as outgroup, reveals two stable subgroups, one containing M. fasicularis, M. cyclopis, and M. mulatta, and the other
containing M. sinica, M. radiata, M. assamensis, and M . arctoides (Fig. 5a).
Jackknife analysis of the Sulawesi group, with M. nemestrina as outgroup, reveals
a stable branching arrangement among Sulawesi species (Fig. 5b).
DISCUSSION
Phylogeny: Morphological Inferences and Blood Protein Inferences
Macaques are readily divisible into four well-defined species groups based on
penial morphology (within species groups, species are listed in order of decreasing
tail length): 1) silenus-sylvanus g r o u p M . silenus, M. nemestrina, Sulawesi
stumptail species, M. sylvanus; 2) fascicularis g r o u p M . fascicularis, M . cyclopis,
M . mulatta, M. fuscata; 3) sinica g r o u p M . sinica, M. radiata, M. assamensis, M.
226 I Fooden and Lanyon
fascicularis
c y c lop i s
mulatta
fuscata
arctoides
sinica
radiata
assamensis
1
-
**
maurus
tonkeana
,-------.
--------- "';E
;ir;
**
"
I
nigrescens
b r u nne s c e n s
ochreata
thibetana; and 4) arctoides g r o u p M . arctoides only [Fooden, 19801. Structure of
the female reproductive tract unites the silenus-sylvanus group and the fascicularis group, but sharply separates these two groups from the mutually dissimilar
sinica and arctoides groups. Outgroup comparison with other catarrhines indicates
that penial anatomy is relatively primitive in the silenus-syluanus and fascicularis
groups-the former apparently more primitive than the latter-and is derived in
the sinica and arctoides groups. Zoogeographic evidence suggests that the silenussylvanus group was the first of these groups to disperse.
Within each of the three multispecies groups, interspecific variation of tail
length is directly correlated with the geographic distribution of species, except in
the geographically isolated North African species M. sylvanus. Assuming that a
long tail is primitive in macaques, as in other monkeys, the regular relationship
between tail length and geographic distribution suggests that, within each group,
species with shorter tails are successively derived relative to species with longer
tails.
Phylogenetic inferences based on a jackknife strict consensus analysis (JSCA)
of blood protein variation in macaques (Figs. 4, 5) are largely compatible with
inferences based on morphology and zoogeography. Some JSCA results indicate
new interrelationships unanticipated by morphological analysis; one JSCA result
is ambiguous; and one is inconsistent with morphological inferences.
Blood Proteins in Macaca I 227
Compatible results. JSCA of blood protein variation reveals three unambiguous groups of macaque species (Fig. 4;solid lines). The first group includes M.
nemestrina only; the second includes M. fascicularis, M . cyclopis, and M . mulatta;
and the third includes M. sinica, M. radiata, and M . assamensis. The three species
in the second group are characterized by high frequencies of CA-I:A and Dia:C; the
three species in the third group are characterized by high frequencies of ADA:l,
Alb:B, and CA-1:C (Table V). These three groups determined by blood protein
similarity obviously correspond to the silenus-sylvanus group, the fascicularis
group, and the sinica group as determined by penial morphology. Available data on
blood proteins in M. silenus are inadequate-because alleles at monomorphic loci
are unspecified-to include this species in JSCA. However, Shotake et al. [1986;
letter August 19871, who produced the original blood protein data on M . silenus,
report that the genetic distance of this species to M . nemestrina is less than the
distance to any other macaque species. This strengthens the concordance between
protein inferences and morphological inferences beyond that revealed by JSCA.
In JSCA (Fig. 41, M. nemestrina, representing the silenus-sylvanus group,
emerges as the sister-group of all non-Sulawesi macaques, including M . fascicularis, M. cyclopis, and M . mulatta (fascicularis group) and M. sinica, M. radiata,
and M. assamensis (sinica group). This agrees with morphological and geographic
indications that the silenus-syluanus group is the least derived of macaque species
groups.
Within the sinica group, JSCA indicates that M. sinica and M. radiata are
more closely related to each other than either is to M. assamensis. This corresponds
to the relationships among these species indicated by morphology and geography
[Fooden, 19881.
As discussed above, although JSCA is equivocal concerning the interrelationships of the Sulawesi stumptail species (Fig. 41, Fitch-Margoliash analysis of the
entire Macaca-Papio blood protein data set (without sequential deletion of individual species) tends to indicate that these species constitute a monophyletic unit
(Fig. 3) [also see Kawamoto et al., 19851, which is in agreement with morphology
and geography. When the Sulawesi protein dataset is segregated and subjected to
JSCA with M . nemestrina as outgroup (Fig. 5b), M. maurus emerges as closely
related to M. tonkeana and M. hecki emerges as closely related to M . nigra; a close
relationship between the species in each of these two species pairs also is indicated
by morphology and geography [Fooden,19691.The groupings indicated by JSCA are
not fully concordant with interrelationships implied by the taxonomy of Groves
[1980], who regards M. hecki as a subspecies of M. tonkeana [cf. Kawamoto et al.,
19851.
New indications. JSCA of non-Sulawesi species with M. nemestrina as
outgroup (Fig. 5) suggests that M . arctoides may be the sister-group of the
sinica-group species M . sinica, M. radiata, and M. assamensis, as previously
implied by Delson [1980]. A close relationship between M. arctoides and sinicagroup species is supported by allele frequencies of ADA:l and 3, CA-I:C, and HbA:I
and 2; such a relationship is contradicted by allele frequencies of A1b:A and 3
(Tables 111, V). Superficial evidence of tail length and facial skin color has been
interpreted to indicate a close relationship between M. arctoides and M . fuscata, a
member of the fascicularis group [cf. Bertrand, 19691.
JSCA of non8ulawesi species indicates that, within the fascicularis group,
long-tailed insular M . cyclopis and short-tailed continental M . mulatta are more
closely related to each other than either is to long-tailed M. fascicularis. M . cyclopis
and M. mulatta share relatively high frequencies of IDH:2 and TEC (Table V). A
228 I Fooden and Lanyon
TABLE V. Frequencies (%) of Major Alleles at Polymorphic Loci in Macaque Species
and Pupio; Condensed Summary of Data Presented in Tables I11 and IV*
Common
major
Locus
ACP
ADA
AK
Alb
CA-I
Ca-IC
CA-I1
CellEs
ChEs
Dia
HbA
HbB
IDH
LDHB
PGD
PGM-I
PGM-I1
PHI
PI
TBPA
Tf
allele
A
2
silenus group
Pwio
SIL
NEM
MAU
none
100
100
100
100
100
100
98
62lB
701A2
5716
lOO1B
89lX581X- 100
95
(87)
100
100
lOOlPb
100
100
100
100
100
(86)
100
6211
(91)
(91)
10013
100
9813
100
100
100
100
100
100
96
lOO1Pb
100
100
99/Pb (72)
98
lOO1Pb
100
100
95
100
95
(74)
lOOlPb
99
(84)
100
97
99
361G
100IPb 951G
531F
N=
502
1
A
A"
X+
B
1
1
A
2c
1
1
1
A
1
Id
1
C
F
100
96
98
100
98
-
100
7813
20
39 521
1575
TON
OCH
BRU
HEC
NGS
99
100
100
(91)
77103
100
95
100
99
100
(90)
8913
100
100
98
100
(90)
96
100
100
-
100
100
100
100
39lA2
100
100
100
100
100
97
100
100
100
100
411A2
100
100
100
100
100
100
8213
100
100
(74)
100
(82)
100
100
100
-
100
100
100
(54)
56lA2
100
100
100
100
(94)
100
6215
100
100
(87)
100
6212
99
99
100
-
100
100
100
100
1001A2
100
(88)
100
100
100
(94)
6215
100
100
100
100
(84)
100
97
100
-
50
(84)
100
100
(87)
100
5012
(92)
97
100
19
17
35
16
relationship between M . cyclopis and M . mulatta that excludes M . fascicularis
probably would not be anticipated on the basis of morphological and geographic
evidence, which instead tends to suggest that M. mulatta was derived directly from
a M. fascicularis-like ancestor [cf. Fooden, 1964, 19711.
Ambiguity. JSCA fails to resolve the relationship of the Japanese stumptail
macaque M . fuscata to other non-Sulawesi macaques. High frequencies in M .
fuscata of ADA:I, CA-II:A, IDH:2, TBPA:S, and TEF indicate divergent relationships to other macaque species (Table V). Morphological and geographic evidence,
however, strongly indicates that M . fuscata is a member of the fascicularis group,
probably derived from a M . mulatta-like ancestor [Fooden, 19803. Protein evidence
of the relationship of M . fuscata to other macaques may have become obscured a s
a result of insular founder effect or genetic drift.
Inconsistency. JSCA separates Sulawesi species from all non-Sulawesi species (Fig. 4) including M . nemestrina. Sulawesi species are unique in their high
frequencies of CA-I:A2 and 0 3 , HbB:3 and 5, and PGM-I1:2 (Table V). This directly
contradicts morphological and geographic evidence, which strongly implies that
Sulawesi species are members of the silenus-syluanus group and probably are
derived from a M . nemestrina-like ancestor [Fooden, 19751. As noted above for M .
fuscata, insular founder effect or genetic drift may have obscured protein evidence
of the relationship of Sulawesi macaques. Other authors, however, using different
subsets of the protein data and different statistical procedures, have found
Sulawesi species to be closely related to M . nemestrina [Darga et al., 1975; Cronin
e t al., 1980; Melnick and Kidd, 1985; Kawamoto et al., 19851. JSCA results
Blood Proteins in Macaca I 229
TABLE V. (continued)
fascicularis group
__
NGA
FAS
CYC
MUL
FUS
SIN
100
96
99
100
43lA2
100
100
100
97
100
98
6315
100
100
100
98
9912
98
100
100
911F
98
100
100
96
99
100
6OlA
97
100
97lC
6911
100
(68)
100
(94)
97
100
97
67lB
(91)
5810
100
100
99
99
100
100
100
931C
10011
100
9212
100
100
100
100
(92)
(90)
(73)
901c
100
97
100
(66)
99
100
(64)
100
100
75lC
10011
100
9512
100
(92)
99
100
(93)
100
(86)
391C
100
10011
98
100
95
100
96lA
98
100
100
looil
98
100/2
100
100
99
97
(94)
98
1001s
96lF
100
lOOl1
96
98lB
67lC
100.
100
99
100
9511
100
(90)
100
100
100
(68)
(75)
100
711s
34lG
10OlB
lOO1C
100
100
100
(81)
100
7411
100
100
100
100
(74)
100
100
100
(66)
631C
18-
1491492
39 206
55239
171
58
~
65 1414
arctoides
group
sinica group
1282005
RAD
ASS
ARC
100
100
6411
84lB
1OOlC
100
100
(72)
6211
100
7013
100
71lC
100
98lA
(94)
100
100
5111
100
10012
100
5810
100
100
99
98
100
531H’
5311
-
19-
-
5312
(91)
100
100
100
100
100
97
57lE
1835
9359
~~
*Where tabulated frequency is followed by allele designation, major allele of species differs from common major
allele in Mucacu and Papio; parentheses enclose common major allele frequencies that are less than 0.95 (i.e.,
“not fixed”); Dash (-1 indicates no data. Excludes Gc, known only in SIL, where frequency of D is 0.72.
“Allele A designated a s common major allele because of its high frequency in Papio; in OCH, the frequency of
allele A is 0.39 (same frequency as allele A2).
bAlleles restricted to Papio (for details, see Table 111).
‘Allele 2 designated as common major allele because of its high frequency in Papio.
OCH, the frequency of allele I is 0.50 (same frequency a s allele 2).
concerning relationships of Sulawesi species might have been different had we
been able to include M . silenus in this analysis.
Genetics of Insular Populations
Analysis of the hierarchical distribution of genetic variation in macaques
using Wright’s FsT statistics demonstrates that insular populations of macaques
have differentiated to a greater degree than have mainland populations. Subsequent investigation of within-population variation suggested that this differentiation was a result, in part, of lower genetic variability in island populations. These
findings concerning the distinction between insular and continental forms, are
consistent with other biochemical investigations [cf. Berry, 1986; Kilpatrick, 1981,
and references therein].
Founder effect and genetic drift are thought to be the primary causes of
reduced genetic variability in natural populations. The significantly lower genetic
variability described herein for insular populations of macaques, and for mammals
in general [Berry, 19863, suggests that the gene pools of island populations are
230 I Fooden and Lanyon
more likely to be affected by these factors than are continental populations.
The actual cause of reduced variability, whether due to founder effect or
genetic drift, is of great interest to island biogeographers [Berry 19861. Berry
argues that mammalian biochemical data support the hypothesis that reduction in
genetic variability occurs at the time of colonization because “a relict population
will be expected to have an amount of variation initially similar to the source or
parental population, whereas a population founded by a finite number of colonizers
will be expected t o have a reduced amount of variation” (our emphasis). However,
the key word here is initially. Reduced genetic variability would also be expected
in small relict populations that have subsequently experienced increased genetic
drift. The linear arrangement of M . fascicularis populations provides an excellent
opportunity t o determine whether the insular populations of this species are
relictual or the result of colonization. If islands in a linear series were colonized in
stepping-stone fashion by a small number of individuals, then we would expect to
observe nested subsets of shared primitive alleles from mainland to nearshore
islands to the terminus. Each population should possess only those ancestral
alleles, or some subset of them, that are present in the adjacent population from
which it was derived. In contrast, if each population in a linear series were the
result of vicariant events that subdivided a single large panmictic population, then
each population could be expected to be independent in terms of the alleles present.
In over one-third of polymorphic loci in M . fascicularis (7/18) an allele is present
that was observed in two or more populations but was absent in geographically
intervening populations. The presence of this “leapfrog” pattern of geographic
variation [Remsen, 19841 is more easily explained if the 11 M . fascicularis
populations were formed through vicariant subdivisions of a single ancestral stock
and have become less genetically variable as a result of subsequent genetic drift.
Vicariance may have been initiated by postglacial rise of sea level, which
fragmented previously continuous Sunda Shelf habitats of M . fascicularis [cf.
Heaney, 19841.
Examining levels of genetic variability alone may be insufficient to determine
whether island populations are relictual or the direct result of dispersal. Both
scenarios can produce the same reduction in the level of genetic variability; the
former as a result of genetic drift and the latter as a result of founder effect. Only
through an investigation of allele distributions can we hope to distinguish between
these two alternative explanations for the origin of island populations.
Phylogeny Reconstruction
Having confirmed that island populations are generally less genetically
variable than are mainland populations, we would like to discuss the implications
of this finding for phylogeny reconstruction. Most distance analyses cluster taxa on
the basis of perceived genomic similarity by assuming that time-dependent
divergence characterizes the proteins that are being analyzed. If changes in allele
frequency have occurred as a result of founder effect or increased genetic drift, this
correlation between genomic similarity and time since divergence will be weakened because such factors can result in drastic changes in a few generations
[Throckmorton 1978; Aquadro and Kilpatrick 19811. For example, two species
reproductively isolated for thousands of generations may be less distinct electrophoretically than are two populations (one of which experienced a severe population bottleneck) that have been separated for only one or two generations.
The macaque data presented herein provide an excellent example of how rapid
changes in allele frequency could affect phylogeny reconstruction. The jackknifed
Fitch-Margoliash analysis of the Sulawesi macaques identified M . ochreata as the
Blood Proteins in Macaca 1 231
sister taxon of the remaining Sulawesi species. However, an analysis of allele
distributions demonstrates that M. brunnescens could be interpreted as having
resulted from the recent isolation of a small group of individuals of M . ochreata. M.
brunnescens has no alleles that are not found in M . ochreata (the reverse is not
true). These two taxa were not identified as sister-taxa because of frequency
differences-differences that are highly susceptible to change during colonization
or population bottlenecks. We are not arguing that this is necessarily the true
sister-group relationship, only that electrophoretic frequency data must be interpreted cautiously when dealing with insular distributions. The unusually high FST
values found for variation between troops of M . fascicularis at a single locality in
West Sumatra, between troops of M. sinica at a single locality in Sri Lanka,
between localities for M . fascicularis in West Java, and between M . fuscata
populations in the prefectures of Japan suggest that such serious bottlenecks are
not uncommon in macaques.
CONCLUSIONS
1. In Macaca, at the species-group level, phylogenetic interpretations of
electrophoretic data are largely compatible with hypotheses generated from
morphological studies.
2. Electrophoretic data support a monophyletic assemblage consisting of M .
arctoides, the sinica-group species, and the fascicularis-group species; these data
further suggest that M.arctoides may be more closely related to the sinica group
than to the fascicularis group.
3. Insular populations of macaques are significantly less genetically variable
than are continental populations.
4. Allele distributions in M . fascicularis are most parsimoniously explained by
a relictual rather than a dispersal origin for the 11 populations that have been
studied electrophoretically .
5. The low genetic variability of insular populations indicates that caution is
required when attempts are made to extract phylogenetic patterns for these taxa
from allele frequency data.
6. The comprehensive data matrix compiled for this study provides a research
resource for future comparative biochemical studies of Macaca.
ACKNOWLEDGMENTS
We thank Takayoshi Shotake, Primate Research Institute, Kyoto University,
for providing va-luable unpublished data on allele frequencies in Macaca silenus;
George Barrowclough, American Museum of Natural History, for supplying the
FSTcomputer program; and Bruce D. Patterson, Field Museum of Natural History,
for helpful advice and discussions. We also thank Clara R. Simpson, Field Museum
of Natural History, for skillfully assisting in the preparation of Figure 1. Four
anonymous reviewers contributed valuable suggestions for improving the manuscript.
232 I Fooden and Lanyon
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APPENDIX A: ANNOTATED LIST OF SOURCES OF DATA
Sources of data are organized in this list according to the laboratory or
laboratory-group affiliations of a u t h o r s cited. Where d a t a derived from the same
specimens h a v e been published more than once, only the most comprehensive and
detailed presentation of these d a t a is listed here. For keys to abbreviations of
species and loci, see Tables I and 11. In “Species” entries, a parenthetical notation
Blood Proteins in Macaca I 235
following a species abbreviation indicates that more than one troop or locality have
been sampled for that species in the cited study. In “Loci” entries, the notation
“All” refers to 30 proteins listed in Table 11; five proteins that are monomorphic in
Macaca and Papio (Table 11, footnote) are omitted from consideration. Comments
accompanying each reference indicate how problems in collating data published in
various sources have been resolved and how data have been used in the present
analysis.
Columbia University; New York University; Yale University
Melnick et al. [19841, p. 349.
Species: MUL(5). Total samples, 5.
Loci: All except Alb, CA-IC, Dia, Gc, LAP, PI, TBPA, and TO.
Total loci, 22 (see Comment).
Comment: Dia excluded, phenotypes not comparable with those
in other studies [Melnick et al., 1986, p. 133,
footnotel; ten monomorphic loci excluded, not reported
in other references.
Melnick et al., 1986, p. 133.
Species: MUL. Total samples, 1.
Loci: All except Alb, CA-IC, Dia, Gc, LAP, PI, TBPA, and TO.
Total loci, 22 (see comment under Melnick et al. [1984]).
Comments: 1)Allele frequencies for this sample have been
computed by subtraction, based on data in columns P2
and P, Table 2 (cf. Table 1, p. 131).
2) Frequencies of minor Tf alleles A, C’, G’, H , and
H‘ have been estimated by equal allocation of residual
X = 0.032 (see Table 2, p. 133, footnote).
Gifu University; Japan Monkey Centre; Kyoto University; Mie Prefectural University; Nagoya University; University of Indonesia, Jakarta; University of Tokyo
Hayasaka et al. 119871, p. 508.
Species: FUS. Total samples, 1.
Loci: All except CA-IC and Gc. Total loci, 28.
Comment: This paper was received too late for its data to
be used in calculation of FSTvalues or generation of
trees; however, these data are included in Table 111.
Ishimoto [1972al, p. 263.
Species: FAS. Total samples, 1 (see Comment 1).
Loci: HbA. Total loci, 1 (see Comment 2).
Comments: 1)Kampuchea sample only; other data are
encompassed within more comprehensive references.
2) Alp data excluded, not concordant with
corresponding data published by Nozawa et al. [1977,
p. 22, footnote] and Kawamoto et al. [1982, p. 2751.
3) For HbA allele concordance, cf. Darga et al.
[1975, p. 8041 and Nozawa et al. [1977, p. 221.
Ishimoto [1972bl, pp. 339, 343, 344.
Species: ARC, CYC, FAS(4), NEM(2). Total samples, 8 (see Comments 1-3).
Loci: Acp, Dia, PHI. Total loci, 3 (see Comment 4).
Comments: 1)FUS and MUL excluded, superseded by Nozawa
et al. 11977, p. 22; 1982, p. 2551 and Kawamoto et al.
[1982, p. 2751.
2) FASPhilippines sample also reported in part by
236
t
Fooden and Lanyon
Kawamoto et al. [1982, p. 2751; cited here for larger
Acp sample size only.
3) CYC sample also reported in part by Nozawa et al.
[1977, p. 221; cited here for larger Acp and PHI sample
sizes only.
4) PGM excluded, not concordant with corresponding
data in other references [cf. Nozawa et al., 1977,
p. 231; PGD excluded, superseded by Darga et al.
[1975, p. 8031.
Ishimoto et al. [19741, p. 55.
Species: FAS, MAU, MUL, NGA. Total samples, 4 (see Comment).
Locus: IDH. Total loci, 1.
Comment: FAS and MUL samples included here are those of
unknown country of origin only; 13 samples reported in
this reference are encompassed within more
comprehensive references.
Kawamoto & Ischak, [1981], p. 240.
Species: FAS(4). Total samples, 4 (see Comment 1).
Loci: All except CA-IC, CA-11, and Gc. Total loci, 27.
Comments: 1) Kukuh East sample excluded, superseded by
Kawamoto et al. [1984, p. 1331.
2) HbA allele frequency computation based on one-locus
hypothesis to preserve comparability with other studies
[Darga et al., 1975, p. 804; Nozawa et al., 1977, p. 221.
3) PI allele frequency computation in this reference
omits minor variants in one sample; Hp allele
frequency computation omits one silentomorph in one sample.
Kawamoto & Suryobroto [19851, p. 36.
Species: FAS. Total samples, 1.
Loci: All except CA-IC, CA-11, GC, HbA, Hp, PGM-I, PGM-11,
TBPA, and Tf. Total loci, 21 (see Comment).
Comment: Four monomorphic loci (CA-11, HbA-I, HbA-11, TBPA)
excluded, alleles unreported; Tf data excluded,
obtained by new polyacrylamide technique, not
comparable with corresponding data in other references.
Kawamoto et al. [1982], p. 275
Species: FAS(3), MUL(2). Total samples, 5 (see Comment 1).
Loci: All except Alb, AK, CA-IC, CA-11, Es-D, Gc, and TBPA.
Total loci, 23 (see Comment 2).
Comments: 1) FUS excluded, superseded by Nozawa et al.
[1982, p. 2541; MUL:China, and MULIndia excluded
superseded by larger samples in Shotake [1979, p. 4481;
Papio excluded, superseded by expanded and more
detailed data in Shotake [1981, p. 2871.
2) Alb data excluded, superseded by revised data in
Shotake [1979, p. 4441.
3) FAS:Philippines/Acp data excluded, larger samples in
Ishimoto [1972b, p. 3391.
Kawamoto et al. 119841, p. 135.
Species: FAS(29), Total samples, 29.
Loci: All except CA-IC, CA-11, and Gc. Total loci, 27 (see Comment 1).
Comments: 1) HbA-I and HbA-I1 are treated as a single locus
Blood Proteins in Macaca I 237
(HbA) to preserve comparability with other studies
[cf. Darga et al., 1975, p. 804; Nozawa et al.,
1977, p. 221. In the Sumatra:Belawan sample, where exact HbA
phenotype frequencies are not available, HbA allele frequencies
used here are the means of theoretically possible values.
2) Tf data presented in this reference were obtained
by a new polyacrylamide method and are not comparable
with starch gel Tf data reported in other studies.
These polyacrylamide Tf data are therefore excluded
from the present analysis. Instead, starch gel Tf data
previously reported for many of these populations
[Kawamoto et al., 1981, p. 201 are substituted here.
Kawamoto et al. [19851, pp. 46, 49.
Species: BRU, HEC, MAU(41, NEM(21, NGA, NGS, OCH, TON.
Total samples, 12.
Loci: All except Gc, Hp, and Tf. Total loci, 27 (see
Comments 1 and 2).
Comments: 1)HbA-I and HbA-I1 are treated as a single locus
(HbA) to preserve comparability with other studies
[cf. Darga et al., 1975, p. 804; Nozawa et al.,
1977, p. 221.
2) Tf data presented in this reference were obtained
by a new polyacrylamide method and are not comparable
with starch gel Tf data reported in other studies;
polyacrylamide Tf data are therefore excluded from the
present analysis.
3) For CA-IC concordance, cf. Darga et al.
[1975, p. 8001.
4) Two typographical errors in Table 6 (allele
frequencies of MAU/Alb:B and NEM:Sumatra/CA-1:B)
corrected.
Nozawa et al. [19771, p. 22.
Species: ARC, CYC, FUS(2), NEM. Total samples, 5
(see Comment 1).
Loci: All except AK, CA-IC, CA-11, Es-D, Gc, and HbB.
Total loci, 24 (see Comments 2 and 3).
Comments: 1)FAS excluded, superseded by Kawamoto et al.
[1982, p. 2751; FUS:troop-known excluded, superseded
by Nozawa et al. 11982, p. 2561; MUL and RAD excluded,
superseded by Shotake [1979, p. 4481.
2) ADA and Alb data (except for FUS:troop-unknown
sample) excluded, superseded by Shotake [1979, p. 4441;
CYC/Acp and CYC/PHI excluded, superseded by larger
sample in Ishimoto [1972b, pp. 339, 3431; FUS:
YakdTBPA excluded, superseded by Tanabe et al.
[1977, p. 3201.
3) FUS:Yaku/MDH data from Shotake and Nozawa
[1974, p. 2211; FUS/LDHA and FUS/LDHB data from
Shotake [1974, p. 2991.
4) For Hb[Al concordance, cf. Darga et al.
[1975, p. 8041 and Kawamoto et al. [1985, p. 491.
Nozawa et al. [1982], p. 256.
238 I Fooden and Lanyon
Species: FUS(33). Total samples, 33.
Loci: All except CA-IC, CA-11, and Gc. Total loci, 27.
Omoto et al. [19701, p. 221.
Species: FUS(2). Total samples, 2 (see Comment).
Loci: PI. Total loci, 1.
Comment: ARC, CYC, FAS, MUL, and NEM excluded, superseded by
Weiss et al. [1973, p. 2191.
Shotake [19791, pp. 444, 448.
Species: ARC(3), ASS, CYC, FAS(3), FUS, MUL(3), NEM(2), RAD.
Total samples, 15 (see Comments 1 and 2).
Loci: All except AK, CA-IC, CA-11, Es-D, Gc, and HbB.
Total loci, 24 (see Comments 3 and 4).
Comments: 1)FUS:M. f. fuscuta excluded, superseded by
Nozawa et al. [1982, p. 2551; FASPhilippines,
MUL:Pakistan, and MUL:Thailand excluded, superseded by
Kawamoto et al. [1982, p. 2751.
2) FAS:Indonesia and FASMalaysia samples also
reported by Kawamoto et al. [1982, p. 2751, cited here
for revised Alb data only; ARC:Thailand, CYC, FUS:Yaku
and NEM:Thailand samples also reported in part by
Nozawa et al. [1977, p. 221, cited here for revised Alb
and ADA data only.
3) For supplementary information on seven loci (Alp,
CellEs, GGPD, Hp, LAP, PI, TO) th at are monomorphic in
ASS, MUL:China, MUL:India, and RAD samples, cf. Shotake
[1979, p. 4471 and Kawamoto et al. [1982, p. 2751.
4)One undetermined monomorphic locus (possibly HbB) excluded [cf. Shotake,
1979, p. 447).
Shotake [19811, p. 290.
Species: Papio anubis (31, P. hamadryus (5).
Total samples, 8 (see Comment 1).
Loci: All except CA-IC, CA-11, Es-D, and Gc. Total loci,
26 (see Comments 2 and 3).
Comments: 1)Hybrid population samples excluded.
2) Two monomorphic loci (CA-11, Es-D) excluded, alleles undetermined; three
other monomorphic loci
(PA-1, PA-2, PlasmaEs) also excluded, not matched with
loci in other references.
3) For TBPA allele frequency, cf. Shotake et al.
[1977, p. 2281, Tanabe et al. [1977, p. 3201,
and Shotake [1981, p. 2901.
4)For supplementary information on alleles at
monomorphic loci, see Kawamoto et al. [1982, p. 2751.
Shotake & Santiapillai t19821, p. 83
Species: SIN(13). Total samples, 13 (see Comment 1).
Loci: All except CA-IC, CA-11, and Gc. Total loci, 27
(see Comment 2).
Comments: 1)Global data presented for one sample include
separately tabulated data and untabulated data.
2) Gc monomorphic in samples studied, allele
unspecified.
3) For ADA allele designations, cf. pp. 83, 89,
Blood Proteins in Macaca / 239
and 91; for TBPA:S allele frequency in Dambula I
sample, cf. pp. 83 and 86; for Tf allele concordance,
see p. 82.
Shotake et al. [1986], p. 231.
Species: SIL(3). Total samples, 3 (see Comments 1 and 2).
Loci: Acp, ADA, Alp, CA-IC, GGPD, Gc, HbA, Hp, LAP, PGM-I,
PHI, Tf, and TO. Total loci, 13 (see Comment 3).
Comments: 1)Supplementary details provided in letter,
August 1987.
2) Includes one global sample based on 19 localized specimens and one
unlocalized specimen.
3) Twenty unspecified monomorphic loci excluded.
Tanabe et al. [19771, p. 320.
Species: FAS(4), FUS, MAU, MUL(3), NGA. Total samples,
10 (see Comments 1 and 2).
Loci: TBPA. Total loci, 1.
Comments: 1)ARC and NEM (localities unspecified) excluded
[cf. Shotake, 1979, p. 4441; ASS, MUL:China, M U L h d i a ,
and RAD excluded, superseded by Shotake [1979, p. 4481;
CYC excluded, partly overlaps data in Nozawa e t al.
11977, p. 221; FUS:M. f . fuscata excluded, superseded
by Nozawa et al. C1982, p. 2541.
2) FUS:M. fuscata yakui sample also reported in part
by Nozawa et al. [1977, p. 221, cited here for larger
sample size.
3) Typographical error, MUL:Pakistan/TBPA:S, allele
frequency corrected.
Institute of Experimental Pathology and Therapy, Sukhumi
Annenkov et al. 119721, p. 237
Species: MUL(4). Total samples, 4.
Loci: Tf. Total loci, 1.
Comment: Designations of alleles TEF and TEF’ in this
reference apparently are the reverse of those of other
authors [cf. Annenkov, 1974, p. 60; Darga et al., 1975,
p. 801; Nozawa et al., 1977, p. 22: ARC, NEMI; in the
present analysis, these designations have been
transposed to bring them into accord with general
usage.
Annenkov [19741, p. 60.
Species: ARC, ASS, FAS, MUL, NEM. Total samples, 5 .
Loci: Tf. Total loci, 1.
Comments: 1)MUL data given here apparently include data
tabulated in Annenkov et al. [1972, p. 2371 plus
additional data.
2) See comment under Annenkov et al. 119721.
Laboratoire de Gknktique Moldculaire du CNTS, Paris; Universitk Paris
Hazout et al. [1984], p. 344.
Species: FAS(4). Total samples, 4 (see Comment 1).
Loci: PI, TBPA, Tf. Total loci, 3.
Comments: 1)W Malaysia sample excluded, previously
reported by Lucotte et al. [1984b, p. 3401.
2) In Java sample, T f C and TED allele frequencies
240 I Fooden and Lanyon
may include small components of alleles TEC’ and
TED‘, respectively [cf. Darga et al., 1975, p. 801;
Kawamoto and Ischak, 1981, p. 240; Kawamoto et al.,
1981, p. 201.
3) FAS:Thailand/Tf allele frequencies excluded, not
concordant with corresponding data published by Darga
et al. [1975, p. 8011.
Hazout et al. [19861, p. 244.
Species: ARC, MUL, NEM, MAU, NGA, SIN.
Total samples, 6 (see Comments 1 and 2).
Loci: Tf. Total loci, 1.
Comments: 1)Seven samples excluded, previously reported by
Lucotte et al. [1984a, p. 350, captive colony; 1984b,
p. 3401 and Hazout et al. [1984, p. 3441.
2) CYC, FAS:Malaysia, and MUL:India excluded, not
concordant with corresponding data published by Darga
et al. [1975, p. 8011, Nozawa et al. [1977, p. 221,
Shotake [1979, p. 4481, and Kawamoto et al.
[1982, p. 2751.
3) For ARCITEF’ and ARCITEH’ concordance, see Darga
et al. [1975, p. 8011 and Nozawa et al. [1977, p. 221.
4) NEM:MalaysialTEF allele frequency may include a
small component of allele TEF’ [cf. Darga et al.,
1975, p. 8011.
Lucotte et al. [1984bl, p. 340.
Species: ARC, FAS, MUL, NEM, RAD. Total samples, 5.
Loci: PI, TBPA. Total loci, 2 (see Comment 1).
Comments: 1)Tf excluded, superseded by Hazout et al.
[1986, p. 2441.
2) For country of origin of ARC sample, see Hazout
e t al. [1986, p. 2441.
3) RAD/PI data excluded, not concordant with
corresponding data published by Nozawa et al. [1977,
p. 221 and Shotake [1979, pp. 444, 4471.
University of Michigan; Wayne State University
Darga et al. [19751, p. 800.
Species: ARC, CYC, FAS(41, FUS, MAU, MUL(31, NEM(31, NGA,
RAD, SIN. Total samples, 17.
Loci: CA-I, CA-IC, HbA, HbB, PGD, TBPA, Tf. Total loci, 7.
Comments: 1) CA-I data for FAS:W Malaysia and FUS excluded,
presented in greater detail by Tashian e t al.
[1971, p. 1911; TBPA data for FAS:W Malaysia and NEM:W
Malaysia excluded, presented in greater detail by
Weiss et al. [1971, p. 761.
2) For locality restrictions of ARC, FAS:Philippines,
FAS:Thailand, MUL:India, MUL:Thailand, NEM:W Malaysia,
and NEM:Thailand, see Darga [1975, p. 191.
3) For ARC/TBPA sample size, see Weiss e t al. [1973,
p. 2181; for FAS:Thailand/TEC’ frequency, see
Prychodko et al. [1971, p. 1801; for MAUIHbA and HbB
allele concordances, cf. Kawamoto et al.
[1985, p. 491.
Blood Proteins in Macaca I 241
Goodman et al. [1965], p. 885.
Species: ARC(2), FAS(2). Total samples, 4 (see Comment).
Loci: Tf. Total loci, 1.
Comment: ARC:India, ARC:misc., FAS:Vietnam, and FAS:misc.
samples only; other data superseded by Darga et al.
[1975, p. 801; reduced MUL sample size assumed to be
more accurate].
Tashian et al. 119711, p. 190.
Species: ARC(2), FAS(7), FUS(21, MAU, MUL(2), NEM(3), NGA
RAD. Total samples, 19 (see Comment 1).
Loci: CA-I, CA-11, Total loci, 2 (see Comment 2).
Comments: 1)MUL:Bangladesh and CYC excluded, superseded by
Darga et al. [1975, p. 8001.
2) CA-I data cited here for ARC:misc., FAS:misc.,
F A S W Malaysia (4 samples), FUS, and MUL:misc.; CA-I
data for other samples superseded by Darga e t al. [1975,
p. 8001.
3) For locality restriction of ARC:Thailand,
FASPhilippines, FASThailand, MUL:Thailand, and
NEM:Thailand, see Darga. [1975, p. 191.
4) NEM:Thailand/CA-11 allele frequencies recalculated
from phenotype frequencies.
Weiss & Goodman [19721, p. 42.
Species: FAS(3). Total samples, 3.
Loci: Alb, MDH. Total loci, 2 (see Comments 1 and 2).
Comments: 1) CA-I, TBPA, and PGD data excluded; these data
are superseded or presented in greater detail by Weiss
et al. [1971, p. 761, Tashian et al. [1971, p. 1901, and
Darga et al. [1975, p. 8001.
2) Es-A1 excluded, data unreliable [Weiss et al.,
1973, p. 214, footnote]; LDH-M excluded, not
matched with loci in other references.
3) For locality restrictions of these samples, see Comment 3 under Weiss et a1
[1973].
Weiss e t al. 119711, p. 76.
Species: FAS(31, NEM(2). Total samples, 5 (see Comment).
Locus: TBPA. Total loci, 1.
Comment: W Malaysia samples only; other samples superseded
by Darga et al. [1975, p. 8021.
Weiss e t al. [19731, p. 219.
Species: ARC, CYC, FAS(3), MUL(2), NEM(2).
Total samples, 9 (see Comment 1).
Loci: PI. Total loci, 1 (see Comment 2).
Comments: 1)FUS excluded, presented in greater detail by
Omoto et al. [1970, p. 2211.
2) CA-I, CA-11, Hb, PGD, TBPA, and Tf excluded,
superseded by Darga et al. [1975, p. 8001.
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