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Şempanzelerin Evrimi Ve Dahası
Şempanzelerin Evrimi Ve Dahası
Phillip A. Morin; James J. Moore; Ranajit Chakraborty; Li Jin; Jane Goodall; David S. Woodruff
Science, New Series, Vol. 265, No. 5176. (Aug. 26, 1994), pp. 1193-1201.
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individuals in the Kasakela social community
Kin Selection, Social Structure, (1, 4). Adult chimpanzees make nests (in
trees) of leaves and branches, and, with the
Gene Flow, and the Evolution of exception of mother-infant pairs, typically
sleep individually in a fresh nest each night.
Chimpanzees Hairs from Gombe were collected by follow-
ing known individuals, watching them build
nests, and then returning at dawn to search
Phillip A. Morin,* James J. Moore, Ranajit Chakraborty, Li Jin, the abandoned nest. Genetic characterization
Jane Goodall, David S. Woodruff of this community is the first step in under-
standing the diversity and similarities among
Hypotheses about chimpanzee social behavior, phylogeography, and evolution were chimpanzee communities, populations, and
evaluated by noninvasive genotyping of free-ranging individuals from 20 African sites. subspecies. Our study is necessarily limited by
Degrees of relatedness among individuals in one community were inferred from allele- the logistical difficulties of intensive sample
sharing at eight nuclear simple sequence repeat (SSR) loci. Mates are related on the order collection across Africa, but ongoing and
of half-siblings, and homozygosity is significantly increased at several SSR loci compared planned studies at other sites will elucidate
to Hardy-Weinberg expectations. These data support the kin-selection hypothesis for the the constants and variables in chimpanzee
evolution of cooperation among males. sequence variation patterns at two mitochondrial population genetic structure.
loci indicate historically high long-distance gene flow and clarify the relationships among D N A was amplifiied by the polymerase
three allopatric subspecies. The unexpectedly largegenetic distance between the western chain reaction (PCR) from hair samples
subspecies, Pan troglodytes verus, and the other two subspecies suggests a divergence collected from animals at 20 sites across
time of about 1.58 million years. This result, if confirmed at nuclear loci and supported by Africa (Fig. 1). I n all, we genotyped 67
eco-behavioral data, implies that P. t. verus should be elevated to full species rank. individuals at eight variable nuclear SSR
loci ( 8 ) and determined D N A sequence
variation for many individuals at two in-
formative mtDNA loci (5). T h e highly
A l m o s t nothing is known about genetic ers of concern to ecologists- and evolu- polymorphic di- and tri- and tetra-nucle-
variation of the chimpanzee, Pan trog- tionary and conservation biologists. otide SSR loci differ in the number of
lodytes, in nature. Hypotheses concerning Chimpanzees are geographically wide- times the core sequence is repeated (typ-
chimpanzee sociobiology and evolution s ~ r e a dand eco-behaviorallv diverse. De-
L
icallv 10 t o 30 times). (5-7) . and such
have gone untested for many years be- spite up to 34 years of field study at a few s i m d e sequence length polymorphism
cause of difficulties surrounding tissue ac- sites, little is known about the phylogeny of (SSLP) was scored o n autoradiographs of
quisition for genetic analysis. W e here the chimpanzee subspecies, their times of polyacrylamide gels ( 8 ) . Individual mul-
demonstrate a method of noninvasive divergence, historical population sizes, or tilocus genotypes were used to establish
genotyping based o n D N A amplified from patterns of gene flow. Phylogenetic recon- pedigree relationships and characterize a
hair shed in night nests or plucked from structions are hampered by a complete lack population's relative genetic variability
captive apes ( 1 ) . Using eight hypervari- of a fossil record, and data o n long-distance and behaviorally important substructur-
able simple sequence repeat (SSR) nucle- dispejsal and genetic variation. This study ing. T h e mtDNA sequences were ampli-
ar loci and two mitochondrial ( m t D N A ) of genetic variation of chimpanzee popula- fied and double-stranded products were
sequences, we demonstrate how multilo- tions across Africa describes phvlogeo- directly sequenced to detect phylogeneti-
cus data can be used to provide critical graphic patterns, begins to test hypotheses cally informative genetic variation. A
information concerning kin selection, for the evolution of chimpanzees' social 178-bp (base pair) segment of the cyto-
mating structure, individual reproductive structure. and sets the foundation for com- chrome b (cyt b) region of 3 4 chimpan-
success, inclusive fitness, population parative studies among communities within zees and one human was used to examine
structure, gene flow, phylogeography, and and between subspecies. the deeper branches of chimpanzee phy-
phylogenetic relationships. This techni- The Kasakela community in the Gombe logeny, and a 345-bp segment of the more
cal advance also permits a reexamination National Park. Tanzania (Fie.
. - 1,. site L),
. . is the variable control region of 66 chimpan-
of the relevance of chimpanzee behavior- longest studied wild chimpanzee population zees, two bonobos (Pan paniscus), and one
al ecology ( 2 , 3) to the elucidation of the (2). A t Gombe, we sampled all (N = 43) human was used to characterize phylogeo-
evolution of human behavioral and genet-
ic patterns. Although this report focuses
Fig. 1. Map of equatorial Afri-
o n one species of primate, these methods
ca, with sample collection
are immediately applicable to many oth- sites or countries indicated by
letters A to N , and approxi-
P. A. Morin and D. S. Woodruff are with the Department mate modern distributions of
of Biology and Center for Molecular Genetics, University
of Ca~forn~a, San Diego, La Jola, CA 92093-01 16, USA.
chimpanzees indicated by
J. J. Moore is with the Department of Anthropology, Uni- shading (2, 1 2 ) . The approxi-
versity of California, San Diego, La Jolla, CA 92093, USA. mate position of the poorly de-
R. Chakraborty and L. Jin are at the Center for Demo- fined subspecies boundaries
graphic and Population Genetics, Universrty of Texas in central Africa is indicated by
Graduate School of Biomedical Sciences, P.O. Box
20334, Houston, TX 77225, USA. J. Goodall can be
the dashed line.
reached at Jane Goodall Institute-USA, P.O. Box 599,
Rid~efield,CT 06877, USA.
*To whom correspondence should be addressed. The
present address of P. A. Morin is Department of Anthro-
pology, University of California, Davis, CA 95616-8522,
USA.
icant (P 5 0.05). cation of kin selection theory to evolu- 0.05) were detected at two loci, Mfd-23 and
Pla2a. This indicates that the wan-African
sample, at least at two loci, does not ade-
Fig. 3. Phylogenetic trees for A quately represent the population of which
chimpanzees and bonobos. P.t schweinfurthii P.t. schweinfurthii
P.t. troglodytes the Gombe community is part. Subdivision
(A) Basedon weighted genet- P.t. troalodvtes
- . of the species into three genetically distinct
ic distances corrected for in- X groups (subspecies) and population sub-
traspecific polymorphism for
the cytochrome b locus (23).
There were four synapomor-
\ P't. verus P.t. verus structuring into social communities (see be-
low) are most likely the reasons for the
phic transitions between P.t. observed allele distribution differences.
verus and the other two sub- P. paniscus Comparisons between the data sets, howev-
species at sites correspond- er, reveal relative patterns that indicate the
ing to 14995, 15004, 15052, probable causes of substructuring.
and 15100 in the human ref- If female dispersal was high enough to
erence seauence 144), and
three polyhorph~c'sites in
each subspecies (one site
, ,
\ H. sapiens , ,, \ H, sapiens maintain a large and effectively panmictic
population, we would expect pooled sam-
polymorph~c ~n both P. t. 2.8 0 91.2 51.1 32.48.90 ples from across the species range and from
schweinfurthiiand P. t. troglo- individuals within a single social communi-
Genetic distance (% change per site)
dytes). (B) Based on weight-
ty to be in ~ a r d ~ - ~ e i n equilibrium
ber~
ed genetic distances corrected for intraspecific polymorphism for the control region locus (23)(Table4).
(HWE). Deviations from the predictions of
panmixia can be caused by several factors
including nonrandom mating, distortions in
Table 2. Comparison of observed heterozygote frequencies (Obs.)_withHWE expectations (Exp.) based
the contributions of gametes to offspring,
on (i) total frequency of heterozygotes, in which all heterozygotes were used to calculate the expected
allele frequencies for each locus, which were compared to the observed allele frequencies by chi-square
Table 3. Test of association of alleles among loci from the distribution of each locus (Table 2)were used for computations; in method (2)the unbiased
heterozygous loci. Only 57 individuals tested for all eight Loci are included in estimates of heterozygosities (50)were used. Tests for nonrandom associa-
this test. The expected distributions of the number ofheterozygous loci and tion of alleles among loci from the distribution of heterozygous loci were
the theoretical mean, variance, and 95% confidence interval (CI)of variance performed using the method described (57), following the theory of Brown et
are reported. In method (1)the observed proportions of heterozygotes for An alternative method (53)provides equivalent results.
a/. (52).
Population
Gombe
Number of Non-Gombe
heterozygous Unrelated Total
loci
Exp. Exp. Exp.
Obs. Obs. Obs
I 2 1 2 1 2
Within P. t. troglodytes, there were 17 others (Fig. 4). Using the neighbor join- ior in this species (18). The sequence sim-
haplotypes among 18 individuals, and ing method, a phylogenetic tree was con- ilarities of some individuals from Gombe to
within P . t. werus, all 11 sequences were structed from the pairwise distances (Fig. individuals from a geographic range cover-
different from each other; n o haplotypes 5; summarized in Fig. 3B). Alternative ing over 600 km suggests that historical
were shared between subspecies. Several parsimony and distance cluster analyses gene flow has been significant. In the last
synapomorphies (shared derived charac- also vielded trees with the same subspe- 50 years, however, the 32-km2 Gombe Na-
ters) were fixed or nearly fixed in each cies ;lades and very similar subc1us;ers tional Park, now occupied by 150 to 160
subspecies (Fig. 4). Despite the large vari- within subspecies (1 6, 17). chimpanzees, has become completely isolat-
ation within subspecies, cladistic analysis Of 24 adults in the Kasakela social com- ed from other habitats by deforestation
shows that 10 fixed (and 2 slightly poly- munitv at Gombe in Tulv 1991, 19 individ- (1 9). In the absence of gene flow with other
morphic) synapomorphies link the east- uals kAown or susperted to be maternally populations, genetic erosion due to genetic
ern and central subspecies to the exclu- unrelated were sampled for sequencing; we drift and inbreeding may begin to signifi-
sion of t h e western subspecies, which in found 15 different haplotypes in the control cantly increase the probability of extirpa-
turn exhibits 11 fixed and 1 polymorphic .region. This surprisingly high within-com- tion of this and other populations experi-
(in one individual) synapomorphies that munity genetic variation is attributable to encing genetic isolation and habitat frag-
...........
31001825228887480577541220274809194141236712821941441980696373223496224224424433381594
24799777892378188346856289591463584031493700114775496841164877743755788505593225893058
TTCACA-GCCAATTCCAACGTGTT-ACCAGTCCCTTACCCCTACCTCCCCGTCATTCTCCCACTTTCTAGCCCTAAACCCAACCACCWDE
Evered GOMBE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .C.T.C . . . . . . . . . . . . . . . . . .
California GOMBE . . . . . . . . . . . . . . . . . . . . .? ? ? . . . . . . . . . . . . . . . . . . . . ?. . . . . . . . . . . . . . . . . .? . C T C . . . . . . . . . . . . . . . . . .
l 73 GOMBE . . . . . . . . . . . . . . . . . . . . . .? ? . . . . . . . . . . . . . . . . . . . . .? . . . . . . . . . . . . . . . . .? . C T C . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T. . . . . . . T . . . . . . . . . . . . . . . . . . . C T C . . . . . . . . . . . . . . . . . .
Spindle
Gigi
GOMBE
GOMBE
.
. . . . . . . . . ? . . . . . . . . . . . .? . . . . . . . . . . . . . .T . . . . . . T . . . . . . . . . . . . . . . . . . .C . TC . . . . . . . . . . . . . . . . . .
I
Tubi GOMBE . . . . . . . . . . . .? . . . . . . . . . .? . . . . . . . . . . . . . T . . . . . . T ? . . . . . . . . . . . . . . . . .? C . T C . . . . . . . . . . . . . . . . . .
Skosha GOMBE . . . . . . . . . . . . . . . . . . . . . . ? . . . . . . . . . . . . . . T . . . . . . T . . . . . . . . . . . . . . . . . . .C . T C . . . . T . . . . . . . . . . . . .
Prof GOMBE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . G. T. C . . . C . . . . . . . . . . . . . . . . . .
JF 1b GOMBE . . . . . . . . . . . . . . . . . . . . . ?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . G . T C . . .C . . . . . . . . . . . . . . . . . .
Pts 49 MAHALE . . . . . . . . . . . . . . . . . . . . . .? ? . . . . . . . . . . . . . . . . . . . . . ? . . . . . . . . . . . . . . . GT ? . . . C . . . . . . . . . . . . . . . . . .
Pts 2 MAHALE . . . . . . . . . . . . . . . . . . . . . ?. ? . . . . . . . . . . . . . . . . . . . . ?. . . . . . . . . . . . . . . .G T . . . . C . . . . . . . . . . . . . . . . . .
Pts21 TONGWE . . . . . . . . . ? . . . . . . . . . . . ? ? ? . . . . ? . . . . . . . . . . . . . . . . ? , . . . ? . . . . . . . . .T G T ? . . . C . . . . . . . . . . . . . . I . . .
Pts20 TONGWE . . . . . . . . . . . . . . . . . . . . . ? ? ? . . . . ? . . . . . . . . . . . . . . .. ? . . . . ? . . . . . . . . . T G T ? . . . C ? . . . . . . . . . . . . . T , ..
Rs6 TONGWE . . . . . . .. ? ? . . . . . . . . . .. ? ? ? . . . . ? . . . . . . . . . . . . . . . . ? G . . .?.G. . . . . . .TGT?. . .C? , . . . . . . . . . . . .T. . .
Ptsl2 TONGWE . . . . . . . . . ? . . . . . . . . . . .7 ? ? . . . . ? . . . . . . . . . . . . . . . .? . . . . ? . . . . . . . . . T G T ? . . . C . . . . . . . . . . . . . . T . . .
George RWANDA . . . . . . . . . . . . . . . . . . . . . . ? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .u c. 7
4 . . .
Ruhara BURUNDI . . . . . . . . . . . . . . . . . . . . . ?. ? . . . . . . . . . . . . . . . . . . . . . .? . . T . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . G. .. T . . .
Rs35 UGANDA . . . . . . . . . . . . . . . . . . . . .? ? . . . . . . . . . . . . . . . . . . . . .? . . . . . . . . . . . . . . . . .? . . . . . . . . C . . . . . T G . T . . .
Gimble GOMBE . . . . . . . . . . . . . . . . . . . . . .? . . . . . . . . . . . C . . . . . . . . . . . . . T . . C . . . . . . . . . . . . . . . . . . . . . . . . . . .T G . T , . . 3
Pts43
DH 1
UGANDA
GOMBE
-- --
. . . . . . . . . . . . .. ? . . T ? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C G . . . T . . . . . . . . . . . . . . . . . . T G T . T , , . . . .-
. . . . . . . . . . . . . . . . . . . . . .? ? . . . . . . . . . . . . . . . . . . . . . ? . . . . . C . . . . . . . . . . .7 . . . . . . . . . , . .ti I . I t i . I . . .
Georgette RWANDA . . . . . . . . . . . . . . . . . . . . . . ? ? . . . . . . . . . . . . . . . . . . . . . ? . . . . . C . . . . . . . . . . . ? C . . . . . . . . . . .G T . T G . T , . .
Frodo GOMBE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .G A , T . . C . . . T T . . T . . .
Kidevu GOMBE . . . . . . . . . ? . . . . . . . . . . .? ? . . . . . ? . . . . T . . . . . . . . . . . . . . . ?. . . . . . . . . . . . . . . . . .G A , T . . C . . . T T . . T . . .
Noel ZAIRE . . . . . . . . . . . . . . . . . . . . . .? ? .,. . . . . . . .T . . . . . . . . . . . ? . . . . . . . . . . .C . . . . . ? . . . . G A . . . . C . . . T T . . T . . .
WL3 GOMBE . . . . . . . . . . . . . . . . . . . . . ? . . . . . . . . . . .T , . . ~. . . . . . . . . . . . . .C . . . . . . . . . . . . . . . .GA . . . . C- G , . -- T T , . -T , , .
Pal ZAIRE . . . . . . . . . . . . . . . . . . . . . ?. . . . . . . . . . . . . . . . . . . . . . . . . . . . .C . . . . . . . . . . . . . . . . . . . . . C. . . . T I . . I , . .
SY2 GOMBE . . . . . . . . . . . . . . . . . . . . . . ? ? . . . . . . . . . . . . . . . . . . . . . ? , . . . . . . . . . . . . . . . . . . . . . . . . T. C C . . . T . . , T . . . 4
BE1 GOMBE . . . . . . . . . . . . . . . . . . . . .. ? ? . . . . . . . . . . . . . . . . . . . . . ? , . . . . . . . . . . . . . . .. ? . . . . . . T , T C C . . T . . . T . . .
AL2 GOMBE . . . . . . . . . . . . . . . . . . . . . .? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
T.TCC, . , T . , . T . . .
ME1 GOMBE . . . . . . . . . . . . . . . . . . . . . ?. ? . . . . . . . . . . . . . . . . . . . . . ? . . . . . . . . . . . . . . . . . ? . . . . . . . . T C C . . . T , . , T . . .
Sandi
-.. ~ . GOMBE . . . . . . . . . . . . . . . . . . . . . .? . . . . . . . . . . . . . . . . . . . . .? . . . . . . . . . . . . . . . . . ? . . . . ? . . . T C C . . . T . . . T , . . --
Maggie RWANDA . . . . T . . . . . . . . . . . . . . . . . ? . . . . . . . . . . . . . . T . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .I I . .
Milla CAMEROON . . . . . . T . . . . G C . . . . . . C . ? . T . . . . . . . . . . . . . . . . . . .T C T T T T C T G . . . C . . . . . . . C . . . . . . . . . . . . . . . . . . . .
Berlhe
. .
CAMEROON. C . . . G C . . . . G . . . . . . . . . . . . . . . . . . . .T . . . . . . . . . . . T C T T T T A . T G C . . . . . . . . . AC . , . . . . . . , . . . . . . . .T . T 5
Rt36 CONGO . C . . . . C . . . . G . C . . . . . . . . . . C . . . . . . . . . . . . . . . . . . .T C T T T T A C T G C . . . . . . . . . . C . . . . . . . . . . . . . . . . . . . .
Rt43 GABON ... . G . . . . . . . . . . . . . . . . .? ? . . . . . ? . . . . . . . . . . G T C T T T . . . . T ? C . G C C T C . . . . T . . . . . . . . . . . . . . . . . . .
T. . . 6
Ntebe GABON . . . G . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . G T C T T T . . . . T . C . G C C T C . . . . T . . . . . . . . . . . . . . . . . . .T . . .
Ponia GABON . . . . . . . . . . . . . . . . . . C. . . . . . . . . . . . . C . C TGTCG. ..T . . T A C GG. T . . . . . . . . . .C . . . . . . . . . . . .G T . . .
Mopia GABON . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. C. C T. . G T C . . . . . . . T A C .. GG. . . . . . . . . . . .C . . . . . . . . . . . .G . . . .
Ptt37 CONGO . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. C . . . C C C T . G . C . . . . . T . T A C T G G . . C . . . . . . . C . C . . . . . . . . G . . . G G , . . .
C1 UNKNOWN . . . . - . C . . . . . . . . . . . . . . . . .C . T . . . . . . . C C C T A G T C . . . . . . . . A C T G G . . . . . . . . . . .C . . . . . . . . . . . . . . . . . .
Makokou GABON . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .C . C C T G T C . . . . . . . T A C T G G . . . . . . . . . . . .C . . . . . . . . . . . . . . . . G .
Ptt62 E.Guinea . . . . . . . . . . . . . . . . . . . . .? ? : . . . . . . . . . C C C T . G T C . ? . . . T A C T G G . . . . . . . . ? . . . C . . . . . . . . . . . . . . .G T
Rt35 CONGO . . . . . . . . . . . . . . . . . . . . . ?. ? . . . . G . . . . . C C C T T. G T C . .. .. ? . . . . A C T G G . T . ? T . . T ? . . .? C. ?. .. . . . . . . . . . . . . 7
Mouilla
Pt159
GABON
GABON
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T.C C C T T G T C . . . . . . . T A C T G G . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . ?. ? . . . . . ? . . . . T C C C T T G T C . . . . . . .T ? C T G G . . . . . . . . . . . . C . . . . . . . . . . . . . . . .G , .
-
lvindo GABON . . . .T . . . . . . . . . . . . . . . . . . . . . . . . . . . . C . C C T T G T C . . . . . . . T A C T G G . . . . T . . . . . . .C . . . . . . . . . . . . . . . . G .
Gemini GABON . . . . . . . . . . . . . . . . . . . . . . . . G . . . . .'. . . T C C C T T G T C . . . . . . . T A C T G G . . . . . . . . . . . .C . . . . . . . . . . . . . . . . . .
Rt33 CONGO . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .T.C C C T T G T C . . . . . . . T A C T G G . . . T . . . . . . . . C . . . . . . . . . . . . . . . . . .
Rt34 CONGO . . . . . . . . . . . . . . . . . . . . . ?. . . .':
. . . . . . T C C C T T G T C . . . . . . . T A C T G G . . . T . . . . . . . .C . . . . . . . . . . . . . . . . . .
PN5 IVORYC. C C T T T G C . . . . G C C T A C G T A A A C C . . . . . . . . . . CC . . T . . . . . . . . . . A . C T . . . . C . . T . . . CC . . . . . . . . C . . . T A G . . - . .
Edgar
.
.
UNKNOWN C C T T T G C ? ? ? G . C T A C G T A A ? ? ? . . . . ? . . . . . C C . T . . . . . . ? . . . A ? C T . . . C . . T . . ? C C : . . . . . . . C . . . T A G . . . . .
Ptvl5 IVORYC. C C T T T G C . . . . G C C T A C G T A A A C C . . . . . . C . . . C . . . T . . . . . . . . .A A C T . . . . C . . T . . . C C . . . . . . . . C . . . T A G . . . G T 8
P1 MALI C ? T T T G C . . . . G C C T A C G T A A A ? C . . . . . . . . ? CC . . T . . . . ? . . . . . A A C T . . . . C . . T . . . C C . . . . . . . . C . . . T A G . ? .
.
..
C3 UNKNOWN . C . C T G C . . T . G C C T A C G . A A A C C . . . . . C . T . T C . . T . . . . . . . . . . A A C . . . . . C . . . . . . .C . . . . . . . . C . . . . A G . . . . .
NC.588 UNKNOWN . . . . T G . A A T . G C C T A C G T A A A ? ? G T . G A . . T . C C . . . . C . . . . T . . A A C . . . C . C . . . . T . . . . . . A . . . . C . . . . A . . . . . .
W 4 IVORYC . . . . . . . A A T G G C C T A C G T A A ? C C .. . . T ? ? . T T . C C . . . . . C . . . . . . . A ? C . . . . . C . T G . . . C . . . . . . . . C . . . . A . . . . . .
P 2a MALI . C . . . . . A A T G G C C T A C G T A A ? ? C . G . T ? A . . T . C C . . . . .C . . . . T . . A ? C . . . . . C . . T . . . . C . . . . . . . . C . . . . 9
C2 UNKNOWN . . . . . . C A A T G G C C T A C G T A A A C C . . . T . A . T . . C C . . . . . C . . . . . . . A A C . . . . . C . . T . . . . C . . . . . . . . C . . . . A . . . . . .
Tobar LIBERIA . . . . . . .A A T G G C C T A C G T A A A C C . . . T . A . ? T . C ? . . . . . C . ? . . . . . ? A C .. . ? . ? . . T . . . . C ? . . . . . . . C. . . . A . . . . . .
P3 MALI . . . . . . .A A T G G C C T A C G T A A ? ? C ...T ? A . T T . C C . . . . . C . . . . . . .A ? C . . . . . C . . T . . . . C . . . . . . . . C . . . . A . . . . . .
Bosandjo P.paniscus . . . . A . C . . . . G . C T A . G T A . . ? ? C . A . . . . . . . A C . T . - A , . . . ? . . . A . C . . . C . . . . T . . ? . A . . ? . . . . . C . G T T A . . . . C T
P. paniscus . . . . A G C . . . . G . C . A . . T A . . . CC . A . . . . . . . A C C . . - A , . . . . . . . A . C . . . C . . . . T . . . . G T C . . . . . . C . G . . A . . . . . T
-
H.sapiens . C . C A . C . A . G G C . . . . . . A . . . C . G T . . A . T . . C . C T A . T . C . . . . T . A . C T G . C A . . . . . G C C G . C T . . T . . C . . . T A . . . . . .
Fig. 4. Individual chimpanzee by control region nucleotide site matrix for subspecies separationsmatch those in Fig. 5, described in text);sites 1 to 345
nucleotide positions variable in two or more P. troglodytes individuals.Nucle- refer to the human reference sequence (44),with 1 correspondingto position
otide sites have been rearranged to cluster markers for each clade (cladesand 16047; ? = missing data; reference = chimpanzee consensus sequence.
-
furthii, the samples include 32 individuals of
(26) (41) precisely known geographic origin and 7 of
Ptt37 G
C1 t
known country of origin. Both parsimony
and neighbor joining (Fig. 5) methods cre-
ated trees with four primary clades (clades 1
to 4) within this subspecies, each with iden-
Mouilla F tical individual composition. There is some
Ptt59 F geographic differentiation; clade 3 contains
lvindo F primarily samples from the northernmost
Gemini F sites (Uganda, Rwanda, and Burundi) and
clade 2 includes all nine apes from the two
- - - - - - - - - - -
Ptt34G - - southernmost sites (Mahale and Tongwe).
Widespread historical gene flow is evi-
I R 99/98 Edgar t denced, however, by inclusion of the geo-
graphically intermediate Gombe genotypes
in all four clades. The absence of any of the
southernmost samples in "northern" clade
3, and of northernmost samples in "south-
ern" clade 2, indicates possible isolation by
distance beyond about 600 km.
Control region variation provides evi-
- - - - - - - - -p 3 n - dence for similar high historical gene flow
P. paniscus ( ~ o s a n d j o r patterns in the other two subspecies. With-
I in the central subspecies, P. t. troglodytes,
I P. paniscus
H. sapiens we can show three clades (clades 5 to 7)
1198 SCIENCE VOL. 265 26 AUGUST 1994
one another in such forest fragments (39). 3. T. Nishida, The Chimpanzees of the Mahale Moun- Morin, Yearb. Phys. Anthropol. 36, 179 (1993).
tains: Sexuai and Life History Strategies (Univ. of 11. E. B. Spiess, Genes in Populations (Wiley, New
Reconstructing the history of the genus Pan Tokyo Press, Tokyo, 1990); T. Kano, The Last Ape: York, 1989); K. C. Staub, D. S. Woodruff, E. S.
and of our common ancestor will have to Pygmy ChimpanzeeBehavior and Ecology (Stanford Upatham, V. Viyanant, Am. Malacol. Bull. 7, 93
allow for the previously underappreciated Univ. Press, Stanford, CA, 1991). (1990).
variation within chimpanzees. This may 4. Localitydata from P.A. Morin [thesis,Universityof Cal- 12. W. C. 0 . Hill, in The Chimpanzee,G. H. Bourne, Ed.
ifornia, San Diego (1992)] are generalized in Figs. 4 and (Karger, Basel, Switzerland, 1969),pp. 22-49; C. P.
help to resolve the gorilla-chimpanzee-hu- 5. Samples from non-Gombe named individuals and Groves, A Theory of Human and Primate Evolution
man "trichotomy" question (40) by improv- F't-59, FT-62 are from captive animals with inferred (Clarendon, Oxford, 1989); R. M. Nowak, WalkePs
ing the resolution of synapomorphies over country of origin and were obtainedfrom the Chimfun- Mammals of the World (Johns Hopkins Univ. Press,
shi Wildlife Orphanage,Zambia; the Centre Internation- Baltimore, 1991), vol. 1; D. E. Wilson and D. M.
homoplasy (the phylogenetic "signal"). al de Recherches Medicales de Franceville (CIRMF), Reeder, Eds., Mammal Species of the World,
Fourth, our discovery of considerable genet- Gabon; and the Jane Goodall Institute, Burundi. It is (Smithsonian Institution, Washington, DC, ed. 2,
ic variation within chimpanzee populations possiblethat some of these captives have been misio- 1993)
cated within the subspecies' range. 13. C. P.' Groves, C. Westwood, 5. T. Shea, J. Hum.
across broad geographic ranges provides us 5. The hair sample coliection, DNA extraction and am- Evol. 22, 327 (1992); B. T. Shea, S. R. Leigh, C. P.
with a way of quantifying genetic diversity plification, electrophoresis, and autoradiography Groves, in Species, Species Concepts, andprimate
in these endangered species and monitoring procedures have been described: P. A. Morin and D. Evolution, W. H. Kimbel and L. B. Martin, Eds. (Ple-
S. Woodruff, in Paternity in Primates: Genetic Tests num, New York, 1993), pp. 265-296; U. S. Seal and
genetic erosion in both wild and captive and Theories, R. D. Maoin, A. F. Dixson, E. J. Wick- N. R. Flessness, in Primates, The Road to Self-Sus-
populations. ings, Eds. (Karger, Basel, Switzerland, 1992), pp. taining Populations, K. Benirschke, Ed. (Springer,
Conservation efforts in the wild and in 63-81. New York, 1986), pp. 47-55.
6. J. T. Epplen et al., in DNA Fingerprinting:Approach- 14. N. Saitou [Am. J. Phys. Anthropol. 84, 75 (1991)]
captivity need to account for the genetic reviewed published interspecific and intergeneric
es andAppiications, T. Burke, G. Dolf, A. J. Jeffreys,
diversity in the genus Pan and its partition- R. Wolff, Eds. (Birkhauser,Basel,Switzerland, 1991), comparisons involvirig DNA sequence data. Other
ing into several well-differentiated evolu- PP. 50-69. reports involving chimpanzees of unknown identity
tionarily significant units (41). Although 7. A. Edwards, A. Civitello, H. A. Hammond, C. T. Cas- include: B. B. Normark, A. R. McCune, R. G. Harri-
key, Am. J. Hum. Genet. 49, 746 (1991). son, Mol. Biol. Evol. 8, 819 (1991); M. Stoneking et
captive chimpanzees have traditionally 8. P. A. Morin, J. J. Moore, J. Wallis, D. S. Woodruff, a/., Am. J. Hum. Genet. 48,370 (1991); G. Ruano, J.
been sorted into and managed as two spe- Mol. Ecoi., in press. The eight loci studied were (lo- Rogers, A. C. Ferguson-Smith, K. K. Kidd, Mol. Biol.
cies, the three subspecies of P . troglodytes cus:human chromosome): (dinucleotide repeats): Evol. 9, 575 (1992); see also (75, 30).
Mfd3: 1, Mfd78:8, Mfd23: 16, Mfd32:18, LL:15 [J. L. 15. T. D. Kocher et a/., Proc. Nati. Acad. Sci. U.S.A. 86,
have, for example, been afforded no special 6196 (1989).
Weber and P. E. May, Am. J. Hum. Genet. 44, 388
significance under current NIH colony (1989); NucieiAcids Res. 18, 6465 (1990); J. L. We- 16. Paitwise distances for neighbor-joining analysis [N.
management policies. Our results suggest ber, A. E. Kwitek, P.E. May, ibid., p. 4034; J. L. Saitou and M. Nei, Mol. Biol. Evol. 4, 406 (1987)]
Weber, D. Patterson, H. Drabkin, ibid., p. 4038; M. were calculated by means of the Kimuratwo-param-
that treating the >2000 chimpanzees in eter model [M. Kimura, J. Mol. Evol. 16, 111 (1980)]
Litt and J. A. Luty, Am. J. Hum. Genet. 44, 397
biomedical facilities in the United States as (1989)]; (trinucleotide repeats): Pia2a:12, FABP:4, in MEGA [S. Kumar, K. Tamura, M. Nei, "MEGA:
genetically equivalent requires reassess- and (tetranucleotiderepeats):Rena4: I(7). Chromo- Molecular Evolutionary Genetics Analysis Software
somal locations of loci in chimpanzees are unknown. for Microcomputers," Comput. Appl. Biosci 10, 189
ment. Inappropriately matched individuals 11994)]
Genotypes for all 67 individuals and eight loci are
are undesirable in both experimental and available from P. A. Morin. 17. Cladistic analysis was performed with the PAUP par-
breeding situations, and some previous re- 9. The section of the cyt b gene amplified corresponds simony program [D. L. Swofford, PAUP: Phyloge-
sults based o n genetically dissimilar apes to bases 14816 through 15174 of the human mito- netic Inference Using Parsimony (version 3.1. I ) Illi-
chondrial sequence (44):the sequenced portion cor- nois Nat. Hist. Survey, Champaign (1991)] with a
may require reinterpretation (42). Howev- heuristic search method, 20 replications with ran-
responds to human positions 14964 to 15141. The
er, chimpanzee social, emotional, and intel- primers are identifled by a coded name, followed by dom addition of sequences, and 100 trees saved
lectual similarities to humans render man- the human nucleotide reference number of the 3' from each replicate (all other search variables were
end and L or H to indicate light or heavy strand: default settings; Consistency Index = 0.537,
agement from a purely genetic standpoint Rescaled Consistency lndex = 0.440, Retention In-
Cytb 1 (114841) 5'-CCATCCAACATCTCAGCAT-
unethical; the behavioral or social (or both) GATGAAA-3' and Cytb2 (HI5149) 5'-GCCCCTCA- dex = 0.819, Homoplasy lndex = 0.463, number of
needs of captive individuals must also be GAATGATATTTGTCCTCA-3' (15; without restric- steps = 337). The transition/transversion ratio (R) of
tion sites). The section of the control region amplified 15 (control region)was used.
considered. W e do not advocate breaking 18. T. Nishida, in The GreatApes, D. A. Hamburg and E.
corresponds to bases 16019 through 16428 of the
up mismatched but long-bonded pairs. human sequence (44), 0-88 (L16041) 5'-CTCTGT- R. McCown, Eds. (Benjamin-Cummings, Menlo
Finally, management of increasingly frag- TCTTTCATGGGGAAGC-3' and 0-44 1 (HI6407) Park, CA, 1979), pp. 73-121; A. E. Pusey, in (10);
5'-CGGGATATTGATTTCACGGAGG-3' (K. Garner, Anim. Behav. 28, 543 (1980); P. A. Morin etal., in ( I ).
mented populations in Africa may require
Zool. Soc. San Diego, personal communication). Se- 19. J. Goodall, in Understanding Chimpanzees, P. G.
occasional translocation. of individuals for quencing was done from both strands of the control Heitne and L. A. Marquardt, Eds. (Harvard Univ.
their own protection and to preserve naturally region PCR product as described [J. C. Garza and D. Press, Cambridge, MA, 1990), pp. 360-361.
occurring variability i n the wild. Such inter- S. Woodruff, Mol. Phyiogenet Evol. 1, 202 (1992)l. 20. M. Lynch and W. Gabriel,Evolution 44, 1725 (1990);
Sequencing of the cyt b region was only performed D. S. Woodruff, in Proceedings of the International
ventive management is fraught with hazards with the heavy strand (Cytb2) primer for most sam- Conference on Conservation Tropical Biodiversity,
including disease introduction and the behav- ples. Cyt b sequences: GenBank L35346-L35379; Y. S. Kheong and L. S. Win, Eds. (Malay NatureSoc.,
ioral problems of translocated wild individuals control region sequences; GenBank L35380- Kuala Lumpur, Malaysia, 1992), pp. 258-272; Pro-
L35442. Five additional published sequences were ceedings of the Second Princess Chulabhgrn Con-
and reintroduced captive-born or raised indi- gress (Bangkok, in press).
included in the analyses: three P. troglodytes (CI,
viduals (43). Our results suggest that the pos- C2, C3), one P. panlscus (plus another sequenced 21. Captive Breeding Specialist Group, IUCN, SSC,
sibility of outbreeding depression must also be by us, GenBank L35443), and one human [D. R. Giobai CaptiveAction Plan for Primates with Supple-
considered. Our appreciation of the natural Foran, J. E. Hixson,W. M. Brown, NucleicAcids Res. ment (CBSG, Apple Valley, MN, 1991).
16,' 5841 (1988); T. D. Kocher and A. C. Wilson, in 22. Genetic distances and divergence times can also be
diversity within these species may have im- Evolution of Life, S. Osawa and T. Honjo, Eds. based on SSR ailele trees if the loci studied are se-
portant implications for their future evolution (Springer,Tokyo, 1991), pp. 391-413; A. Di Rienzo lected at random and homoplasy can be detected
and for their use as models in biomedical, and A. C. Wilson, Proc. Natl. Acad. Sci. U.S.A. 88, and excluded; neither assumption can be met here.
1597 (1991)]. All sequences were aligned by hand. 23. Genetic distances have been corrected for intrasub-
paleoanthropological, and evolutionary stud- All chimpanzee control regions had a 1-bp deletion specific polymorphism according to M. Nei [Molec-
ies of humans. at human position 16077 (44). Chimpanzee se- ular Evoiutiona~yGenetics (Columbia Univ., New
quences differed from one another by deletions of 1 York, 1987), p. 2761, and for multiple hits and tran-
or 2 bp at sites 127 and 128 (Fig. 4); two individuals sition bias according to the methods [W. M. Brown,
REFERENCES AND NOTES also had deletions at site 250 (Fig. 4). E. M. Prager,A. Wang, A. C. Wilson, J. Mol. Evol. 18,
10. A. E. Pusey, in The GreatApes, D. A. Hamburgand E. 225 (1982)] for the cyt b sequence, because of the
I . D. S. Woodruff, J. Sci. Soc. Thailand16, 117 (1990); R. McCown, Eds. (Benjamin-Cummings,Menlo Park, lack of transversionswithin P, troglodytes, we used a
Primates 34, 333 (1993); P. A. Morin, J. Wallis, J. J. CA, 1979),pp. 465-480; R. W. Wrangham, ibid., pp. transition to transverslon ratio (R) of 8 (25), and the
Moore, R. Chakraboriy, D. S. Woodruff, ibid, p. 347. 481-489; in Current Probiems in Sociobiology, King's transversion method [R. Higuchi, B. Bowman, M.
2. J. Goodall, The Chimpanzees of Gombe (Harvard College Sociobiology Group, Eds. (Cambridge Univ. Freiberger, 0 . A. Ryder, A. C. Wilson, Nature 312,
Univ. Press, Cambridge, MA, 1986). Press, Cambridge, UK, 1982), pp. 269-289; P. A. 282 (1984); (24, 28)] with R = 15 for the control