American Journal of Primatology 38:157-168 (1996)

Nucleotide Polymorphism, Effective Population Size, and Dispersal Distances in the Yellow Baboons (Papio hamadryas cynocephalus) of Mikumi National Park, Tanzania

JEFFREY ROGERS AND KENNETH K. KIDD' 'Department of Genetics, Southwest Foundation for Biomedical Research, Sun Antonio, Texas; and 'Department of Genetics, Yale Uniuersity School of Medicine, New Haven, Connecticut

We investigated genetic variability and population structure in a natural population of yellow baboons (Papio hamadryas cynocephalus) from Mi- kumi National Park, Tanzania. The amount of nuclear DNA polymor- phism in a random sample of animals from four social groups was esti- mated by using Southern blotting to detect restriction fragment length polymorphisms in five nuclear autosomal loci. The average nucleotide het- erozygosity was estimated to be 0.0033. This level of DNA polymorphism is higher than available estimates for human populations, but is consis- tent with protein and DNA sequence data from other nonhuman primates. The observed level of genetic variability suggests that the inbreeding ef- fective population size of the Mikumi baboons is approximately 14,000. Predictions regarding the distribution of male dispersal distance are de- veloped using Wright's isolation by distance model. The results of these analyses, while derived from genetic methods, are consistent with and provide additional information for behavioral and demographic descrip- tions of baboon population dynamics. o 1996 Wiley-Liss, Inc.

Key words: nucleotide diversity, DNA polymorphism, heterozygosity, dispersal, male migration, cercopithecines

INTRODUCTION The effective size of an animal population reflects the influence of a number of

different demographic and genetic processes, including mating structure, immi- gration, and recent population history. Estimation of the effective size of popula- tions is a fundamental aspect of evolutionary biology, because knowledge of effec- tive sizes allows researchers to develop quantitative inferences regarding many aspects of evolutionary dynamics, including levels of genetic variability, the rate of fixation of new alleles, average coefficients of kinship, and other aspects of popu- lation biology. A number of investigators have estimated the effective size of var-

Received for publication January 2, 1995; revision accepted August 2, 1995.

Address reprint requests to Dr. Jeffrey Rogers, Department of Genetics, Southwest Foundation for Biomedical Research, P.O. Box 28147, San Antonio, TX 78228.

0 1996 Wiley-Liss, Inc.

158 / Rogers and Kidd

ious mammalian populations, and the results are somewhat contradictory. Nei and Graur [1984] derived estimates of effective population size (N,) for 74 species, including 41 mammals, from observed levels of protein polymorphism. Among the mammals examined, most of the estimates were between 10,000 and 200,000. Melnick [19881 reviewed data on the geographic distribution of protein polymor- phisms in seven species of cercopithecine primates and concluded that extensive gene flow maintains genetic similarity among populations. While he did not cal- culate N, for any population or species, Melnick's analysis suggests that both local and regional populations of these primates have large effective sizes. However, all the estimates described above depend upon the assumption that protein polymor- phisms are selectively neutral, and there is growing reason to question that as- sumption [e.g., Karl & Avise, 19921.

Other approaches that do not use protein data have been used to estimate effective population size. Chepko-Sade and Shields [ 19871 used demographic data to estimate N, in several mammalian taxa, and concluded that local effective population sizes are generally quite small, often less than 200. Analyses of captive breeding programs suggest that many mammalian species have local effective population sizes that number in the thousands rather than the hundreds [Temple- ton, 19871.

The substantial differences among these previous estimates may be the result of true biological differences among the species investigated. On the other hand, the methods used are subject to inherent uncertainties. Definitive estimates of N, for primate populations are not yet available. We report here the estimation of effective population size in a local population of yellow baboons (Pupio hamadryas cynocephalus). Our estimate is based on the sampling of nucleotide heterozygosity or diversity across five single-copy nuclear, autosomal genes in a natural popula- tion. In addition, we use our estimate of effective population size to develop infer- ences about male dispersal distance among the study animals.

METHODS Study Site and Study Population

Mikumi National Park is an area of savanna woodland and grassland covering approximately 3,300 square kilometers in central Tanzania. Studies of the behav- ior, ecology, and demography of the yellow baboons in Mikumi Park were begun in 1974 [Rhine, 1986; Rhine et al., 19881 and continue at this time. We report here on one aspect of a combined study of genetics, morphology, and parasitology con- ducted by one of us (J.R.) and Dr. Jane Phillips-Conroy of Washington University, St. Louis. The study population for the present analyses consists of four social groups of baboons. These study groups ranged in census size from 26 to 70, and inhabit overlapping home ranges in the central region of the park (7" 15' South, 37" 10' East). Several reproductively active adult males have been observed to migrate among these groups. Consequently, the four groups are considered to be members of a single, large breeding population (deme) with boundaries that are presently undefined, but that encompass at least the four study groups and several others regularly observed in the area. To obtain DNA for molecular genetic analyses, individual baboons were captured, blood samples drawn, and the animals released. Details of capture techniques and field processing of blood samples have been previously described [Rogers, 1989; Rogers & Kidd, 19931. The following analyses are based on a sample of 27 animals that were randomly drawn from the four social groups examined.

DNA Polymorphism in Yellow Baboons / 159

TABLE I. Loci Tested and Probes Used in Screen for RFLPs Among the Mikumi Baboons

Locus Probe Type Source AT3 PATIII-2 cDNA S. Orkin APOB pABF" cDNA J. Scott HEXB pHEXX Genomic R. Gravel REN pHRnES1.9 Genomic J. Chirgwin VIM hp4Fl cDNA R. Baserga

"2.1 kb BamHI fragment.

Laboratory Methods High-molecular-weight DNA was extracted from white blood cells using a

modification of standard procedures [Rogers & Kidd, 19931. DNA samples from 27 individuals were digested separately with six restriction endonucleases, five with six-base restriction sites (EcoRI, HindIII, BamHI, PuuII, and BgZII) and one with a four-base restriction site (TaqI), according to manufacturers' recommendations. For each of the six endonucleases, 8 p,g of total genomic DNA was digested per individual. Digested DNA was run in standard 1% agarose gels and transferred to nylon membranes (Hybond-N, Amersham, Inc.) following standard capillary trans- fer procedures.

The DNA probes used in this study to detect restriction fragments of baboon genomic DNA are either human cDNA clones or human genomic clones that in- clude at least one exon for a functional gene. We chose to use human DNA clones that include coding sequence in order to obtain reliable hybridization to specific identifiable loci. The five loci examined were antithrombin I11 (AT3), apolipopro- tein B (APOB), vimentin (VIM), renin (REN), and hexosaminidase B (HEXB). The probes used for each are listed in Table I. Linear human DNA probes were labeled with radioactive 32P-dCTP using oligolabeling procedures [Feinberg & Vogelstein, 19831. Hybridization of radiolabeled probe to baboon genomic DNA followed stan- dard procedures using 50% formamide, 5% dextran sulfate, and Denhardt's solu- tion [Rogers & Kidd, 19931. After hybridization for 48 hr a t 42"C, the membranes were first washed for 3 x 15 min in 2 x SSC (0.3 M NaC1, 0.03 M sodium citrate, 0.1% SDS) at room temperature, and then at higher stringency (15 min in 0.5 x SSC at 65°C). Autoradiography of washed membranes used Kodak X-OMAT AR x-ray film and cassettes with intensifying screens.

RESULTS To calculate effective population size for the Mikumi baboons, we first esti-

mated nucleotide heterozygosity (or diversity) in the five loci. The DNA probes for restriction fragment length polymorphism (RFLP) testing were selected at random from a set used by K.K.K. in studies of human genetic linkage and in human population studies. We had no prior information concerning the number, size, or variability of baboon restriction fragments detected with these probes. Collec- tively, the five probes detected 14 distinct RFLP systems (polymorphisms). Each locus exhibited at least one polymorphism, and all the restriction enzymes except BamHI revealed at least one polymorphic site. All polymorphisms appear to be inherited in a codominant Mendelian fashion. In five cases we have investigated the pattern of inheritance in captive pedigreed baboons, and found codominant inheritance in each [Rogers & Kidd, 1993; Rogers, unpublished data]. In both the Mikumi and captive samples, no one RFLP was revealed by more than one enzyme,

160 / Rogers and Kidd

TABLE 11. Restriction Sites Sampled at Each of Five Loci

Total sites sampled Total sites polymorphic

Locus

AT3 APOB VIM REN HEXB Total

4-Base 6-Base sites sites

3-4 21-28 8-12 25-37

2 13-15 5 11 5 18

23-28 88-109

4-Base sites

0 2 0 2 1 5

6-Base sites n* = Polymorphic enzymes

4 54 PuuII,HkfIII&coRI,BglII 3 54 TaqIQuuI1,BglII 1 46 BglII 1 52 TuqI,BgZII, 3 48 TuqI,HiindIII,BglII~uuII

12 50.8

an is the number of chromosomes sampled for each restriction enzyme at each locus.

which strongly suggests that these polymorphisms are caused by basepair changes rather than insertioddeletion mutations. The following analyses assume that all RFLPs are the result of single basepair mutations. Detailed descriptions of frag- ment sizes and estimated allele frequencies have been published elsewhere [Rogers & Kidd, 19931.

The 14 polymorphic systems are summarized in Table 11. For the two human genomic probes used (probe pHRnES1.9 for locus REN and probe pHEXX for locus HEXB) it is simple to determine the number of restriction sites sampled by each restriction enzyme and the proportion that are polymorphic. The total number of sites sampled is the number of restriction fragments observed plus one. The num- ber of polymorphic sites is the number of alleles minus one.

The situation is somewhat more complicated when using cDNA clones. When two or more restriction fragments are detected with a single cDNA probe, it is not apparent how many distinct restriction sites have been sampled by the enzyme because the restriction fragments may not be contiguous in the baboon genomic DNA. Consequently, it is not possible to determine the exact number of restriction sites sampled and hence the average heterozygosity. We have calculated minimum and maximum estimates of nucleotide polymorphism for the three cDNA probes used, based on the alternative assumptions that the number of restriction sites sampled is the largest and the smallest number consistent with the observed num- ber of baboon restriction fragments (Table 11). In all three cases the number of polymorphic sites is readily apparent but the number of constant (nonpolymorphic) sites is not.

The minimum and maximum percentage of restriction sites polymorphic and the standard errors of these estimates are presented in Table 111. As expected, the proportion of sites polymorphic varies from locus to locus. To determine whether this variation among loci is greater than would be expected by chance, we used the x2 test of homogeneity across loci. The expected values for each locus were calcu- lated separately for minimum and maximum percent polymorphic using the cor- responding observed proportion of sites polymorphic for the complete dataset (i.e., all loci together). The differences among loci are not larger than would be expected by chance for either test (x2 tests of homogeneity, P > 0.70). Calculation of Average Heterozygosity

Molecular variability in this population sample was quantified in three ways. First, average heterozygosity per nucleotide was calculated using the method of Ewens et al. [1981]. With this approach, heterozygosity (0) is given by

DNA Polymorphism in Yellow Baboons / 161

TABLE 111. Percentage of Restriction Sites Polymorphic

Minimum percent Maximum percent restriction sites restriction sites

Locus polymorphic polymorphic

AT3 12.5 16.7 APOB 10.2 15.2 VIM 5.9 6.7 REN 18.8 18.8 HEXB 17.4 17.4 Mean 12.96 (22.36) 14.96 (22.14)

where k4 is the number of polymorphic restriction sites detected by restriction enzymes with four-base recognition sequences, k, is the number of polymorphic restriction sites detected by enzymes with six-base recognition sequences, m4 is the total number of four-base restriction sites sampled, m6 is the total number of six-base restriction sites sampled, and n is the number of DNA sequences or alleles examined. We calculated this value separately for each locus (Table IV), and as with the estimates of percentage restriction sites polymorphic, the heterozygosity values vary among loci.

The mean estimates calculated using the method of Ewens et al. [1981] suggest that nucleotide heterozygosity in the Mikumi baboons is approximately 0.003. It must be emphasized that this estimate is based on a limited sample of five loci and is subject to considerable sampling error. However, the total number of restriction sites sampled is substantial: at least 111 and possibly as many as 137 sampled in each of 50 chromosomes (Table 11). Since the x2 tests of homogeneity for percent sites polymorphic showed no evidence of statistically significant heterogeneity across loci, the differences among loci can be attributed to sampling, and the mean heterozygosity over the five loci is considered the best estimate of overall nucle- otide heterozygosity .

Hudson’s [ 19821 method of calculating average heterozygosity differs only slightly from that of Ewens et al. [1981]. In Hudson’s method, heterozygosity is calculated as

P (3=- In n

where

k (2m - k)j P = t 3)

and m is the total number of different restriction sites sampled, k is the number that are polymorphic, and j is the weighted average length of enzyme recognition sites.

This second set of heterozygosity estimates is also presented in Table IV. The results are consistently higher than the previous estimates, but the differences are small. Note that the difference between the minimum and maximum estimates of heterozygosity for each method is larger than the difference between analogous values for the two methods.

162 I Rogers and Kidd

TABLE IV. Average Heterozygosity at Five Loci Calculated Using Formulae of Ewens et al. [19811 and Hudson [19821

Locus

AT3 APOB VIM REN HEXB Mean"

Ewens' estimator Hudson's estimator

Minimum 0 Maximum 0 Minimum 0 Maximum 0

0.00272 0.00363 0.00232 0.00344 0.00133 0.00152 0.00441 0.00441 0.00404 0.00404 0.00296 0.00341

0.00291 0.00396 0.00245 0.00373 0.00137 0.00157 0.00487 0.00487 0.00442 0.00442 0.00320 0.00371

"Includes estimates for REN and HEXB in calculations for both minimum and maximum 8.

Nucleotide Diversity as Calculated by the RESTSITE Program Table V presents the values for average nucleotide diversity calculated by the

RESTSITE program package generously provided by Dr. J. Miller. This program calculates average nucleotide diversity directly using observed allele frequencies [see Nei & Miller, 1990, for details]. Standard errors were calculated by the RESTSITE package using jackknifing procedures. To calculate standard errors by jackknifing, first one data point is removed, the nucleotide diversity recalculated, and the removed value is replaced. Next the process is repeated by removing the second value. After all data points have been individually removed and replaced, the resulting distribution of parameter values is used to estimate the standard error of the original diversity estimate. As with the previous estimators, diversity varies from locus to locus. The standard errors of individual locus estimates indi- cate that much of the variance among loci may be due to sampling error rather than true biologically meaningful differences among loci.

These RFLP data indicate that a substantial amount of intra-population vari- ation exists in this local population of baboons. The two estimates of nucleotide heterozygosity based on the methods of Hudson [1982] and Ewens et al. [1981] are in close agreement. The mean estimate of diversity derived by the RESTSITE program is higher than the other values, and this disparity is a consequence of differences in the assumptions made by the various methods. Both of the first two methods use estimates of the proportion of restriction sites that are polymorphic to estimate average nucleotide heterozygosity. They assume that all polymorphisms are neutral and that true population allele frequencies conform to the expected equilibrium distribution predicted under the model of neutral mutations subject to genetic drift. The RESTSITE program calculates average diversity directly using the observed allele frequencies. This Mikumi dataset contains a somewhat larger proportion of polymorphisms with individually high levels of heterozygosity than is predicted at equilibrium in the neutral model. This is probably the result of sampling error due to the small number of loci and polymorphisms studied. The higher mean level of heterozygosity per RFLP system produces a higher estimate of the level of nucleotide variability when the RESTSITE program is used as compared with the Hudson or Ewens methods. It seems most conservative to accept the Hudson or Ewens values rather than the RESTSITE values, since these are less subject to sampling error in allele frequencies. The best single estimate of average nucleotide heterozygosity in the Mikumi population may be the average of the minimum value from the Ewens et al. [1981] equations and the maximum value from the Hudson [19821 equations, which is 0.0033.

DNA Polymorphism in Yellow Baboons / 163

TABLE 5. Average Nucleotide Diversity Calculated by RESTSITE Program

Locus Minimum P Maximum P

AT3 0.0040 (0.0013)a

APOB 0.0051 (0.0022)

VIM 0.0008 (0.0008)

REN 0.0079 (0.0049)

HEXB 0.0085 (0.0026)

Mean 0.00526

0.0055 (0.0018) 0.0077

(0.0034) 0.0010

(0.0009) 0.0079

(0.0049) 0.0085

(0.0026) 0.00612

"The numbers in parentheses are standard errors derived by the RESTSITE program via jackknifing.

Calculation of Inbreeding Effective Population Size The Mikumi RFLP dataset constitutes a random sample of (presumably) neu-

tral polymorphism across several regions of nuclear DNA. Consequently, the re- sults can be used to estimate the inbreeding effective size of the population. The relationship between nucleotide heterozygosity and effective population size is given by

4 N e ~ Het = 4N,p + 1 (4)

where Ne is the inbreeding effective population size and p is the nucleotide mu- tation rate per generation [Crow & Kimura, 19701. The mutation rate in mammals can be determined from the average substitution rate in completely neutral se- quences. Li et al. [19851 found that the average substitution rate across seven pseudogenes was 4.85 x lo-' per basepair per year. We assume this is the muta- tion rate per year and that the generation time for baboons is 12 years, which yields a mutation rate per generation of 5.82 x Using the observed value of 0.0033 for nucleotide heterozygosity in the Mikumi baboons, an estimate of 14,212 is obtained for the inbreeding effective population size. However, this estimate is subject to sampling error and should be taken as preliminary.

Furthermore, we note that 13 of the 14 RFLP systems were polymorphic in all four social groups examined. This suggests that any one group contains a large proportion of the genetic variation found in the surrounding population, and there- fore that the inbreeding N, of individual groups is nearly as large as that of the deme. It seems that alleles found in a single generation of any one group must be derived from a large number of ancestors, much larger than the number of indi- viduals in a single social group. Given the known behavior and demography of yellow baboons, the best explanation for this observation is that male migration acts to transfer alleles among groups. The genetic data presented above can serve as the basis for a quantitative analysis of male migration. These analyses are presented in the next section. DISCUSSION Comparisons With Other Species

The level of nucleotide variability found in the Mikumi baboons is higher than the level reported for humans. Li and Sadler [19911 calculated nucleotide diversity

164 I Rogers and Kidd

in humans using sequence data from 49 loci. The overall level of diversity in their dataset is 0.0006. This estimate includes both coding and noncoding sequences, and the exact value obtained in this type of analysis will depend on the proportion of coding vs. noncoding regions included. The Mikumi RFLP data also includes both noncoding regions and coding sites, though probably much more of the former than the latter. Other studies have also found higher levels of polymorphism in nonhuman primates than in humans [Ferris et al., 1981; Melnick & Hoelzer, 1992; Ruano et al., 1992; Morin et al., 1994; Ruvolo et al., 19941. Taken together these data suggest that humans have an unusually low level of nucleotide diversity compared with other primates. The possibility that humans have a low effective population size has been discussed by Ferris et al. [1981] and Li and Sadler [1991].

Effective Population Size Studies of protein polymorphism have found lower overall levels of heterozy-

gosity in primates and other large mammals than in other groups of organisms, including insects and fish [Selander, 1976; Ward & Skibinski, 19851. In addition, many mammalian populations are subdivided into social groups such as those typical of the Mikumi yellow baboons. This has led some to propose that, as a general rule, mammalian populations have small effective sizes due to inbreeding in subdivided populations [Bush et al., 1977; Chepko-Sade & Shields, 19871.

Nevertheless, studies of protein polymorphisms in baboons and other primates with similar social organization (e.g., macaques) have often found particular loci with multiple alleles and high levels of heterozygosity [VandeBerg, 1992; Olivier et al., 19861. On the basis of protein data, Melnick [l988] suggested that baboon and macaque populations are not inbred and generally have large effective popu- lation sizes. Observations concerning inbreeding depression in mammals also sug- gest that many species have large effective population sizes [Templeton, 19871. Our estimate of approximately 14,000 for the Mikumi baboons agrees with the conclu- sions of Melnick and Templeton.

Inferring Local Population Structure and Male Dispersal Distance in the Mikumi Baboons

The Mikumi RFLP data also allow us to draw two conclusions regarding the genetic structure of this population. Yellow baboons live in social groups that range in size from less than 20 to more than 100 members. Most groups in Mikumi Park number between 50 and 80 individuals. An effective population size two orders of magnitude larger than the average group size suggests that breeding populations or demes consist of large networks of groups interconnected by gene flow.

The majority of male savanna baboons disperse from their natal social groups around the time of sexual maturity [Packer, 1979; Melnick, 1987; Altmann et al., 1988; Smith, 19921. These males migrate to and eventually breed in other groups, whereas females generally remain in their natal groups throughout their lives. The occurrence of male dispersal and intergroup migration is well documented, but the long-term pattern of dispersal and the distribution of dispersal distances, crit- ical parameters in modeling baboon population structure, have been very difficult to estimate [Smith, 1992; see also Sprague, 1992, for a discussion of Japanese macaques]. Field observers studying well habituated groups are unable to follow habituated males as they disperse to distant, unhabituated groups, and it is usu- ally not possible to determine the place of birth for adult males that immigrate into habituated study groups.

DNA Polymorphism in Yellow Baboons I 165

X p.

0 10 20 30 40 50 60

Kilometers

Fig. 1. Probability distributions of male dispersal distance based on estimated effective population size and two estimates of population density.

With our estimate of 14,212 for effective population size and estimates of population density based on field census counts, we can use Wright’s [19461 model of isolation by distance to estimate the probability distribution for male dispersal distances. For the case in which individuals of only one sex disperse from their birthplaces, Wright showed that the effective size of the genetic “neighborhood” N = 2 T u2 d, where u is the standard deviation of dispersal distances and d is the population density. We obtained two estimates of population density (minimum estimate = 5 animals per km2 and maximum estimate = 10 animals per km2) based on daily observations over 2 years in the area inhabited by the study groups [Rogers, 1989, and unpublished data].

The probability distributions for dispersal distance were calculated using these two density estimates, the estimated effective population size of 14,212, and the formula above (Fig. 1). It is assumed that dispersal distance is normally dis- tributed. The distributions we obtain suggest that approximately two-thirds of infants are fathered by males that have dispersed less than 15-22 km, while one-third of infants are the progeny of males that have traveled farther. These estimates are reasonable given that the home ranges of groups in Mikumi are large, often greater than 80-90 km2. Dispersal of about 15 km can be interpreted as dispersal out of a male’s natal home range to join a group with a neighboring but nonoverlapping territory. Movement of less than about 12 km can be interpreted as transfer from the natal group to a group with a home range that partially overlaps that of the natal group. In Mikumi, very few if any groups have home ranges that are entirely exclusive. However, if dispersal distances are not normally distrib- uted, then this description may not hold.

We also note that demographic and behavioral processes other than male migration influence effective population size. The ratio of number of females to number of males breeding in each generation, and the variance in reproductive success among males or among females affect effective population size. We cannot estimate these variables in this study. In addition, substantial fluctuations in population census size over time would alter long-term effective size. Our analysis

166 I Rogers and Kidd

here predicts male dispersal distances given current observed population densities, and will not be valid if one or more of these other parameters (e.g., variance in reproductive success or population census size) have changed dramatically in the recent past.

Despite these potential complicating factors, our results for male dispersal among the Mikumi baboons are similar to results from previous studies of other cercopithecine species. In an investigation of male migration among olive baboons, Packer [ 19791 found that all males moved between adjacent groups, but some males moved several times during their adult life. It is possible that many or most transfers by natal males in the Mikumi population involve movement from the natal group to a group with an overlapping or adjacent territory, and that subse- quent migrations take some individuals even farther from their natal home ranges. Nozawa et al. [1982] used information on demography and protein poly- morphisms to show that the population structure of Japanese macaques can be described as a series of local demes or “local concentrations’’ of social groups. The genetic differentiation observed by Nozawa et al. suggests that male migration is common among groups within small clusters, but that dispersal from one cluster to another is much less frequent. Such a pattern of dispersal would be consistent with the RFLP results for Mikumi baboons presented above. Cheney and Seyfarth [1983] studied male migration among vervet monkeys, and found that 26 of 28 transferring males moved between neighboring groups. This pattern of male mi- gration, in which transfer occurs predominantly, but not exclusively, between neighboring social groups, may be broadly applicable to many cercopithecine mon- keys.

CONCLUSIONS

1. The Mikumi population of yellow baboons exhibits high levels of nuclear DNA polymorphism. Our estimate based on five autosomal loci indicates that the average nucleotide heterozygosity is 0.0033.

2. This observed level of DNA polymorphism suggests that the inbreeding effective population size of the Mikumi population is approximately 14,000. This estimate is concordant with estimates based on protein polymorphisms in macaques, but not with estimates for other large mammals derived from demo- graphic data.

3. Using field census data and the calculated effective population size, we derive a predicted distribution for male dispersal distance. It suggests that two- thirds of infants in this population are sired by males that have traveled less than 22 km from their birthplace. This distribution is reasonable given observed de- mography and behavior of the Mikumi baboons.

ACKNOWLEDGMENTS We thank Dr. Jane Phillips-Conroy for her efforts and guidance during the

fieldwork phase of this project. We also thank the Tanzanian National Scientific Research Council, Serengeti Wildlife Institute, and Tanzanian National Parks for permission to work at Mikumi, and acknowledge the help provided by Park War- dens Mr. E. Kishe, Mr. E. Kibasa, and Mr. S. Dembe. C. J. Jolly, R. Rhine, G. Norton, S. Wasser, E. Sterling, J . R. Kidd, and J . Blangero also provided assistance at various stages. We also thank anonymous reviewers for their helpful comments on this manuscript. This research was funded by NSF Grant BNS83-03506 to Jane Phillips-Conroy and NSF Grant BNS86-19703-01 to K.K.K.

DNA Polymorphism in Yellow Baboons / 167

REFERENCES Altmann, J.; Hausfater, G.; Altmann, S.A.

Determinants of reproductive success in savannah baboons, Papio cynocephalus. Pp. 403-418 in REPRODUCTIVE SUC- CESS. T.H. Clutton-Brock, ed. Chicago, University of Chicago Press, 1988.

Bush, G.L.; Case, S.M.; Wilson, A.C.; Patton, J.L. Rapid speciation and chromosomal ev- olution in mammals. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCI- ENCES USA 74~3942-3946,1977.

Cheney, D.L.; Seyfarth, R.M. Nonrandom dispersal in free-ranging vervet monkeys: Social and genetic consequences. AMERI- CAN NATURALIST 122:392-412,1983.

Chepko-Sade, B.D.; Shields, W.M. The ef- fects of dispersal and social structure on effective population size. Pp. 287-322 in MAMMALIAN DISPERSAL PATTERNS. B.D. Chepko-Sade; Z.T. Halpin, eds. Chi- cago, University of Chicago Press, 1987.

Crow, J.F.; Kimura, M. AN INTRODUC- TION TO POPULATION GENETICS THEORY. New York, Harper and Row, 1970.

Ewens, W.J.; Spielman, R.S.; Harris, H. Es- timation of genetic variation at the DNA level from restriction endonuclease data. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES USA 78:3748- 3750,1981.

Feinberg, A.P.; Vogelstein, B. A technique for radiolabeling DNA restriction endonu- clease fragments to high specific activity.

13, 1983. Ferris, S.D.; Brown, W.M.; Davidson, W.S.;

Wilson, A.C. Extensive polymorphism in the mitochondrial DNA of apes. PRO-

EMY OF SCIENCES USA 78:6319-6323, 1981.

Hudson, R.R. Estimating genetic variability with restriction endonucleases. GENET- ICS 100:711-719,1982.

Karl, S.A.; Avise, J.C. Balancing selection at allozyme loci in oysters: Implications from nuclear RFLPs. SCIENCE 256:lOO-102, 1992.

Li, W.-H.; Sadler, L.A. Low nucleotide diver- sity in man. GENETICS 129:513-523, 1991.

Li, W.-H.; Luo, C.-C.; Wu, C.-I. Evolution of DNA sequences. Pp. 1-94 in MOLECU- LAR EVOLUTIONARY GENETICS. R.J. MacIntyre, ed. New York, Plenum Press, 1985.

Melnick, D.J. The genetic consequences of primate social organization: A review of macaques, baboons and vervet monkeys. GENETICA 73:117-135,1987.

Melnick, D.J. The genetic structure of a pri-

ANALYTICAL BIOCHEMISTRY 132~6-

CEEDINGS OF THE NATIONAL ACAD-

mate species: Rhesus macaques and other cercopithecine monkeys. INTERNA- TIONAL JOURNAL OF PRIMATOLOGY 9:195-231, 1988.

Melnick, D.J.; Hoelzer, G.A. Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. INTERNA- TIONAL JOURNAL OF PRIMATOLOGY 13:379-393, 1992.

Morin, P.A.; Moore, J.J.; Chakraborty, R.; Jin, L.; Goodal, J.; Woodruff, D.S. Kin se- lection, social structure, gene flow and the evolution of chimpanzees. SCIENCE 265:

Nei, M.; Graur, D. Extent of protein poly- morphism and the netural mutation the- ory. EVOLUTIONARY BIOLOGY 17:73- 118, 1984.

Nei, M.; Miller, J.C. A simple method for estimating average number of nucleotide substitutions within and between popula- tions from restriction data. GENETICS 125873-879, 1990.

Nozawa, K.; Shotake, T.; Kawamoto, Y.; Tanabe, Y. Population genetics of Japa- nese monkeys: 11. Blood protein polymor- phisms and population structure. PRI- MATES 23:252-271, 1982.

Olivier, T.J.; Coppenhaver, D.H.; Steinberg, A.G. Distribution of immunoglobulin allo- types among local populations of Kenyan olive baboons. AMERICAN JOURNAL OF

1986. Packer, C. Inter-troop transfer and inbreed-

ing avoidance in Papio anubis. ANIMAL

RESTSITE. A computer program package distributed by J.C. Miller, Whitehead In- stitute, Boston, Maine.

Rhine, R.J. Ten years of cooperative re- search at Mikumi National Park. PP.

1193-1201,1994,

PHYSICAL ANTHROPOLOGY 70~29-38,

BEHAVIOUR 27:l-36,1979.

13-22 in PRIMATE ONTOGENY, COG- NITION AND SOCIAL BEHAVIOR. J.G. Else; P.C. Lee, eds. Cambridge, Cambridge University Press, 1986.

Rhine, R.J.; Wasser, S.K.; Norton, G.W. Eight-year study of social and ecological correlates of mortality among immature baboons of Mikumi National Park, Tanza- nia. AMERICAN JOURNAL OF PRIMA-

Rogers, J. Genetic structure and microevolu- tion in a population of Tanzanian yellow baboons. Unpublished Ph.D. Thesis, Yale University, 1989.

Rogers, J.; Kidd, K.K. Nuclear DNA poly- morphisms in a wild population of yellow baboons (Papio hamadryas cynocephalus) from Mikumi National Park, Tanzania.

TOLOGY 16~199-212, 1988.

168 I Rogers and Kidd

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 90:477-486,1993.

Ruano, G.; Rogers, J.; Ferguson-Smith, A.C.; Kidd, K.K. DNA sequence polymorphism within hominoid species exceeds the num- ber of phylogenetically informative charac- ters for a HOX2 locus. MOLECULAR BI-

1992. Ruvolo, M.; Pan, D.; Zehr, S.; Goldberg, T.;

Disotell, T.R.; von Dornum, M. Gene trees and hominoid phylogeny. PROCEEDINGS

ENCES USA 91:8900-8904,1994. Selander, R.K. Genic variation in natural

populations. Pp. 21-45 in MOLECULAR EVOLUTION. F.J. Ayala, ed. Sunderland, MA, Sinauer Associates, 1976.

Smith, E.O. Dispersal in sub-Saharan ba- boons. FOLIA PRIMATOLOGICA 59:177- 185,1992.

Sprague, D.S. Life history and male inter- troop mobility among Japanese macaques (Mucacu fuscutu). INTERNATIONAL

OLOGY AND EVOLUTION 9~575-586,

OF THE NATIONAL ACADEMY OF SCI-

JOURNAL OF PRIMATOLOGY 131437- 454,1992.

Templeton, A.R. Inferences on natural pop- ulation structure from genetic studies on captive mammalian populations. In MAM- MALIAN DISPERSAL PATTERNS. B.D. Chepko-Sade; Z.T. Halpin, eds. Chicago, University of Chicago Press, 1987.

VandeBerg, J.L. Biochemical markers and restriction fragment length polymor- phisms in baboons: Their power for pater- hity exclusion. In PATERNITY IN- PRI- MATES: GENETIC TESTS AND THEORIES. R.D. Martin; A.F. Dixson; E.J. Wickings, eds. Basel, Switzerland, S. Karger, 1992.

Ward, R.D.; Skibinski, D.O.F. Observed re- lationships between protein heterozygosity and protein genetic distance and compari- sons with neutral expectation. GENETI- CAL RESEARCH 45:315-340, 1985.

Wright, S. Isolation by distance under di- verse mating systems. GENETICS 31:39- 59, 1946.