The Genetic Consequences of Social Group Fission in a Wild Population of Rhesus Monkeys(Macaca mulatta)Author(s): Don J. Melnick and Kenneth K. KiddSource: Behavioral Ecology and Sociobiology, Vol. 12, No. 3 (1983), pp. 229-236Published by: SpringerStable URL: http://www.jstor.org/stable/4599583Accessed: 23/02/2009 12:38

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Behav Ecol Sociobiol (1983) 12:229-236 Behavioral Ecology and Sociobiology (? Springer-Verlag 1983

The Genetic Consequences of Social Group Fission in a Wild Population of Rhesus Monkeys (Macaca mulatta)

Don J. Melnick' * and Kenneth K. Kidd2 1 Department of Anthropology, Yale University, New Haven, Connecticut 06520, USA 2 Department of Human Genetics, Yale University School of Medicine, New Haven, Connecticut 06510, USA

Received September 2, 1982 / Accepted January 24, 1983

Summary. Micro- and macroevolutionary effects of social group fission will be enhanced if genetic differentiation between fission products is greater than expected by randomly dividing a parent group. There is evidence that division along lines of maternal relatedness produces such an enhanced effect in the provisioned colony of rhesus monkeys on Cayo Santiago Island. In contrast, the genetic analysis presented here of group fission in a wild population of rhesus monkeys in the Himalayan foothills of northern Pakistan shows no 'matrilin- eal effect'. There is a greater than 70% chance of obtaining the observed differences between fis- sion products by random fissioning alone (Fig. 1).

The differing consequences of fission between these two populations are most likely the results of differences in their demographic structure and patterns of paternity. Under conditions of rapid population growth, diffuse paternity and clear ge- netic differences between matrilines, the division of social groups along lines of maternal relatedness should have the greatest genetic effects. When pop- ulations are growing slowly and groups are com- posed of many small matrilines or when restricted paternity prevails the genetic consequences of ma- trilineal fission should be no different from those resulting from random group division.

Fission with and without a matrilineal effect probably occurs at different points in the evolu- tionary history of a primate population. In either case the fission process usually accelerates subpo- pulational differentiation beyond the rate expected by drift alone and may yet prove most important in understanding the genetic structure of many mammalian populations.

* Present address and that for offprint requests: Department of Anthropology, Columbia University, New York, New York 10027, USA

Introduction

Studies of rhesus monkeys in the provisioned col- ony on Cayo Santiago Island (Carpenter 1972) have shown that new social groups are formed by the division or fission of formerly cohesive larger social groups (Chepko-Sade and Sade 1979). This phenomenon has also been observed in wild popu- lations of a number of cercopithecoid primates (Southwick et al. 1965; Furuya 1968, 1969; Nash 1976). Cayo Santiago rhesus social groups have been found to split along lines of maternal related- ness (Chepko-Sade 1974; Chepko-Sade and Sade 1979), though occasionally matrilineal kinship groups themselves spilt during the fission of larger social groups. When a matrilineal division occurs, it is usually between the eldest daughter and her offspring and the rest of her genealogy (Chepko- Sade and Sade 1979). The average degree of mater- nal relatedness is always higher in fission groups than in preexisting parent groups. This higher degree of relatedness seems to be reflected in greater social cohesiveness within the fission groups. Since smaller social groups tend to be sub- ordinate to larger ones, the smaller fission group is usually forced from the home range it once occu- pied when part of the parent social group. Fission group dispersion is the only way females disperse in rhesus populations.

Fission along lines of maternal relatedness can theoretically have profound microevolutionary and macroevolutionary effects and thus provide a clear link between social structure, maternal kinship and the dynamics of genetic change. In a microevolutionary sense, if matrilineal fission creates differences between fission groups greater than expected from a random fissioning process, it would have the effect of accelerating social group differentiation beyond the rate expected by drift

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and random subdivision alone. Consequently, the ubiquity of matrilineal splitting would result in a very heterogeneous set of social groups within a population and populations within a species. This is analogous to the 'lineal effect' suggested by Neel (1967) and Neel and Salzano (1967) for Amerin- dian village fission and is graphically illustrated in one population of Amerindians by Smouse et al. (1981).

The creation of founder groups through the fission of preexisting social groups may have con- siderable macroevolutionary consequences as well. If a daughter fission group moves into a previously uninhabited area, it may constitute a founder group that is genetically quite different from either the parent group or the entire population from which it was derived. The extent to which it de- viates from the parent group (or population) will be inversely proportional to its size and the related- ness of individuals within the group (Fix 1978). Templeton (1980) has shown that lineal fission- founder group formation may also result in consid- erable alterations in the intrinsic genetic environ- ment inducing a selective bottleneck and thereafter a genetic transilience (Templeton 1979). This could lead to speciation. In short, lineal fissioning of small social groups may create novel gene fre- quency combinations which may affect both a founder group's ability to colonize a new area and the potential for its reproductive isolation and spe- ciation.

A central hypothesis to be tested, then, is whether the genetic consequences of matrilineal fis- sion are significantly different from those that arise from a random assortment of individuals during a fission. If the answer is yes, we can begin to establish a causal relationship between the social dynamics of group formation and the extant genet- ic structure of a primate population. We may also be able to explain in part the unusually rapid rates of chromosomal evolution and speciation among the primates (Wilson et al. 1975; Bush et al. 1977).

The genetic effects of matrilineal fission have been assessed in the rhesus monkey colony at Cayo Santiago (Duggleby 1977; Cheverud et al. 1978; Olivier et al. 1978; Ober 1979; Olivier et al. 1981). Here we report results of a study on a wild popula- tion of rhesus monkeys. These results offer a some- what different perspective from which to assess the generality of previous findings for this species and potentially shed light on the circumstances under which a matrilineal effect in the fission of rhesus social groups will and will not be different from the effect of simple random group division.

Materials and Methods

Social Group B. Social group B is one of seven social groups in a population of 291 rhesus monkeys inhabiting a section of moist temperate forest (Dunga Gali) in the Himalayan foot- hills of the Northwest Frontier Province of Pakistan (Melnick 1981; Melnick, Jolly, and Kidd, in preparation; Richard, in preparation). Groups in this population ranged in size from 18 to 65 members. Social group B was one of the smaller groups numbering 29 individuals. It was observed intact from June 1978 until March 1979, when it divided. During the intact peri- od, one high ranking adult male left the group (November 1978) leaving only 28 members. Though small, this group had approximately the same age and sex composition as the entire population and each of the constituent social groups (Melnick 1981; Melnick and Phillips-Conroy, in preparation). When the group divided, it formed two daughter groups of 18 and 10 members. Observations on social interactions and individual associations (Pearl, personal communication) as well as geno- type data suggest that at least some maternally related individ- uals joined the same fission group. Thus social group B may have split along lines of maternal relatedness. The smaller fis- sion group left the range of our study population when the split was complete, leaving behind a social group (i.e. large fission group) of 18 individuals.

Genetic Data. The genetic data used to assess the effects of group fission were obtained from blood samples taken from 26 of the 29 original members of social group B. Animals were individually live-trapped in June 1978 and 14 ml of blood were removed from each monkey (Melnick 1981). Sixteen plasma proteins and red-cell enzymes were assayed by starch and poly- acrylamide electrophoresis (Melnick 1981; Melnick, Jolly, and Kidd, in preparation) of which four were found to be poly- morphic. All systems of protein variation (Transferrin, NADH- Diaphorase, Glucose phosphate isomerase, Adenosine deami- nase) have been shown from previous mating experiments (Goodman and Wolf 1963; Vandeberg and Stone 1978; Shotake 1979; Smith, personal communication) to be the prod- ucts of codominant alleles at individual autosomal loci. Gene frequencies were obtained by simple gene counting (see Ta- ble 1). The gene and genotype frequencies of group B formed the data base on which computer simulations were performed.

Genetic Distance. The genetic difference between the resulting fission groups of the actual fission and those of simulated fis- sions (see below) was estimated using a genetic distance measure (Cavalli-Sforza and Edwards 1967) analogous to a standardized variance (Wahlund 1928) or FST (Wright 1943). If there are only two alleles at the locus examined then the distance between any pair of populations can be calculated directly using Wah- lund's formula,

pq

where U2 is the variance in the frequency of one of the two alleles, p is the mean frequency of that allele and q =(1 -p). When the number of alleles at a particular locus exceeds two, an angular transformation can be used to estimate a Wahlund's variance (Cavalli-Sforza 1969; Cavalli-Sforza and Edwards 1967). We calculated an average, f8, of the Wahlund's variances at the four polymorphic loci using the methods of Kidd and Cavalli-Sforza (1974). Cavalli-Sforza (1969) has shown that if no selection is assumed fo values and not distance values (i.e.

f0) are a more appropriate measure of difference. Since sam- pling is assumed to produce differences between fission groups,

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we have chosen to use fd to measure the differences between groups.

Simulation Model. In the absence of sufficient data to recon- struct pedigrees we were unable to construct a simulation model which divided groups along lines of relatedness with which to compare the observed fission groups. Instead, we compared the resulting genetic differences between the large and small fission groups of social group B with a distribution of differ- ences expected from a process of random fissioning. In this way we could eliminate at the very least the possibility of the fission occurring randomly if in fact the genetic differences ob- served between the fission products of group B were extremely unlikely under such a model.

The computer model developed to simulate the random aggregation of individuals during the fission of a social group chose a predetermined number of individuals (n) from an array of individuals comprising the members of a parent group (N) and placed them in one fission group. The remaining individ- uals (N-n) were placed in the second group. This is analogous to hypergeometric sampling (Sokal and Rohlf 1969) because it is done without replacement. All groups were modelled to split into two smaller groups. This reflects observations in both our study population and in the Cayo Santiago colony (Chepko-Sade and Sade 1979).

Once the composition of each fission group was deter- mined, the multilocus genotype of each monkey was assigned to its fission group. Gene frequencies for all loci were calcu- lated. An f, genetic distance was then calculated between the fission groups. The entire procedure was replicated a predeter- mined number of times (t). After each simulated fission (or trial), the genetic distance was stored in an array. A collation of the resulting genetic distances was subdivided into a continu- ous set of intervals from zero to one. The number of cases assigned to each interval was used to create a distribution of expected distances. Similarly, a count (d) was kept of all genetic distances which fell below the actual observed distance. In this way a probability (p= 1 - dlt) of achieving a genetic distance as great or greater than the one observed could be calculated. The simulation described here is analogous in many ways to Fisher's randomization test (Fisher 1960), particularly because it makes no a priori assumption about the distribution of inter- populational differences (or distances). It is also worth noting that this model, while developed independently, is virtually identical to that of Smouse et al. (1981).

Results

Changes in Genetic Differentiation

At the time of the split only 25 of 28 members of group B had been trapped. Therefore our genet- ic assessment of the split is based on samples of 16 and nine monkeys from actual fission groups containing 18 and 1O members, respectively. Ta- bles 1 and 2 illustrate the magnitude of genetic dif- ferentiation at various levels resulting from the split. Table 1 also demonstrates, as did the work of Duggleby (1977) for the Cayo Santiago popula- tion, that the smaller fission group deviates from the parent group to a greater extent than the larger fission group. However, the smaller fission group

Table 1. Gene frequency distributions for total population, parent group B, and the fission groups of B

Locus allele Total Group B Larger Smaller popula- fission fission tiona group group

Tf A 0.052 C 0.238 0.400 0.406 0.389 D" 0.138 0.180 0.219 0.111 D' 0.049 D 0.049 0.040 0.111 F 0.129 0.040 0.031 0.056 G 0.281 0.300 0.281 0.333 H 0.063 0.040 0.063

DIA 1 0.705 0.440 0.469 0.389 2 0.235 0.540 0.500 0.611 3 0.060 0.020 0.031

GPI 1 0.912 0.920 0.938 0.889 9 0.088 0.080 0.062 0.111

ADA 2 0.964 0.960 0.969 0.944 3 0.036 0.040 0.031 0.056

a Includes social group B before fission

Table 2. Genetic distances between total population, parent group B and the fission groups of B

1 2 3 4

Total population -

Parent group B 0.0471 -

Large fission group 0.0540 0.0090 -

Small fission group 0.0751 0.0175 0.0454

would be more likely to deviate from the parent group, whether the samples were drawn at random or whether by maternal correlation (Fix 1978; Ober 1979). Greater deviation from the parent group is reflected in a genetic distance between the smaller fission group and the parent group (JO=0.0175) that is twice as large as the distance between the larger fission group and the parent group (J0=0.009). We know from this study and others (Southwick et al. 1965; Furuya 1969; Nash 1976) that the smaller fission group disperses from the home range of the parent group. The evidence suggests that, in the role of founder group, this small fission group may constitute a small unrepre- sentative sample of an already small unrepresenta- tive sample (i.e. social group) of the population. Even in the absence of matrilineal fissioning the complexity of this double finite sampling process may be sufficient to result in significant microgeo- graphic differentiation.

The genetic distance between the two fission groups of B is 0.0454. This is smaller than the

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500-

400-

NUMBER

OF 300- OBSERVATIONS

200-

100

0.025 /0.050 0.075 0.100 0.125 0.150 0.175

a GENETIC DISTANCE

500

400-

NUMBER OF 300-

OBSERVATIONS

200

100-

0.025 / 0.050 0.075 0.100 0.125 0.150 0.175 0.200

b GENETIC DISTANCE

Fig. 1. A distribution of genetic distances between fission groups formed at random using all members (a) and only the natal portion (b) of parent group B. The shaded portion of each distribution represents all values equal to or greater than the observed distance (marked by the arrows): t= 0.0454 and 0.0380, respectively. Note the definite skewness of the distributions as estimated by the simulation

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average genetic distance between social groups, 0.0624. Similar differences were found calculating homogeneity chi-squares for the fission groups and for social groups within the population (2 = 2.194, P <0.90 and X2 =82.23, P<0.001, respectively). These results are similar, again, to those for Cayo Santiago, indicating that fission does not explain all intergroup differences but -that it has a substan- tial effect on the baseline differences between newly formed groups. The portion of group B remaining in the population is more different from the other social groups than was the parent group B. This is reflected in an average increase in go of approxi- mately 0.009 (or 13%). As in the case of fission- founder group formation, sampling a social group already quite different from other groups in the population may cause further differentiation. This may lead to increased differences between social groups within a population over time.

Simulation of Random Fission

Twenty-five monkeys with the genotypes of those in parent group B were divided randomly into two smaller groups of 16 and 9 monkeys. There are 25 !/16 !9! or 2,042,975 different ways in which this division could occur. Therefore the 'true' distribu- tion of fission group differences was approximated by simulation. The division was simulated 10,000 times and a distribution of resulting genetic distances was drawn (Fig. la). Only 2,601 dis- tances fell below the observed distance 0.0454. Hence, the probability (p) of achieving a genetic distance equal to or greater than the observed dis- tance by random fission is very large. The esti- mated probability is 0.7399 or approximately 74%.

In rhesus monkey social groups, subadult males usually leave their natal group while females remain in the group into which they were born throughout their lives (Sade 1972; Melnick, Pearl, and Richard, in preparation). In order to avoid the possibility that the inclusion of non-natal males in the analysis obscured the matrilineal effects of fission, we simulated a split that included only natal animals and excluded subadult and adult males known to have originated outside group B. The observed genetic distance (J0) between natal portions of the fission groups was 0.0380. As before, this division was simulated 10,000 times and the distribution of resulting genetic distances is illustrated in Fig. 1 b. Again, the probability of achieving a genetic distance equal to or greater than the observed by random fission is extremely high. An estimate of that probability from the sim-

ulation is 0.9468 or approximately 95%. Thus it appears that the genetic differences observed be- tween the larger and smaller fission products of social group B are no different than expected from a random division of the parent group.

Discussion

It has been reported (Olivier et al. 1978; Ober 1979) that a random fission model does not ade- quately explain the genetic differences between the fission products of social groups in two of three fissions in the rhesus colony of Cayo Santiago. The differences are more likely the result of sam- pling with maternal correlation. This is at odds with the effects of fission we have just described in a wild rhesus population. The conflicting results for the Cayo Santiago and Dunga Gali popula- tions could be a product of errors in our simulation or differences in the structure and dynamics of the two populations.

There are two possible sources of error in the simulation experiment: (1) repeated drawing of the same fission compositions and (2) the creation of biologically meaningless fission groups (e.g. all im- mature individuals). We do not believe that either of these factors has had major effects on the outcome of the experiment. There are more than two million possible ways of splitting 25 monkeys into groups of 16 and 9. The probability of drawing any particular combination more than once in a set of 10,000 trials is very small. If it does occur in this analysis, it is a very rare event and should have little effect on the final distribu- tion of genetic distances. The importance of the second source of error is more difficult to evaluate. A number of combinations which could be con- structed by the simulation model have little biolog- ical meaning. However, we have no a priori reason to believe that the distribution of genetic distances among biologically meaningless fission groups is any different from that for biologically meaningful splits. In addition, we have no firm empirical data on which to judge a particular hypothetical split, meaningless or not. Thus it is unlikely that the inclusion of biologically 'meaningless' splits biases the results (i.e. alters the shapes or means of the resulting distributions in an appreciable way).

There are at least three substantive explana- tions (not necessarily independent) for the differ- ences between the Dunga Gali results and the Cayo Santiago results. First, the demographic structure of the two populations is very different. Infant mortality, interbirth intervals and inferred average

234

life spans for female rhesus in Dunga Gali (Melnick 1981; Melnick and Phillips-Conroy, in preparation) result in very small mother-offspring groups. In other words, having a female half-sib is more the exception than the rule. Altmann and Altmann (1979) believe that this is the case in most natural primate populations. Altmann (1980) and Seyfarth and Cheney (personal communication) have demonstrated this in baboons and vervets, respectively. The existence of small mother-off- spring groups manifest itself in two important ways: (1) Matrilines, defined here as all adult females and juveniles linked through a common female ancestor over any period of two or more generations, will be relatively smaller in Dunga Gali than comparably defined matrilines on Cayo Santiago. Hence, a given sized fission group in Dunga Gali may contain a greater number of ma- trilines (depending upon the generational depth used to define a matriline) and its members will almost certainly share a more remote common female ancestor, than the same sized fission group on Cayo Santiago; (2) Alternatively, for any given matriline size the number of generational links be- tween individuals will be on average greater and the average kinship coefficient smaller in Dunga Gali than Cayo Santiago. Thus, however one chooses to define a matriline, the overall average kinship coefficient for a fission group will be very small and the sampling involved in its formation only weakly correlated in the Dunga Gali popula- tion. Under these conditions the matrilineal effect of social group fission will be almost nonexistent. This is not the case on Cayo Santiago (Chepko- Sade and Olivier 1979; McMillan and Duggleby 1981), where matrilines (regardless of definition) are substantially larger and average matrilineal and fission group kinship coefficients are relatively higher than found in the Dunga Gali population. In this case, the assortment of individuals by matri- lineal identity can have a major effect. We would argue that this effect is rare in extant natural primate populations, though it may have played an important role at other points in the evolution- ary history of some species.

A second explanation for the different results lies in patterns of paternity (Melnick and Kidd 1981). The Cayo Santiago population contains an abundance of males (Sade, personal communica- tion) and partial paternal exclusion tests cannot exclude a large number of males from being the fathers of offspring in one group. If these are actu- al fathers, and if the pattern holds in other social groups, paternal half-sibs are less common than if only a few males father a year's cohort. In the

Dunga Gali population paternity may be much more restricted. In our main focal group A it was impossible to exclude the highest ranking male from paternity of any offspring born in 1978. If restricted paternity is commonplace many individ- uals of an age cohort in a particular social group will be paternal half-sibs (cf. Altmann 1979). Thus many individuals may be more closely related through their fathers than their mothers and ma- ternal relationships may not reflect total genetic relatedness (i.e. through both parental lines). Since fission takes place along matrilines, individuals who share a common father may be separated in the resulting fission groups. With restricted pater- nity and low female fecundity over several genera- tions, the average kinship coefficient will be deter- mined predominately by paternal relationships. Hence, with high proportions of paternal relatives in the parent social group the degree of lineality (Cheverud et al. 1978) after a matrilineal split, in- versely proportional to the number of shared rela- tions between fission groups, will be lower than when few paternal relations are shared. In short, a matrilineal split on Cayo Santiago may be much closer to a complete lineal split than a matrilineal split in Dunga Gali. Since genetic distances measure contributions through both parental lines, the lower the degree of lineality the weaker the lineal effect of fission. Thus, small matrilines and/ or mixed patrilineal assortment in any fission group will account for the near random appear- ance of the genetic composition of fission groups in the Dunga Gali population. It may, in fact, result in differences between fission groups smaller than expected from random fission alone (cf. Fig. I b).

A third factor which may reduce the matrilineal effect of fission is the degree to which matrilines in a particular group are genetically different. In the absence of substantial differences matrilineal assortment of individuals during social group fis- sion will be of little genetic consequence. On Cayo Santiago matrilines are genetically quite distinct (Ober et al. 1979; McMillan and Duggleby 1981; Olivier et al. 1981) and thus the potential for a matrilineal effect of fission is present (Cheverud et al. 1978). Unfortunately a lack of longitudinal genealogical records makes it impossible for us to assess the genetic differences between matrilines in our population. However, it seems probable that small finite matriline size and high interindividual genetic variability, combined with the multinomial sampling processes of zygote formation and indi- vidual survival, result in genetically distinct matri- lines in Dunga Gali. In short, absence of genetical-

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ly differentiated matrilines in Dunga Gali is unlike- ly to explain the differences in genetic effects be- tween social group fission on Cayo Santiago and in Dunga Gali.

Analysis of one social group fission in the wild suggests that the genetic consequences of group splitting can be accurately modelled in some cases as a process of random sampling without replace- ment, i.e. hypergeometric sampling. This does not mean that the formation of new social groups and potential founder populations through the fission- ing of social groups has trivial genetic conse- quences. The evidence presented here would argue strongly against such a conclusion. The fission of group B and the subsequent departure of one of the resulting fission groups, raised the overall level of intersubpopulational differentiation by 13%. Formation of founder groups by sampling a social group that is itself a sample of the total population may result in a genetic composition markedly dif- ferent from, and thus unrepresentative of, the orig- inal population. This may amplify the divergence of founder groups from the parent population beyond what might be expected from the isolation of a larger, more random and thus more represen- tative portion of a parent population.

It is probable that fission with and without a matrilineal effect occurs at different points in the evolutionary history of a primate population. The actual strength of the matrilineal effect will depend on prevailing vital rates and mating patterns. Dur- ing a colonizing phase when a population is growing, survival rates and interbirth intervals permit large matrilines to develop. In such circum- stances fission groups are probably composed of a few large matrilines with relatively high average kinship coefficients and hence matrilineal splitting can accentuate the effects of social group fission. This may also be a time when fission-founder groups are more susceptible to geographic isola- tion, genetic transilience and subsequent specia- tion. We believe that the population dynamics, de- mographic structure and genetic consequences of group fission in the rhesus population on Cayo Santiago represent a good model of this colonizing phase. Alternatively, during phases of stasis, when populations are either stable or growing very slow- ly, matrilines will be small and fission groups will consist of many of these small matrilines with rela- tively low average kinship coefficients. Under these conditions genetic effects of matrilineal splitting will not be distinguishable from those of hypergeo- metric or random splitting. We believe that the characteristics of the rhesus population in Dunga Gali represent a good model of this phase. It is

important to note that both phases described here should be viewed as two ends of a spectrum within which different combinations of demographic rates and mating patterns will produce intermediate ge- netic consequences of group fission. However, whether fission is a process of random sampling without replacement (e.g. Dunga Gali), a process of sampling with high correlation (e.g. Cayo San- tiago) or something in between, it accelerates to one degree or another subpopulational differentia- tion and founder group divergence.

The genetic consequences of social group fis- sion are only beginning to be understood and many questions remain: Under what precise demo- graphic conditions will a matrilineal fission effect be significant? To what extent does group fission augment differentiation within and between popu- lations? What conditions necessary for genetic transilience are present after fission-founder group formation? The answers to these and other ques- tions may yet prove most important in understand- ing the genetic structure of mammalian popula- tions as well as the rates of chromosomal evolution and speciation among mammals in general and pri- mates in particular.

Acknowledgements. We would like to thank C. Burns, J. Clapp, R. Dewar, S. Goldstein, C. Jolly, W. Keene, H. Khan, M. Pearl, and A. Richard for help in collecting data necessary for this study and N. Cox and D. Pauls for advice in construct- ing the simulation model. We are grateful for the logistic support of Gulzar Khan and Abdul Razak of Bispani village; the American community in Islamabad, particularly Ambassa- dor and Mrs. Arthur Hummel, David and Karen Thurman, Ric and Joel Sherman; Richard Baker, Richard Sakai and Curtis Hayes at the Pakistan Medical Research Council; Sher Mohammed at the U.S. Embassy; Eugene Nasir at the National Herbarium of Pakistan and Tom and Frances Roberts. We appreciate the comments of M. Pearl, A. Richard, D. Sade and T. Olivier on earlier drafts of this paper. This research was supported by an H.J. Carman Doctoral Fellowship and Columbia University Council for Research in the Social Sciences grant 717 to D. Melnick and NSF grants INT7808281 and BNS 77-07342 to A. Richard.

References

Altmann J (1979) Age cohorts as paternal sibships. Behav Ecol Sociobiol 6:161-164

Altmann J (1980) Babbon mothers and infants. Harvard Uni- versity Press, Cambridge (Massachusetts)

Altmann SA, Altmann J (1979) Demographic constraints on behavior and social organization. In: Smith EO, Bernstein IS (eds) Ecological influences on social organization. Garland, New York, pp 47-64

Bush GL, Case SM, Wilson AC, Patton JL (1977) Rapid specia- tion and chromosomal evolution in mammals. Proc Natl Acad Sci USA 74:3942-3946

Carpenter CR (1972) Breeding colonies of macaques and gibbons of Santiago Island Puerto Rico. In: Beveredge WI (ed) Breeding primates. Karger, Basel, pp. 223-230

236

Cavalli-Sforza LL (1969) Human diversity. Proc XII Int Congr Genet 3:405-416

Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analy- sis: models and estimation procedures. Am J Hum Genet 19: 233-257

Chepko-Sade BD (1974) Division of group F on Cayo Santiago. Am J Phys Anthropol 41:472

Chepko-Sade BD, Olivier TJ (1979) Coefficient of genetic rela- tionship and the probability of intragenealogical fission in Macaca mulatta. Behav Ecol Sociobiol 5:263-278

Chepko-Sade BD, Sade DS (1979) Patterns of group splitting within matrilineal kinship groups. Behav Ecol Sociobiol 5:67-86

Cheverud JM, Buettner-Janusch J, Sade DS (1978) Social group fission and the origin of intergroup genetic defferentiation among the rhesus monkeys of Cayo Santiago. Am J Phys Anthropol 49:449-456

Duggleby CR (1977) Blood group antigens and the population genetics of Macaca mulatta on Cayo Santiago. II. Effects of social group division. Yearb Phys Anthropol 20:263-271

Fisher RA (1960) The design of experiments. Oliver and Boyd, Edinburgh

Fix AG (1978) The role of kin-structured migration in genetic microdifferentiation. Ann Hum Genet (Lond) 41:329-339

Furuya Y (1968) On the fission of troops of Japanese monkeys. Primates 9:323-349

Furuya Y (1969) On the fission of troops of Japanese monkeys (Part II). Primates 10:47-60

Goodman M, Wolf RC (1963) Inheritance of serum transferrins in rhesus monkeys. Nature 197:1128

Kidd KK, Cavalli-Sforza LL (1974) The role of genetic drift in the differentiation of Icelandic and Norwegian cattle. Evolution 28:381-395

McMillan C, Duggleby C (1981) Interlineage genetic differenti- ation among rhesus macaques on Cayo Santiago. Am J Phys Anthropol 56: 305-312

Melnick DJ (1981) Microevolution in a population of Himalay- an Rhesus monkeys (Macaca mulatta). PhD dissertation, Yale University

Melnick DJ, Kidd KK (1981) Social group fission and paternal relatedness. Am J Primatol 1: 333-334

Nash LT (1976) Troop fission in free-ranging baboons in the Gombe Stream National Park, Tanzania. Am J Phys Anth- ropol 48:63-77

Neel JV (1967) The genetic structure of primitive human popu- lations. Jpn J Hum Genet 12:1-16

Neel JV, Salzano FM (1967) Further studies of the Xavante Indians. X. Some hypotheses-generalizations resulting from these studies. Am J Hum Genet 19:554-574

Ober CL (1979) Demography and microevolution on Cayo San- tiago. PhD dissertation, Northwestern University

Ober CL, Buettner-Janusch J, Olivier TJ (1979) Genetic differ- entiation between matrilines in the Cayo Santiago macaque groups. Am J Phys Anthropol 50:468

Olivier TJ, Ober CL, Buettner-Janusch J (1978) Genetics of group fissions on Cayo Santiago. Am J Phys Anthropol 48:424

Olivier TJ, Ober CL, Buettner-Janusch J, Sade DS (1981) Ge- netic differentiation among matrilines in social groups of rhesus monkeys. Behav Ecol Sociobiol 8:279-285

Sade DS (1972) A longitudinal study of social behavior of rhe- sus monkeys. In: Tuttle R (ed) Functional and evolution- ary biology of primates. Aldine, Chicago

Shotake T (1979) Serum albumin and erythrocyte adenosine deaminase polymorphisms in Asian macaques with special reference to taxonomic relationships among Macaca assa- mensis, M. radiata, and M. mulatta. Primates 20:443-451

Smouse PE, Vitzthum VJ, Neel JV (1981) The impact of random and lineal fission on the genetic divergence of small human groups: a case study among the Yanomama. Genet- ics 98:179-197

Sokal RR, Rohlf FJ (1969) Biometry. Freeman, San Francisco Southwick CH, Beg MA, Siddiqi MR (1965) Rhesus monkeys

in North India. In: DeVore I (ed) Primate behavior. Holt, Rinehart and Winston, New York, pp 111-159

Templeton AR (1979) The unit of selection in Drosophila merca- torum. II. Genetic revolution and the origin of coadapted genomes in partheno-genetic strains. Genetics 92:1265- 1282

Templeton AR (1980) The theory of speciation via the founder principle. Genetics 94:1011-1038

Vandeberg JL, Stone WH (1978) Biochemical genetics of ma- caques. II. Glucose-phosphate isomerase polymorphism in rhesus monkeys. Biochem Genet 16:691-694

Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Verer- bungslehre aus betrachtet. Hereditas 11:65-106

Wilson AC, Bush GL, Case SM, King MC (1975) Social structuring of mammalian populations and the rate of chromosomal evolution. Proc Natl Acad Sci USA 72:5061- 5065

Wright S (1943) Isolation by distance. Genetics 28:114-138