Social group fission and the origin of intergroup genetic differentiation among the rhesus monkeys of Cayo Santiago.

The serum transferrin locus is used to investigate the roles of the lineal effect of fission, male migration effect of fission, and genetic drift in causing intergroup genetic differentiation among the rhesus macaques of Cayo Santiago. These three mechanisms prove sufficient to explain the degrees of differentiation between the newly formed social groups A, K, and L as of July 1, 1971. The lineal effect of fission provides a baseline of intergroup differentiation which is altered by forces leading to intragroup genetic change, the male migration effect and genetic drift. The importance of population dynamics for the distribution of alleles among subgroups of a population is recognized.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. II. Phenotypic,genetic, and environmental correlations between traits

The general lack of phenotypic correlation among skeletal nonmetric traits has been interpreted as indicating a lack of genetic correlation among these traits. Nonmetric traits scored on animals in the skeletal collection of rhesus macaques from Cayo Santiago are used to calculate phenotypic, genetic, and environmental correlations between traits. The results show that even when phenotypic correlations are low, there may be large, significant genetic correlations among these traits. The genetic correlation pattern suggests that genes which affect nonmetric trait variation act primarily at a local level in the cranium, even though there are genes with pleiotropic effects on skeletal nonmetric traits throughout the cranium. Environmental and phenotypic correlations do not show this neighborhood pattern of correlation.     

The timing of fission among free-ranging Rhesus monkeys

Behavioral observations were carried out on a large group of free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago from January 1968 to December 1969 and from October through December 1970. During this period, social group A divided. The 24-month study period can be classified into five stages which represent the different phases in the process of group fission. Two criteria for fission were established: the cessation of grooming between adult females of different sub-groups of the main group and the stabilization of the adult female population. The criteria were based on established information on group dynamics and inter-group behavior on Cayo Santiago. Several points became clear from the chronological analysis. Group fission is a long process. The duration of the process of fission and the specification of the season in which fission begins and is completed depends upon the definition applied. For purposes of this analysis, fission was defined as beginning with the onset of spatial fragmentation and corresponded to the initial part of the breeding season. The fission was completed during the breeding season. The duration of the process of fission was 18 months.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. I. Single trait heritabilities

The use of skeletal nonmetric traits in studies of biological relationships often involves the assumption that variation in these traits is genetic. Studies of nonmetric traits in human groups and in inbred strains of mice and rabbits have indicated a genetic component to nonmetric trait variation. Skeletons of animals with known matrilineage membership were obtained from the Cayo Santiago skeletal collection in order to obtain a direct estimate of the heritabilities of several nonmetric traits in the free-ranging population of rhesus macaques on Cayo Santiago. Falconer's (1965) method was used to calculate heritability. Heritability estimates range from zero to one, and half of them are greater than 0.5. This indicates that there is a considerable amount of genetic variation for these traits among the Cayo macaques. There is a significant tendency for traits scoring the number of foramina to have lower heritabilities than those scoring hyperstotic or hypostotic traits.     

Demographic components of gene frequency change in free-ranging macaques on Cayo Santiago

Gene frequency profiles from January 1973 to January 1977 for three polymorphic loci were examined in Cayo Santiago rhesus social groups. The effects of demographic components (i.e., births, deaths, immigrations, emigrations, and group fission and fusion) on total change in gene frequencies are assessed. Allelic frequencies at the carbonic anhydrase II, 6-phosphogluconate dehydrogenase, and transferrin loci were analyzed in four social groups. In the two groups that underwent fission and fusion during the study period, the timing of these processes was related to the largest short-term changes in gene frequences. However, immigration and emigration had the greatest effect on total change in gene frequency in all groups during the study period. The relative importance of births and deaths in producing gene frequency change varied among the social groups. These results suggest that the relative importance of the demographic components of gene frequency change in primate populations is determined by behavioral patterns and ecological conditions specific to the population considered.     

The genetic consequences of primate social organization: a review of macaques,baboons and vervet monkeys

Primates, as long-lived, iteroparous, socially complex mammals, offer the opportunity to assess the effects of behavior and demography on genetic structure. Because it is difficult to obtain tissue samples from wild primate populations, research in this area has largely been confined to terrestrial and semi-terrestrial old world monkeys (e.g., rhesus and Japanese macaques, vervets and several subspecies of baboons). However, these species display a multi-male, multi-female social structure commonly found in many other primate and non-primate mammals. Electrophoretic analyses of blood proteins from individually recognized and/or marked wild Himalayan rhesus monkeys, themselves the subject of long-term behavioral and demographic research, have begun to reveal the genetic consequences of such phenomena as social group fission, malelimited dispersion, non-consanguineous mating patterns, and agonistically defined male dominance.Specifically, rhesus social groups, consisting primarily of clusters of maternal relatives, appear to be nonrandom samples of a population's genotypes and genes. The genetic effects of social group fission are highly dependent on each group's size, demographic structure, and average degree of relatedness. In all cases fission contributes to the degree of intergroup genetic differentiation. Male-limited dispersion appears both to retard genetic differentiation between social groups and to lead to mating patterns that result in an avoidance of consanguinity. Groups, therefore, appear to be genetically outbred.Comparing these results with studies of other free-ranging or wild cercopithecines allows several generalizations: (a) genetic variation seems to be evenly distributed throughout each local population of multi-male social groups; (b) social groups, however, because they contain clusters of relatives, are distinctive in their specific frequencies of genes; (c) the degree of genetic differentiation between a population's social groups, because of the effects of social group fission and non-deterministic forms of male dispersal, is somewhat greater than expected on the basis of migration rates alone; and (d) the asymmetrical pattern of dispersion with respect to sex effectively precludes inbreeding in any one social group or the population as a whole. These observations have important implications for understanding the unusually rapid rates of evolution among the primates.     

Genetic aspects of migration in a rhesus monkey population

Gene frequency distributions in subdivided populations are affected by migration of individuals between groups. This paper considers the effects of such migration on blood protein allele frequency distributions in social groups of the Cayo Santiago rhesus macaque colony. Gene frequencies for complete social groups and their migrant and natal segments were analyzed at four points within a four year period in the colony's history. Gene frequencies varied between the migrant segments of different groups. Gene frequencies of migrant segments of particular groups also varied substantially with time. Usually, but not always, the presence of migrants in groups reduced the levels of inter-group gene frequency differentiation. We suggest that our findings are explained by a model in which the recruitment of immigrants into social groups is largely random with respect to individual genotypes. Such a model implies that migration contributes to both stochastic and directed changes in gene frequencies in rhesus and similarly substructured populations.     

Consequences of group fission for the patterns of relatedness among rhesus macaques

When mammalian social groups exceed their optimal size, they often tend to split. In view of the potential evolutionary benefits, it should be more advantageous for animals to stay with kin, rather than nonkin, during such fission events. In the present study, the spontaneous fission of two social groups, R and S, of rhesus macaques living on Cayo Santiago, Puerto Rico, provided the opportunity to compare the kinship structure of the corresponding parent and daughter groups, using information on both maternal and paternal relatedness. In both instances, maternal half-siblings and pairs of animals from the same family were significantly more prevalent in the fission products than in the parent group. During the split of group R, significantly more paternal half-siblings stayed in the remnants of the parent group than joined the seceding group. Our findings are compatible with previous behavioural studies demonstrating that female primates bias their social behaviour more to maternal than to paternal kin, but that both types of half-siblings prefer each other more than unrelated animals. It remains to be clarified by future research, however, whether the observed co-segregation of paternal half-sibs in our study reflects active choice or is a by-product of the group-specific kin structures, prior to fission.     

Body composition, age and fertility among free-ranging female rhesus macaques (Macaca mulatta)

The relationship of morphometric measures and birth status among 93 females on Cayo Santiago trapped during the 2001 and 2002 seasons was assessed. The proportion of females giving birth differed between the two seasons (0.58 vs. 0.38; P = 0.006) with a prominent decline among older females. Most morphometric measures increased from adolescent to adult groups, but bicep circumference showed a significant decrease among adults. When controlled for age differences, females with infants during the 2002 season exhibited greater bicep circumference, but no difference in abdominal fat than those without. Members of the socially dominant group did not have a higher rate of birth in either 2001 or 2002, despite being significantly longer and weighing more than those of the subordinate group. Abdominal skinfold and bicep circumference were significant predictors of birth status during the 2002 season, controlling for age group, social group membership, and parity in the previous year. Bicep circumference was also a significant predictor of birth status for the 2001 birth season. These findings suggest that individual variation in body composition among females of Cayo Santiago is associated with differences in fertility.     

Models for lineal effects in rhesus group fissions

Gene distributions in daughter groups produced by three rhesus monkey group fissions are analyzed. Data employed are for the Tf, 6PGD, and CA II electrophoretic marker systems in the fissions producing new daughter groups F and M, F and O, and J and N in the Cayo Santiago rhesus colony. Wide variations in FST values were observed among the different markers in the various fissions. Overall, the observed FST values exceeded predictions of simple random fissioning models. However, on average, observations on electrophoretic markers fitted well with predicted values from lineal fissioning models. One of these lineal fissioning models, a simulation, incorporated the propagation of alleles in the matrilines of the fissioning groups. The second, an algebraic expression, utilized group sizes and average kinship values as parameters.     

Behavioral responses of free-ranging rhesus monkeys to food shortage

During early July 1968, a severe food shortage occurred on Cayo Santiago, an island colony of free-ranging rhesus monkeys (Macaca mulatta). The food shortage produced striking changes in the behavior of the monkeys. Within the one social group intensively studied, the total frequencies of grooming, play and fights decreased significantly; the frequency of matings also dropped; body contact, displacements by other groups, and non-displacement movements decreased, but not in statistically significant amounts. Changes in the percentage of total grooming attributable to related and unrelated monkeys reflected the stability of the rhesus matriline. Comparisons made between Cayo Santiago and other primate groups under analogous situations reveal similar responses to food shortage.     

The Impact of Random and Lineal Fission on the Genetic Divergence of Small Human Groups: A Case Study among the Yanomama

Most of the genetic divergence that currently separates populations of Homo sapiens must have arisen during that long period when the local village (or band) was the basic unit of biological evolution. Studies of tribally intact Amerindian groups exhibiting such small-group organization have demonstrated marked genetic divergence between nearby villages. Some of this genetic radiation can be attributed to the effects of random genetic drift over time within these small demes. Some of it, however, might be better ascribed to the consequences of nonrandom genetic assortment at the time of village fission, a recurring event for such groups. Even random genetic assortment at the time of fission would lead to some genetic divergence, due to the finite size of the parent gene pool. We term the genetic consequences of random assortment the random fission effect. Routinely, village fission occurs along family lines, leading to even greater genetic divergence between the daughter villages. We use the term lineal fission effect to describe the genetic consequences of nonrandom assortment and contrast these results with those derived from random assortment.——A formal treatment of random and lineal fission effects is developed, first for the single-locus case, then for the multiple-locus extension. Using this formulation, three Yanomama fission events were examined. Fission in the Yanomama often involves a great deal of mutual hostility between the two factions, so that subsequent gene flow between the two daughter villages is minimal. The first two examples are typical of the Yanomama behavior norm, and are accompanied by a minimum of subsequent gene flow between the daughter villages. In these two cases, the observed divergence values are very large and are also very unlikely under random fission. The lineal fission effect is pronounced. The net impact of lineal fission is to reduce the effective size of the village at the time of fission by a factor of four, relative to expectation from random fission. The third example, however, involved an unusually amicable split of a village, followed by free genetic exchange between the fission products. This "friendly fission" yields an observed divergence value not much in excess of the expectation from random fission.—The long-term consequences of such fission bottlenecks in effective population size are discussed for both intra- and inter-tribal genetic diversity. It appears that the rate of genetic divergence for tribal and subtribal groups may have been somewhat greater than would be expected from classical drift arguments.     

Fission-fusion and lineal effect: aspects of the population structure of the Semai Senoi of Malaysia.

Analysis of histories and genealogies from seven relatively unacculturated, swidden-farming Semai settlements shows that the composition of local groups fluctuates through time. This instability is similar to a pattern which Neel and his colleagues have suggested is typical of primitive society, the fission-fusion model. In addition, the individuals comprising Semai fission groups are kinsmen which implies that the number of independent genomes represented is markedly less than the number of individual migrants (the lineal effect). Fission groups may form new villages or fuse with an established settlement. In either case, the genetic effects of such migration are more pronounced than would be expected on the basis of founder effect or random migration. Despite several conspicuous differences in social organization between the Semai and the South American Indians (e.g., bilateral vs. unilineal descent) whose population structure provided the empirical basis for the fission-fusion, lineal effect model, the basic similarities are striking. The Semai case thus lends support to the proposition that this pattern may be of some generality in technologically primitive populations.     

A study of intragroup biological change induced by social group fission in Macaca mulatta using discrete cranial traits

Eight discrete cranial traits are used as biological indicators to investigate the effect of social group fission on intragroup genetic change leading to intergroup differentiation in Macaca mulatta. The timing of discrete cranial trait frequency change and group fission coincide, indicating a possible causal relationship between fission and genetic change. A significant change in the male mating population during and after fission is proposed as the mechanism causing intragroup genetic change, along with the effects of fluctuations in segregation ratios.     

Blood group antigens and the population genetics of Macaca mulatta on Cayo Santiago. I. Genetic differentiation of social groups

The red blood cell phenotypes for eight polymorphic loci were determined for 293 free-ranging Macaca mulatta living on Cayo Santiago; this number represents the total population of the island, disposed in four social groups plus peripheral males. The rhesus population shows significant genetic heterogeneity over blood group systems (loci) and social groups. No particular genetic locus or social group is solely responsible for the genetic heterogeneity observed. The distributions of genotypes for two loci (G and H) do not deviate significantly from Hardy-Weinberg expectations within social groups or in the population as a whole. Correction of the equilibrium expectations for the effect of population subdivision yields no statistically significant results. Overall, the results suggest that the interaction of a variety of processes (random genetic drift, founder effect, migration and selection) may be responsible for the diversity observed. These data, combined with those from further studies, may allow an application of behavioral and genetic knowledge to the study of microevolutionary processes among nonhuman primates.     

SOME POPULATION GENETIC CONSEQUENCES OF COLONY FORMATION AND EXTINCTION: GENETIC CORRELATIONS WITHIN FOUNDING GROUPS

Extinction and recolonization in an island model affects genetic differentiation among subpopulations through a combination of sampling and mixing. We investigate the balance of these forces in a general model of population founding that predicts first the genetic variance among new groups and then the effect of these new groups on the total genetic variance among all populations. We allow for a broad range of types of mixing at the time of colonization and demonstrate the significant effects on differentiation from the probability of common origin of gametes (φ). We further demonstrate that kin-structured founding and inbreeding within populations can have a significant effect on the genetic variance among groups and use these results to make predictions about lineal fission and fusion of populations. These results show that population structure is critically affected by non-equilibrium dynamics and that the properties of new populations, especially founding number, probability of common origin, and kin structure, are vital in our understanding of genetic variation.     

Genetic studies of serum transferrins of free-ranging rhesus macaques of Cayo Santiago, Macaca mulatta (Zimmerman 1780)

Transferrin phenotypes of plasma from 687 semi-free-ranging Macaca mulatta living on Cayo Santiago, Puerto Rico, were determined by starch-gel electrophoresis and autoradiography. Fifteen phenotypes, homozygous or heterozygous products of six codominant autosomal alleles, were present in the population. The 687 animals, prior to March 1973, were divided into eight troops plus peripheral males. By March 1, 1973 the size of the population was reduced to 333 animals, consisting of four troops plus peripheral males. The distributions of transferrin phenotypes and allele frequencies were determined for the population of 687 animals and for 287 of the March 1973 population of 333 animals. Gametic ratios of 382 offspring of 126 females were enumerated. Statistical tests of homogeneity and equilibrium were applied to the data. The results of these tests suggest that, with only a few exceptions, the Cayo Santiago macaques, although divided into social groups, form a single population, and the results are in accord with behavioral observations. The authors suggest that the data on transferrins provide a good baseline for future genetic and ethological studies of evolutionary processes in a population of nonhuman primates.     

Social dominance and reproductive behavior in male rhesus monkeys

Altmann's model describing the relationship of social dominance to breeding behavior in some non-human primate species has been tested using data from the Cayo Santiago rhesus colony. Although some of the model's assumptions are clearly not met by field observations, a good fit is often found for groups containing relatively few sexually mature, non-pregnant females. It is suggested that genetic change could be rapid under conditions described by this model. It is estimated that a “beneficial mutation” could spread through all the breeding males in as little as six generations regardless of group size. The speed at which an allele can spread through the group is discussed in terms of the mean length of female receptivity.     

Healed fractures in Macaca mulatta: age, sex, and symmetry.

Previous studies utilizing series of wild-shot primates have suggested that there is an association between locomotor behavior, aggression and patterning of healed fractures. In this study, observations taken upon a series of 126 rhesus macaques which represent a total sample of a naturally occurring social group from Cayo Santiago, are used to reexamine the conclusions drawn from previous studies. As a control, a series of randomly collected rhesus skeletons from the same colony is examined. Major differences in pathology incidences by age, sex and laterality is indicated between the two groups. Possible explanation for cross-specific variability in fracture patterning are also considered.     

Variance in intrinsic rates of growth among free-ranging rhesus monkey groups

Differential rates of intrinsic growth for the population of Macaca mulatta on Cayo Santiago partitioned by social group and dominance rank of genealogies indicate that the potential for increase is not uniformly distributed throughout the population. In the period from 1973 to 1974, high-ranking genealogies were growing at a faster rate than low-ranking genealogies. Large differences in r among the social groups indicate the possible existence of demographic, genetic, or social differences between groups. A random resampling procedure was employed to assess the statistical significance of differences in the intrinsic rate of growth among the 5 natural social groups and the 3 partitions formed by, respectively, lumping members of high-, middle-, and low-ranking genealogies across several social groups. Comparisons among social groups shows that there are significant differences in the rate of growth between Group J and Group M, and between Group J and Group F for the period from 1973 to 1974. Among dominance ranks of genealogies, significant differences in r were found between the partitions of the high- and middle-ranking genealogies. These findings suggest that differential reproductive success is influenced and maintained by underlying variations in the distribution of behavioral traits in the population.