The Genetic Structure of a Tribal Population, the Yanomama Indians. Xv. Patterns Inferred by Autocorrelation Analysis

Fifteen allele frequencies have previously been determined for 50 villages of the Yanomama, an Amerindian tribe from southern Venezuela and northern Brazil. These frequencies were subjected to spatial autocorrelation analysis to investigate their population structure. There are significant spatial patterns for most allele frequencies. Clinical patterns, investigated by one-dimensional and directional spatial correlograms, were relatively few in number and were moderate in strength. Overall, however, there is a marked decline in genetic similarity with geographic distance. The results are compatible with a hierarchic population structure superimposed on the geography, and generated by a stochastic fission-fusion model of village propagation, followed by localized gene flow. Strong temporal autocorrelations of allele frequencies based on linguistic-historical distances representing time since divergence were also found. There appears to be a stronger relation between geography and linguistic-historical hierarchic subdivisions than between either feature and genetic distances. These findings confirm by different approaches the results of earlier analyses concerning the important roles of both stochastic and social factors in determining village allele frequencies and the occurrence within this tribe of some allele frequency clines most likely due to the operation of chance historical processes.     

Multivariate classification of human populations. I. Allocation of Yanomama indians to villages.

A set of 12 anthropometric measures and six genetic traits, available for 520 Yanomama Indians from 19 villages in nine clusters, were used to allocate individuals to villages. On the basis of anthropometrics alone, 36% of the individuals were allocated to the right village and 60% to the right cluster. On the basis of genetic traits alone, 16% were allocated to the right village and 26% to the right cluster. A combination of all 18 characters yielded 41% allocation to the right village and 63% to the right cluster. Of the 924 possible combinations of six anthropometric measures, only one provided poorer resolution than did the six genetic traits. We explain the better resolution of the anthropometric traits by noting that the anthropometric traits are not totally heritable and that genetic traits are not continuously distributed. Randomization studies indicated that all of the observed correct-allocation fractions are far in excess of random expectation. We infer that the village phenotype distributions overlap only partially, and that they represent real and substantial population differentiation.     

A Comparison of the Genetic Infrastructure of the Ye''Cuana and the Yanomama: A Likelihood Analysis of Genotypic Variation among Populations

A general procedure is described for measuring and testing population differences in gametic frequencies. The total dispersion among populations is subdivided in hierarchical fashion. The multiple-locus treatment is simply the sum of the single-locus analyses, provided gametic equilibrium obtains among the loci. In the event that gametic equilibrium does not obtain, correlations among loci need to be dealt with.—The analysis is then used to examine the genetic infrastructure of two Indian tribes from South America, the Ye'cuana (Makiritare) and the Yanomama. From historical evidence, we may identify several "clusters" of villages within each tribe. The demographic and cultural practices affecting village formation and the maintenance of peer integrity are rather different in these tribes, however, and lead us to postulate rather different patterns of genetic variation among villages. Analyses of five codominant two-allele loci, four dominant two-allele loci and two complex loci (with four codominant haplotypes each) demonstrate that Yanomama clusters are more disparate than Ye'cuana clusters, as would have been predicted on sociocultural grounds.     

The genetic structure of a tribal population, the Yanomama Indians XI. Gene frequencies for 10 blood groups and the ABH-Le secretor traits in the Yanomama and their neighbors; the uniqueness of the tribe.

In this paper we present the results of blood group typings for a total of 33 villages distributed among five South American Indian tribes--Yanomama (21 villages), Makiritare (eight villages), Macushi (two villages), Piaroa (one village), and Wapishana (one village). These new results for the Yanomama and Makiritare tribes have been combined with those previously reported to allow a better appreciation of the distribution of allelic frequencies in the tribes. The relationship of the Yanomama to other South American Indian tribes is investigated using data on six polymorphic loci (Rh, MNS, Fy, Jk, Di, Hp). By use of four genetic measures (two of genetic relationship and two of genetic diversity), we demonstrate that the Yanomama are genetically unique among a sample of 20 South American tribes. In addition, the Yanomama show somewhat less genetic diversity for the six loci analyzed than the average South American tribe. Taken together, these results indicate a rather long period of isolation for the population antecedent to the Yanomama--perhaps since the time of entry of man into the South American continent. The pattern of genetic relationships and genetic diversity for the 20 tribes is consistent with the hypothesis that evolution in South America proceeded by a process of fission-fusion leading to isolation of subpopulations with subsequent genetic differentiation as a consequence of population isolation. The uniqueness of the Yanomama appears to stem entirely from such a process, there being no evidence of any selective differential for the loci analyzed.     

Intertribal gene flow between the Ye'cuana and Yanomama: genetic analysis of an admixed village

Genetic exchange with a neighboring village of Ye'cuana Indians had introduced two alleles, Dia and ACPa, into the Yanomama Indian Village of Borabuk. After several generations, these alleles had reached frequencies of 0.08 and 0.10, respectively. These frequencies are puzzling because they are higher in Borabuk than in the Ye'cuana village from which they were derived. Single allele estimates of ancestral proportions obtained from either of these traits are biologically unrealistic and suggest that admixture is not a good explanation for genetic variation in Borabuk. Nevertheless, multiallelic admixture models are seen to produce credible estimates of ancestral proportions and to explain a large amount of allele frequency variation in Borabuk. When these results are compared with expectations derived froma formal pedigree analysis, good agreement is seen. Comparison of single allele estimates of ancestral proportions obtained from alleles at 11 loci, with multiallelic estimates obtained from the same 11 loci and with the pedigree-derived estimates, demonstrates the superiority of the multiallelic approach.     

The influence of cultural factors on the demography and pattern of gene flow from the Makiritare to the Yanomama Indians

A single village of Yanomama Indians was found to have frequencies of Di^a of 0.06 and of Ap^a of 0.08, in contrast to 40 other villages whereDi^a was absent and Ap^a quite rare. The source of these genes was identified as a village of Makiritare Indians, but the two allele frequencies were approximately the same or even higher in the Yanomama than in the Makiritare village. Demographic, social and cultural parameters affecting marriage and reproduction in the two tribes explain this. Genealogical relationships and informants' accounts collected in the field, when viewed against the traditional marriage practices, reproductive advantages of headmen, and differential treatment of captured women, indicate that the mating and reproduction parameters inherent in tribal social organization of this kind constitute an essential part of the explanation of the genetic findings. It is argued that mating systems of this sort are such that the probability of a new gene introduced by a captive surviving in the recipient population is a function of the sex of the initial carrier. The implications for tribalization and potentially radical changes in allele frequencies are briefly explored by considering aspects of settlement pattern and population fissioning known to characterize the tribes in question. Finally, it is shown that genetic sampling from a single location can and does result in unrepresentative allele frequencies when this single sample is taken to characterize the tribe as a whole.     

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.     

Multivariate Analysis of Gametic Disequilibrium in the Yanomama

The gametic disequilibria between all possible pairs of loci were examined for a set of eight codominant loci in each of fifty Yanomama villages, using a multivariate correlation analysis which reduces the results to a single measure of departure from multiple-locus-gametic equilibrium. Thirty-two of the fifty villages departed significantly from multiple-locus gametic equilibrium. The largest contributions to the departure from multiple-locus equilibrium were due to the disequilibria between MN and Ss and between Rh(Cc) and Rh(Ee), indicating the effects of tight linkage. After removing the effects of these obvious sources of disequilibrium, sixteen of the fifty villages still remained significantly out of equilibrium. The disequilibrium between any particular pair of loci was highly erratic from village to village, and (with the exception of the MN-Ss and Cc-Ee disequilibria) averaged out very close to zero overall, suggesting a lack of systematic forces (epistatic selection). The departure from equilibrium in any one village is in excess of that expected from random sampling alone, and is attributed primarily to the fission-fusion mode of village formation operative in the Yanomama and the fact that a single village consists of a few extended lineages. Village allele frequencies are highly correlated across loci, and most of the non-independence is accounted for by large correlations in the average allelic frequencies of different loci for related villages. It is suggested that these correlations also are due to territorial expansion and population growth. For the tribe as a whole, all but the tightly linked markers of the MNSs and Rh complexes are approximately uncorrelated, and large departures from multiple-locus Hardy-Weinberg expectation are primarily due to substantial Wahlund variance within the tribe. There is no need to postulate a role for selection in these disequilibria.     

Esterase D in South American Indians.

Significant variation in the frequency of Esterase D isoenzymes was found in 1,070 individuals belonging to eight South American Indian tribes. The Es D1 allele shows frequencies varying from .36 to 1. A region of low prevalence of this allele seems to exist in northern Brazil, involving the Parakanan, Gorotire, and Krahó. The intratribal variation observed in eight Yanomama villages located in Brazil was not exceptional.     

The genetic structure of a tribal population, the Yanomama indians. VII. Anthropometric differences among Yanomama villages

Anthropometric data on 12 variables in 19 villages of the Yanomama Indians demonstrate significant heterogeneity in physique among villages of this tribe. Mahalanobis' distances (D²) calculated from the data lead to the tentative conclusion of a general correspondence between anthropometric and geographic distances separating villages. The mean stature of the Yanomama is smaller than that of most other South American tribes which have been measured, and the Yanomama are genetically distinct from the other small Indians as shown by genetic distances based on allele frequencies for a variety of genetic markers. Since some subjects were measured more than once by the same and by different observers, it was possible to calculate approximate estimates of variance within and between observers. Univariate analysis indicates that face height and nose height are especially susceptible to systematic differences in technique between observers. The variances obtained in this field study compare favorably with those of some classical laboratory studies described in the literature. It was found that measurement error nevertheless probably makes a substantial contribution to anthropometric distance between villages. The median error variance as a fraction of that of Herskovits ('30) is 0.62 for the seven measurements in common with this study. The median value of the error variance for the 12 variables in this study is between 16% and 17% of the total variance.     

The Genetic Structure of a Tribal Population, the Yanomama Indians. VI. Analysis by F-Statistics (Including a Comparison with the Makiritare and Xavante

The infra-structure of three relatively undisturbed tribes of American Indians (Yanomama, Makiritare, Xavante) has been investigated by means of the F-statistics of Wright, using 8, 9 and 6 codominant systems respectively. The data for the first two mentioned tribes are much more extensive (37 and 7 villages) than for the third (3 villages), and much of the argument is based on the first two. An additive model partitioning F(IS) into an average effect (F(A)) and deviations due to deme size, systems effects, village effects, and random error has been employed. The Cannings-Edwards formulation suggests that the small size of the demes alone would result in an F(IS) of -0.008 for the Yanomama and -0.007 for the Makiritare. There is no evidence for significant village or systems effects. Despite considerable scatter, F(A) values are not significantly heterogeneous and tend to be negative (-0.012 to -0.023). On the basis of a computer simulation model, it appears that there is an excess of consanguineous marriage over random expectation, i.e. the negative F(A) values are probably not due to avoidance of close inbreeding in a subdivided population in which demes are small. Aspects of population structure which could contribute to negative F(A) values are identified. These include unequal gene frequencies in the sexes and occasional marked differential fertility. It is at this point unnecessary to introduce overdominance as a cause of the negative F(A) values, since a computer simulation program which does not incorporate selection satisfactorily reproduces the observed F(IS) values. If population breeding structure alone can result in negative F(IS) values, then this may constitute a mechanism for retarding random fixation.-Mean F(ST) values are 0.063 for the Yanomama and 0.036 for the Makiritare. While truly comparable data are lacking, it seems likely these will be found to be relatively high values for human populations. F(IT) values have been calculated by both direct and indirect approaches. The direct approach yields a value of 0.045 for the Yanomama and -0.009 for the Makiritare; the respective indirect values are 0.085 and 0.017. The primary identifiable reason for this difference between tribes is the greater genetic heterogeneity among Yanomama villages. The assumptions underlying the indirect approach to the calculation of F(IT) do not appear to be met in these populations.     

On methods of spatial analysis for genotyped individuals

Spatial autocorrelation methods have commonly been applied to individual-based spatial genetic studies, although their properties and the relations among the statistics have not been carefully examined. This paper first introduces a reformulation of widely used spatial statistics using point processes. When Moran's I statistics are applied to allele frequencies within an individual, the frequencies are no longer continuous variables but have only three discrete values and specific interpretations of Moran's I statistics and the number of alleles in common (NAC) can be expressed as the weighted sum of join-count statistics. The distributions of minor genotypes are amplified in Moran's I depending on the allele frequency in the population, while NAC uses a constant weighting system. Under the point process framework, spatial analysis can be conducted on the common theoretical base, from individual locations to genetic distributions of different levels, (for example, genotype and allele). The methodology is demonstrated by application to field data for molecular ecological studies of Fagus crenata population dynamics.     

Dialect Discrimination by Male Orange-Tufted Sunbirds (Nectarinia osea): Reactions to Own vs. Neighbor Dialects

Male orange-tufted sunbirds ( Nectarinia osea ) exhibit distinct song dialects throughout Israel. Recently, two distinct local dialects with a sharp boundary were discovered in a small (1.5 km²) urban neighborhood densely inhabited by 63 territorial sunbird pairs. We conducted playback experiments to determine song dialect discrimination capability by sunbird males in this neighborhood. Males of both dialects responded significantly more strongly to playback of their own dialect than to that of the adjacent dialect. In spite of the extreme proximity between the two dialect areas, we found no effect of distance to the neighboring dialect on the intensity of any the behavioral responses. We suggest that due to the complex acoustic properties of this urban neighborhood, sunbirds are extremely limited in the number of neighboring males they can assess to establish what the local song is. A stronger response to one's own dialect is therefore expected, and we discuss how local dialects could be maintained via this mechanism regardless of the very small distances between territories and dialect populations.     

Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat,Rattus fuscipes

Dispersal is a fundamental process that influences the response of species to landscape change and habitat fragmentation. In an attempt to better understand dispersal in the Australian bush rat, Rattus fuscipes, we have combined a new multilocus autocorrelation method with hypervariable microsatellite genetic markers to investigate fine-scale (< or = 1 km) patterns of spatial distribution and spatial genetic structure. The study was conducted across eight trapping transects at four sites, with a total of 270 animals sampled. Spatial autocorrelation analysis of bush rat distribution revealed that, in general, animals occurred in groups or clusters of higher density (< or = 200 m across), with intervening gaps or lower density areas. Spatial genetic autocorrelation analysis, based on seven hypervariable microsatellite loci (He = 0.8) with a total of 80 alleles, revealed a consistent pattern of significant positive local genetic structure. This genetic pattern was consistent for all transects, and for adults and sub-adults, males and females. By testing for autocorrelation at multiple scales from 10 to 800 m we found that the extent of detectable positive spatial genetic structure exceeded 500 m. Further analyses detected significantly weaker spatial genetic structure in males compared with females, but no significant differences were detected between adults and sub adults. Results from Mantel tests and hierarchical AMOVA further support the conclusion that the distribution of bush rat genotypes is not random at the scale of our study. Instead, proximate bush rats are more genetically alike than more distant animals. We conclude that in bush rats, gene flow per generation is sufficiently restricted to generate the strong positive signal of local spatial genetic structure. Although our results are consistent with field data on animal movement, including the reported tendency for males to move further than females, we provide the first evidence for restricted gene flow in bush rats. Our study appears to be the first microsatellite-based study of fine-scale genetic variation in small mammals and the first to report consistent positive local genetic structure across sites, age-classes, and sexes. The combination of new forms of autocorrelation analyses, hypervariable genetic markers and fine-scale analysis (< 1 km) may thus offer new evolutionary insights that are overlooked by more traditional larger scaled (> 10 km) population genetic studies.     

Local spatial autocorrelation map of ovine proteins in Europe

Local spatial autocorrelation (SA) is used to analyse six blood protein polymorphisms: haemoglobin, albumin, esterase A, carbonic anhydrase, protein-X and transferrin from 26 European ovine populations. Local SA is a useful technique for exploring the distribution of ovine allele frequencies and identifying hotspots (localities with positive local SA) and coldspots (negative local SA). The local SA map of joint analysis reveals that there are areas of significant protein heterogeneity in Europe.     

VOCAL DIALECTS AND THE STRUCTURE OF GEOGRAPHIC VARIATION IN MORPHOLOGICAL AND ALLOZYMIC CHARACTERS IN THE RUFOUS-COLLARED SPARROW,ZONOTRICHIA CAPENSIS

The geographical patterns of variation shown at 20 allozyme and non-enzymatic protein-coding loci, in 8 external, and in 12 skeletal morphological characters in the rufous-collared sparrow, Zonotrichia capensis, were analyzed in order to test the local (genetic) adaptation hypothesis regarding the origin and maintenance of vocal dialects in birds. Approximately 20 males were collected from each of four sites within each of six different dialect zones. There was significant variability in both external and skeletal morphology among all 24 sites and among dialect groups. Average Wright's corrected fixation coefficient (F_ST) was 0.118, indicating significant genetic differentiation among all sites, regardless of dialect. Hierarchical F statistics indicated that only 50% of among site variability was due to a dialect effect. Puna dialect sites were highly differentiated from all other sites with respect to both morphology (external and skeletal measures) and allozyme frequencies. Heterogeneity at the PGM-1 locus among puna scrub sites was the major cause of the high average F_ST across all sites, and within the puna scrub dialect. Average genetic differentiation among non-puna sites (F_ST = 0.018) was similar to differentiation among sites within each of the five non-puna dialect groups (mean F_ST = 0.0132 ± 0.0069). Hierarchical F statistics indicated that none of the among-site differentiation in this subset of samples was due to a dialect effect. These observations are not consistent with the local adaptation hypothesis. All significant genetic heterogeneity occurred among sites in mountainous habitats, and we suggest that topography and patchiness of habitat may have been major factors involved in population differentiation, rather than vocal dialects.     

The Genetic Structure of a Tribal Population, the Yanomama Indians. Xiv. Clines and Their Interpretation

The Yanomama Indians are a South American tribe distributed over an irregular area approximately 200 x 300 miles. The gene frequencies observed at 12 loci in 47 villages within this area have been analyzed for the occurrence of clines. Apparently significant clines are observed for alleles of the Rh, MNSs, Kidd, Gm, Inv and serum albumin system. Available data concerning recent tribal expansion and admixture permit a tentative analysis of the causes of these clines. Although the action of selection cannot be rigorously excluded, it seems unlikely to be the major cause. Admixture with surrounding tribes plays a role which can be quantified because of the fortuitous circumstance of two genetic markers for admixture. It is suggested that an important factor in the origin of these clines is the manner in which the tribe has recently expanded through successive village fissionings and a predominantly centrifugal pattern of village migration.     

Fission Models of Population Variability

Most models in population genetics are models of allele frequency, making implicit or explicit assumptions of equilibrium or constant population size. In recent papers, we have attempted to develop more appropriate models for the analysis of rare variant data in South American Indian tribes; these are branching process models for the total number of replicates of a variant allele. The spatial distribution of a variant may convey information about its history and characteristics, and this paper extends previous models to take this factor into consideration. A model of fission into subdivisions is superimposed on the previous branching process, and variation between subdivisions is considered. The case where fission is nonrandom and the locations of like alleles are initially positively associated, as would happen were a tribal cluster or village to split on familial lines, is also analyzed. The statistics developed are applied to Yanomama Indian data on rare genetic variants. Due to insufficient time depth, no definitive new inferences can be drawn, but the analysis shows that this model provides results consistent with previous conclusions, and demonstrates the general type of question that may be answered by the approach taken here. In particular, striking confirmation of a higher-than-average growth rate, and hence smaller-than-previously-estimated age, is obtained for the Yan2 serum albumen variant.     

Differences among Yanomama Indian villages: Do the patterns of allele frequencies,anthropometrics and map locations correspond?

In order to determine the degree of correspondence between sets of multivariate observations based on different kinds of traits, two new methods, derived from fundamentally different notions of “correspondence,” are adopted here and compared. Using networks or trees to represent contemporary relationships, the first method tests the similarity of the cluster or hierarchic structures implicit in two sets of data. The second approach tests the departure from perfect geometric congruence or superimposability. Computer simulation was used to generate the distributions needed for significance tests under the null hypothesis. By the first technique, we find significant correspondence among the cluster structures for geographic, allele frequency, and anthropometric data on 19 Yanomama Indian villages. The results are similar and more precise for a subset consisting of seven villages. Some of these results differ from the conclusions which would be reached with the conventional correlations based upon entries in distance tables. The direct test of congruence, used only for the data on the subset of seven villages, gives results which differ substantially from those based on cluster-structure. There are, however, similarities between the measure of congruence and the simple correlations based on entries in the distance tables. The significant correspondences observed call for some explanation. Cultural and demographic features determine the particular non-random allocation of individuals to village fragments when a village splits. These social phenomena are invoked in tentative explanation of the agreement among historical, biological, and geographic relationships of villages.     

Fine scale genetic structure in the wild ancestor of maize (Zea mays ssp. parviglumis)

Analysis of fine scale genetic structure in continuous populations of outcrossing plant species has traditionally been limited by the availability of sufficient markers. We used a set of 468 SNPs to characterize fine‐scale genetic structure within and between two dense stands of the wild ancestor of maize, teosinte (Zea mays ssp. parviglumis). Our analyses confirmed that teosinte is highly outcrossing and showed little population structure over short distances. We found that the two populations were clearly genetically differentiated, although the actual level of differentiation was low. Spatial autocorrelation of relatedness was observed within both sites but was somewhat stronger in one of the populations. Using principal component analysis, we found evidence for significant local differentiation in the population with stronger spatial autocorrelation. This differentiation was associated with pronounced shifts in the first two principal components along the field. These shifts corresponded to changes in allele frequencies, potentially due to local topographical features. There was little evidence for selection at individual loci as a contributing factor to differentiation. Our results demonstrate that significant local differentiation may, but need not, co‐occur with spatial autocorrelation of relatedness. The present study represents one of the most detailed analyses of local genetic structure to date and provides a benchmark for future studies dealing with fine scale patterns of genetic diversity in natural plant populations.