Carbonic anhydrase heterozygosity and FST distributions in Kenyan baboon troops.код для вставкиСкачать
Carbonic Anhydrase Heterozygosity and FSTDistributions in Kenyan Baboon Troops CAROLE OBER,' THOMAS J OLIVIER ' AND JOHN BUETTNER-JANUSCH ' Department ofAnthropology, Northwestern Uniuersrty, Euanston, Illinois 60201 and 'Department ofAnthropology, New York University, New York, N e u York 10003 K E Y WORDS Carbonic anhydrase Microevolution Migration Pupio - . Heterozygous advantage . ABSTRACT An analysis of the distribution of carbonic anhydrase alleles in troops of olive baboons, Pupio cynocephalus, is reported. In an earlier study (Olivier, T. J., J. Buettner-Janusch and V. Buettner-Janusch, 1974, Am. J. Phys. Anthrop., 41: 175-1901 the authors found a significant excess of heterozygotes with a large amount of intertroop differentiation a t the CA ZZ locus. If balancing selection is acting on the CA ZZ locus and maintaining a n excess of heterozygotes, then the degree of local differentiation observed a t this locus is unexpected. In this study the analyses of the CA Z and CA IZ data are extended and some idiosyncratic features of baboon population structure are considered. Nonidealized forms of behavior, such as adult male migration and other age-specific and sex-specific behaviors, may affect observed patterns of gene frequency distributions. The analysis reveals that the excess of heterozygotes a t the CA II locus is localized in the females only and that the males are highly differentiated among the troops. These findings suggest that a female-limited heterozygous advantage exists a t the CA ZZ locus in this baboon population. A computer simulation model, RAMBLE, further suggests that recurrent male migration between troops may explain the intertroop microdifferentiation found in primate populations. In an earlier study, we reported substantial microspatial variations in gene frequencies of neighboring troops of baboons (Olivier et al., '74). We described the distributions of carbonic anhydrase I and carbonic anhydrase I1 alleles in troops of olive baboons, Pupio cynocephulus, from the Laikipia District of Kenya (table 11. The troops studied were grouped in two clusters in a relatively small geographic area. In our previous analyses, the entire sample appeared to be in Hardy-Weinberg equilibrium a t the CA Z locus both before and after applying Wahlunds correction for subdivided populations. Homogeneity tests of the CA Z frequencies indicated the presence of statistically significant heterogeneities. We suggested t h a t migration and drift, acting approximately in accordance with Wright's island model (Wright, '31, '43,'651, were the major forces affecting the distribution of alleles at the CA Z locus. AM. J. PHYS. ANTHROP. (1978)48: 95-100 The frequencies of the alleles at the CA ZZ locus, however, were not as easily analyzed by stochastic models. When Wahlund's version of the Hardy-Weinberg model was applied to the CA I I data, a significant excess of CA I1 heterozygotes was found. Considered alone, the observed excess of heterozygotes could be taken as evidence supporting a balanced polymorphism model for the CA ZZ locus. However, if selection favoring heterozygotes is maintaining the polymorphism in this area of relatively small size, the gene frequencies should be stable throughout the area, a t or near a n equilibrium point (Cavalli-Sforza and Bodmer, '71). The equilibrium point will be determined by the fitnesses of the two homozygous classes relative to that of the favored heterozygote. Although we expected the gene frequencies to be stable throughout the area, we found significant intertroop differentiation for the CA 95 96 C. OBER, T. J. OLIVIER AND J . BUETTNER-JANUSCH TABLE 1 Frequencies of the common alleles at the CA I and CA I1 loci Frequency Troop CA la CA IP A B C D E F G H I J 0.76 0.91 ' 0.91 0.82 0.93 0.77 0.85 0.94 0.87 0.88 0.78 0.97 ' 0.90 0.82 0.88 0.72 0.48 0.57 0.77 0.79 p:- XniPi 0.86 0.79 0.0355 0.0995 In, FsT=V/$-$ Homogeneity X 2 (9d.f.) 32.96 P < 0.001 Hardy Weinberg with Wahlund's correction 0.04 X2 P > 0.95 ' Frequencies < < 97.75 0.001 11.64 0.001 differ slightly from 1974 analysis. see text for details. ZZ frequencies. The level of gene frequency differentiation a t the CA 11 locus is considerably greater than t h a t observed a t the CA I locus (table 1). Such large genetic microdifferentiation is difficult to reconcile with the proposition that there is balancing selection acting on the CA ZI locus; that is, how could the CA I1 polymorphism, one perhaps subject to heterozygous advantage or stabilizing selection, show such large microspatial variations in gene frequencies? Earlier (Olivier e t al., '74) we discussed various conflicting propositions to explain what we found, but we left the questions unresolved. We have become increasingly aware of the degrees to which primate social structures differ from the simple, idealized structures assumed in many population genetic models. In these models (Wright, '31, '43; Crow and Kimura, '70; Cavalli-Sforza and Bodmer, '71; Li, '76; Kimura and Weiss, '64) breeding population sizes are assumed to remain constant over time, and migration usually occurs in a regular, idealized fashion. Migrants are generally considered to represent a random sample of each local population. However, in many primate populations kinship-related patterns of behavior, periodic troop fissioning, and high levels of adult male-only migration occur regularly and probably influence the ob- served gene frequencies. Primate social behavior, potentially influential, is disregarded in most population genetic models and may be a major determinant of the patterns of gene frequency differentiation observed in some human and nonhuman primate groups. Therefore, we have extended the analysis of data on baboon carbonic anhydrase in an attempt to account for the age-specific and sex-specific behaviors t h a t may influence the distribution of alleles within baboon populations. We present the results of a further analysis of the carbonic anhydrase data emphasizing the distributions of levels of heterozygosity and gene frequency differentiation within the adults of ten troops of olive baboons. In addition, we discuss a computer simulation program, RAMBLE, that may be used to explain the observed distribution of gene frequency differentiation in this population. MATERIALS AND METHODS Population Genetic data for the CA Iand CA 11 loci for the adult males and adult females in ten troops of baboons were analyzed. The criteria used to assign ages to individual animals and male and female gene frequencies for each troop are reported in Olivier e t al. ('74). We encountered difficulties in assessing the troop membership of some animals while trapping troops B, E, and F. Several days after Troop B was trapped, a group of animals was trapped and bled a t another location. Many of these animals showed signs of having been bled previously and it was assumed that this group may have been part of Troop B. Most of the newly captured members of this group were bled and designated a s Troop BQ (Olivier, '72). In this paper, as in Olivier's ('72) study, data from Troop BQ were eliminated from the analysis because of the uncertainty of their status. However, in Olivier et al. ('74) BQ was considered a part of Troop B. Therefore, in this paper the gene frequencies for Troop B are slightly different from those reported in Olivier et al. ('74). Troops E and F, two distinct groups of baboons with overlapping home ranges, were trapped a t one site. Olivier ('72) treated these as separate troops. In a later paper (Olivier et al., '74) these groups were pooled and considered as a single troop (E, F) for the purpose of analysis. Because we are interested in finer levels of genetic structure within baboon troops, we have separated the samples from 97 HETEROZYGOSITY AND FST DISTRIBUTIONS groups E and F and treated them as separate troops, as was done by Olivier ('72) and Steinberg et al. ('77). Analysis Heterozygosity levels (No. heterozygoted N) for the C A IZ locus were calculated for each age/sex class to determine whether the overall excess of heterozygotes a t this locus was distributed evenly over all demographic groups. To test for an excess of heterozygotes against gene frequency-corrected expectations, proportions of genotypes expected in the adult male and adult female segments of the population were calculated for each troop using agespecific and sex-specific gene frequencies. We used a binomial probability function as in the Hardy-Weinberg model and assumed that the alleles within each age/sex class are combining randomly. Wahlund's correction for subdivision was applied to yield expected proportions of genotypes for the adult males and for the adult females in the population. To measure the degree to which the troops were differentiated, Wright's FST statistic (Wright, '65) was used as a standardized measure of gene frequency differentiation. These values are computed by the following equation: FST = V p(1- p) - 7, where V is the weighted variance of the frequency of one allele in a set of subpopulations and is the mean frequency of one allele among the troops. The utility of this equation in calculating standardized variances of gene frequencies within subdivided populations was first suggested by Wright 1'65); since then i t has been used frequently as a measure of genetic differentiation (Workman and Niswander, '70; Nee1 and Ward, '70; Lewontin and Krakauer, '73). To determine whether all agehex classes were equally differentiated, we calculated FsT values for the total sample and for the adult male and female components of each troop. A computer program, RAMBLE, was developed by one of us (T. J. 0.) t o test whether fluctuations in the composition of one portion of each troop (such as the adult males) could substantially affect FsT values for that portion of the population. In RAMBLE, 161 individuals with genotype counts identical to those we observed in the adult males at the CA I locus were assigned to ten model troops. FST values were recalculated after each set of ex- changes that might be conveniently taken as occurring during one generation. For baboons, this would be approximately five to seven years (Olivier e t al., '74). In RAMBLE, unweighted means and variances of gene frequencies are used in calculating FST values because we are interested in demonstrating the amount of fluctuation between consecutive generations which is due to male migration and subsequent changes in troop size. Weighted variances should have no effect on the overall degree of these fluctuations. The aim of this part of our analysis was to examine in isolation those fluctuations in FSTvalues for adult males that could occur simply as a result of recurrent male migration. In a future study we will examine the effects of various demographic parameters, such as the number of troops, migration rates, and population size on the distribution of FsT values over time. RESULTS Heterozygosity The observed proportions of females that are heterozygotes exceed the proportion of males that are heterozygotes in both the adult and nonadult classes in nine out or ten troops. The proportions of heterozygotes in the adult males and females are shown in table 2. In part, the higher heterozygosity in the females is attributable to the higher frequency of the rarer CA I1 allele in the females of each troop. An excess of heterozygotes is present among the adult females and no such excess is present in the adult males (table 3). The excess heterozygosity found in our earlier analysis of the CA IZ locus appears to be restricted to the females in this population. Gene frequency differentiation FST values calculated for the CA I locus are fairly homogeneous. They are 0.0355, 0.0484, and 0.0362 for the total troops, the adult females, and the adult males, respectively. At the CA II locus the total troop FsT is equal to 0.0995; this value is greater than any FST obtained for the CA I locus. However, the value for the adult females a t the CA 11 locus is 0.0829 while the adult males show an extremely high index of gene frequency differentiation, with FSTequal to 0.1942. It appears that the gene frequency differentiation found between troops a t the CA ZI locus is primarily a function of the extremely high differentiation found between the adult males of the different troops. 98 C. OBER. T. J. OLIVIER AND J. BUE'ITNER-JANUSCH - I 25 0 TIME i 1 50 75 GENERATIONS Fig. 1 Fluctuations in FSTvalues observed with the exchange of 100 migrants per generation as determined by RAMBLE (see text for details). The horizontal lines represent observed FST values for the adult males. TABLE 2 Adult male and adult female heterozygotes at the CA I I locus Adult 1.3 Adult dd Troop Hetero zygotes (N) A 6 B 0 C D 0 1 1 4 7 7 5 2 33 E F G H I J Total ' Totals dlffer slightly Total (Nl i%) 20 28 13 10 22 15 10 16 16 0.30 0.00 0.00 0.10 0.05 0.27 0.70 0.44 0.31 0.25 0.21 8 158 Total (N) Proportion iX) 16 3 6 11 2 7 4 17 14 13 93 I 39 29 15 18 9 17 9 22 25 21 204 I 0.41 0.10 0.40 0.61 0.22 0.41 0.44 0.77 0.56 0.62 0.46 from 1974 analysis. see text for details. TABLE 3 RAMBLE Genotype counts for adult male and adult females at the CA I I locus Two runs of 100 generations each were conducted. In the first, 40 migrants were exchanged within the set of 10 troops per generation; in the second, 100 migrants were exchanged. In both runs, large fluctuations in FSTvalues were observed. The mean FSTwith 40 migrants per generation was 0.0489, with a range of 0.1134 to 0.0138 and a variance of 0.000749. Figure 1illustrates the fluctuations observed with the exchange of 100 migrants per unit time in the population of 161 adult males. The mean Fsr here is 0.0537, with a IE Genotype CA IIa/CA IIa CA IIa/CA XIb CA Ilb/CA IIb P I Proporiion Hetero zygotes (N) Exp Obs Exp Obs Exp Obs ild (Nl (Nl 114.20 103 70.59 93 19.21 8 119.05 120 32.90 33 5.05 5 < 0.001 > 0.99 'Totals differ slightly from 1974 analysis, Bee text for details. HETEROZYGOSITY AND FST DISTRIBUTIONS range of 0.0099 to 0.0208, and a variance of 0.00121. This range fully encompasses the range of variation found for the adult male baboons between the CA 1 and CA II loci. DISCUSSION The localization of the excess heterozygotes in the females and the extremely high index of gene frequency differentiation in the adult males lead us to suggest that a sex-limited heterozygous advantage exists a t the CA Zl locus among female baboons and that the dynamics of the polymorphism among males are radically different. Although the hypothesis of sex-linked selection seems reasonable within a statistical framework, a physiological model is more difficult to construct. If heterozygosity a t a particular locus confers a selective advantage to females during gestation, but is selectively neutral all other times, female-limited heterozygous advantage may result. The exact role of carbonic anhydrase during pregnancy is largely unknown, however, it has been suggested that in mammals maternal carbonic anhydrase plays an important role during reproduction (Friedley and Rosen, '75), possibly because fetal red cells have been found to have little or no carbonic anhydrase activity (Meldrum and Roughton, '33; Berfenstam, '52, cited in Kirschbaum and DeHaven, '68). Until more is known about the physiology of maternal carbonic anhydrase activity, a mechanistic model for sex-limited balancing selection a t the CA ZZ locus in our baboon sample can only be speculative. In the adult male portion of the population construction of a specific model for the CA ZZ polymorphism is even more difficult. While it may be possible that variations in local selection pressures favoring one allele over the other could account for the observed differentiation, the geographical area in which the troops were trapped is so small that this explanation seems unreasonable. Alternatively, we can argue that random drift, a s in Wright's island model (Wright, '31, '43,'651, is responsible for our observations. However, with such a model an extraordinary degree of isolation between troops would be required to produce the differentiation we have found between adult males a t the CA ZZ locus. Such isolation is difficult to reconcile with our findings at the CA Z locus in the same groups and with recent behavioral reports on migration between baboon troops (Rowell, '69; Packer, '75). Indeed, we 99 expected initially that the adult males would be that least differentiated segment of the population due to such relatively high intertroop mobility. Behavioral observations of troops of cercopithecoid monkeys have indicated a wide range in the numbers of males that migrate between neighboring troops. While several earlier studies described negligible migration rates between baboon troops (DeVore, '65; DeVore and Hall, '651, more recent studies reported high frequencies of intertroop male migration. During eight years of observations of olive baboons, Packer ('75) recorded the exchange of adult males among seven troops. Of the 39 recognizable males who reached pubert y during his study, each migrated out of its natal troop. Approximately 252: of these were reported to have transferred troops more than once during the study. Rowell ('69) reported intertroop movement for 23 out of 25 known adult male olive baboons during five years of observations. The length of association of any one male with a particular troop varied from a few days to several years. Lindburg ('68) reported that one-third of the original adult male rhesus monkeys in India changed groups during 20 months of Observations. Koford ('66) described similar migration patterns for the Cay0 Santiago rhesus monkeys where relatively large indices of gene frequency differentiation have been reported (Duggleby, '77, '78) despite these large migration rates. Similar findings have been reported for some South American Indians where high levels of genetic microdifferentiation between neighboring villages have been observed (Arends e t al., '67; Chagnon, '74; Ward and Neel, '70). If, in fact, adult male baboons are a n unstable adjunct to a more permanent core, then Fs, values would fluctuate somewhat over time simply as a result of the random redistribution of these males. Behavioral observations (Rowell, '69; Packer, '75) suggest t h a t during one generation nearly 100%of the adult male baboons change their troop affiliation a t least once. Under these conditions, fluctuations in FSTvalues between consecutive generations in the adult males may be similar to those observed in the computer simulations program, RAMBLE. Therefore, large amounts of microdifferentiation could exist in the face of very high migration rates, as in the Cay0 Santiago macaque colony (Duggleby, '77, '78b) and in some South American Indian populations (Arends et al., '67; Chag- 100 C. OBER, T. J. OLIVIER AND J. BUE'ITNER-JANUSCH non, '74; Ward and Neel, '70). The difference in FSTvalues between the CA I and CA ZI loci in the adult male baboons may be a result of randomly fluctuating FsTvalues due to high levels of male mobility. The results of our analysis suggest that processes controlling distributions of alleles a t a single locus may vary among the different demographic components of a baboon troop and that the dynamics of a polymorphism within a troop may not be described by a single model. We suggest that gene frequency differentiation can exist in the face of high levels of interpopulation mobility and, in fact, random processes a t times may produce highly divergent FsT values for different independently segregating alleles in a set of small populations. In general, we feel that baboons and other primates have a complex internal genetic structure and this structure must be accounted for if microevolution in these species is to be understood. ACKNOWLEDGMENTS The authors thank Mrs. Wren Olivier for her extensive assistance in the collection of the baboon blood samples on which this study is based. We also thank Mr. Paul Zawa for assistance with calculations. 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