* Department of Animal and Human Biology, University "La Sapienza," Rome, Italy
Institute of Legal Medicine, Catholic University, Rome, Italy
Department of Oncology and Neurosciences and Center for Research and Training on Cancer in Sub-Saharan Africa, University G.d'Annunzio, Chieti, Italy
Department of Ethology, Ecology and Evolution, University of Pisa, Italy
Correspondence: E-mail: destrobisol{at}uniroma1.it.
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Abstract |
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Key Words: sub-Saharan Africa food producers hunter-gatherers mtDNA Y chromosome sociocultural factors
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Introduction |
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The study by Seielstad, Minch, and Cavalli-Sforza (1998) may be regarded as the pioneer study on the relations between genetic variation of unilinearly transmitted polymorphisms and sociocultural factors. In this worldwide analysis of mtDNA and Y-chromosome polymorphisms, the authors observed that the interpopulation differentiation was much higher for the Y chromosome than for mtDNA. Applying an island migration model (Cavalli-Sforza and Bodmer 1971), they obtained a ratio between female and male Nwhich approximates to the product of the effective population size per migration rateclose to 8 (7.96). According to Seielstad, Minch, and Cavalli-Sforza (1998), the higher female to male migration rate associated with the widespread habit of patrilocality may account for most of this difference. The study paved the way for further investigations that substantially confirmed the importance of the social structure in shaping the genetic variation of human populations (e.g. Oota et al. 2001).
In a study recently published in Molecular Biology and Evolution, Hammer et al. (2001) analyzed 43 biallelic polymorphisms of the nonrecombining portion of the Y chromosome in a total of 50 human populations that included five populations from sub-Saharan Africa (Bagandans, East Bantus, Gambians, Khoisan, and Pygmies). These authors obtained a st of 0.251 for sub-Saharan Africans, a value that is sligthly smaller than that obtained for Asians (0.271). They also noted that this finding contrasts with previous estimates for mtDNA (Melton et al. 1997), in which the
st value for sub-Saharan Africans (0.339) largely exceeds those of Europeans (0.045) and Asians (0.009). Hammer et al. (2001) suggested that the relatively small interpopulational variation of Y chromosome among sub-Saharans could be caused by a male-biased gene flow during the expansion of populations speaking Bantu languages. This interpretation is supported by the widespread distribution of haplotype 15 in Bantu-speaking populations (Hg E3a according to the nomenclature suggested by the Y Chromosome Consortium [2002]) and by nested cladistic analysis. Thus, according to Hammer et al. (2001), sub-Saharan Africa might represent another case in which the genetic structure of human populations has been shaped by the greater mobility of males (Mesa et al. 2000; Carvajal-Carmona et al. 2000; Oota et al. 2001), in contrast with what was observed at the worldwide level (Seielstad, Minch, and Cavalli-Sforza 1998; Stoneking 1998). Interestingly, the conclusion drawn by Hammer et al. (2001) also differs from what was observed by Seielstad, Minch, and Cavalli-Sforza. (1998) in another group of African populations. These authors analyzed 14 populations from Eastern and Central Africa and observed that within-population variance for autosomal microsatellite was higher than variance for Y-chromosomal microsatellites. The data set includes populations from Sudan (Beja), Ethiopia (Konso, Tsamako, Ongota, Hamar, Dasenech, Surma, Nyangatom, Bench, and Majangir), and Mali (Dogon, Peulh, Tuareg, and Songhai). According to Seielstad, Minch, and Cavalli-Sforza (1998), this evidence fits the expectation of a higher female than male migration rate and is consistent with the patrilocal habit of most sub-Saharan populations.
The discrepancy between the conclusions drawn by Seielstad, Minch, and Cavalli-Sforza (1998) and Hammer et al. (2001) suggests that sub-Saharan populations analyzed in these two studies differ for variation of maternal and paternal lineages and/or for sex-linked migration rates. A substantial difference between the data sets used by the two studies lies in the fact that Seielstad, Minch, and Cavalli-Sforza (1998) analyzed only populations that can be considered food producers (food-producer populations [FPPs]), that is, agriculturalists and pastoralists, whereas Hammer et al. (2001) also surveyed populations with a traditional economy based on hunting and gathering (hunter-gatherer populations [HGPs], Pygmies and !Kung). Although based primarily on the type of subsistence economy, the distinction between FPPs and HGPs is important from a genetic point of view. In fact, FPPs and HGPs differ in their social structure in three specific aspects that may have important effects on variation of male and female lineages. First, the level of polyginy is higher among FPPs than among HGPs (Cavalli-Sforza 1986a). Second, exceptions to patrilocality have been described for HGPs but not for FPPs (Bahuchet 1999; Biesele and Royal 1999). Third, sociocultural barriers strongly influence the way in which unions between individuals of the two groups take place (see below). Therefore, an investigation of the relations between sociocultural factors and genetic variation may be very useful to better understand the mechanisms driving the genetic structure of sub-Saharan populations and to define more precisely the role of culture in determining the diversity within and between groups.
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Materials and Methods |
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Laboratory and Data Analyses
The genetic systems considered include the hypervariable region-1 (HVR-1, from np 16024 to 16384) of mtDNA, six Y-chromosomal microsatellites (DYS19, 389I, 390, 391, 392, and 393), and haplogroups of the mtDNA and Y chromosome built by use of unique evolutionary events. Sequencing of the HVR-1 (between positions 16024 and 16384) and Y-chromosomal microsatellite typing for Bakaka, Bassa, and Fulbe were carried out as previously described (Caglià et al. 2003; Destro-Bisol et al. 2004). MtDNA sequences were assigned to the phylogenetic tree of Salas et al. (2002).
Parameters of within-population (haplotype diversity and mean number of pairwise comparisons), between-population, and among-population diversity (Fst and st) were calculated by the Arlequin software (Schneider et al. 1997). The N
parameter (which incorporates effective size, migration, and mutation) was calculated by application of the formula N
= (1/Fst) 1, according to the island model of migration for haploid systems (Cavalli-Sforza and Bodmer 1971). Because the contribution of mutation rate to the N
parameter in our genetic systems may be considered negligible, the fluctuations of N
values have been assumed to be the result of differences in migration rate and/or effective population size among populations (see also Wjisman [1984] and Seielstad, Minch, and Cavalli-Sforza [1998]). The Kimura two-parameter (Kimura 1980) and Rst (Slatkin 1995) methods were used to calculate the genetic distances for HVR-1 of mtDNA and Y-chromosome microsatellites, respectively. To visualize the genetic relationships among the groups examined, we analyzed the genetic distance matrices by the nonmetric multidimensional scaling method (MDS [Kruskal 1964]) in the Statistica version 5.0 software.
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Results |
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Discussion |
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Once the robustness of the initial results had been tested, our next logical step was to discuss the microevolutionary processes underlying the different patterns of mitochondrial and Y-chromosomal variation of FPPs and HGPs. To this end, we built a model (fig. 2) that integrates demographic and genetic aspects and incorporates ethnographic knowledge, especially knowledge of African pygmies.
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Another important consequence of the meeting between HGPs and FPPs is their reciprocal gene flow. No substantial taboos or social barriers existed between HGPs and FPPs during the early stages of contact. The two groups to probably exchanged genes symmetrically, an assumption supported by the similarity of anthropometric characters between the Twa Konda (pygmies) and Oto Konda (farmers) of Central Africa (Cavalli-Sforza 1986b). However, the present-day situation indicates that this initial condition changed considerably, and an asymmetric gene flow progressively developed between HGPs and FPPs because of the establishment of sociocultural inequalities (Cavalli-Sforza 1986b). In fact, pygmy women are accepted as wives by Bantu communities, first, because they are famed for their great fertility, and, secondly, because the future husband must pay a relatively low "bride price" to the wife's family to gain the right to marriage. These conditions make a pygmy-to-Bantu flow of maternal lineages possible. A Bantu-to-pygmy flow of paternal lineages is also expected through three mechanisms: first, extramarital unions between pygmy females and Bantu-speaking males, second, adoption of orphans born from mixed unions, and, third, a return to the HGPs of Pygmy women and of their children after the divorce from Bantu-speaking FPP males. On the other hand, both the pygmy-to-Bantu flow of paternal lineages and the Bantu-to-pygmy flow of maternal lineages are inhibited by sociocultural taboos against unions between Bantu-speaking females and Pygmy males (Cavalli-Sforza 1986b). The resulting asymmetric gene flow has left a signature in both pygmies and Bantu speakers, but it must have had a deeper impact on the genetic structure of the latter because of their smaller population size. This asymmetric gene flow between FPPs and HGPs probably affected the gene flow between HGP subpopulations as well. In fact, the females of pygmy groups in which mixed unions with Bantu speakers occur more frequently are less available for marriages with males from other pygmy subgroups (Biasutti 1967). This circumstance is another factor that could have contributed to the high level of genetic differentiation observed for mtDNA among HGPs.
Different levels of poligyny and patrilocality in FPPs and HGPs are other factors probably involved in the differences observed between the two groups. By decreasing the male effective size, polyginy decreases diversity of paternal lineages within populations and increases that among populations. Polyginy is known to be substantially higher among FPPs than among HGPs, both in terms of proportion of polygamists and in terms of average number of wives per polygamist (Cavalli-Sforza 1986a; Biesele and Royal 1999). Furthermore, whereas all FPPs practice a rigid patrilocality, some HGPs do not exclusively follow such social behavior. Among the Aka pygmies, a grouping that includes the Biaka and Mbenzele pygmies analyzed here, the young couple generally settles in the husband's camp after the birth of the first child. However, the husband may remain in the wife's community, where he may be joined by one of his brothers or sisters (Bahuchet 1999). Among some !Kung groups of Botswana, males often join the wife's family (Biesele and Royal 1999). Interestingly, a high level of polygyny and extreme patrilocality have been proposed as probable causes of the low Y-chromosome and high mtDNA diversity observed in West New Guinea populations (Kayser et al. 2003).
Apart from being consistent with the results described above and providing an explanation for the discrepancy between the conclusions of Seielstad, Minch, and Cavalli-Sforza (1998) and Hammer et al. (2001), this model predicts the existence of phylogeographic traces of a sex-biased gene flow between HGPs and FPPs. The existence of a sex-biased gene flow is supported by the distribution of the most-common haplogroups in FPPs and HGPs. Haplogroup E3a is the modal Y-chromosome type in FPP neighbors of HGPs; frequencies range from 42% (Wairak from Tanzania [Luis et al. 2004]) to 96% (Bamileke from Cameroon [Cruciani et al. 2002]). E3a has been indicated as a signature of Bantu expansion (Underhill et al. 2001). It is present in all HGPs, where it ranges from 5% among the Ju/'hoansi !Kung (recalculated from Underhill et al. [2001] by Knight et al. [2003]), who are known to have intermarried with Bantu-speakers to a low degree, to 65% among the Biaka pygmies (Cruciani et al. 2002). The haplogroup E2b1x (E2b1a) is also probably associated with the Bantu expansion (Cruciani et al. 2002). It reaches a frequency of 15% among southern African Bantu and 6% in the !Kung (Underhill et al. 2001; Cruciani et al. 2002). Furthermore, most of the other Y-chromosome types observed among HGPs are absent among FPPs ([A3b1, A2, B2a*, B2b2, B2b4b, B2b*x(B2b3*), B2b3a] [Cruciani et al. 2002]), with two exceptions. The first exception is represented by haplogroups B2a1 and B2b3*x(B2b3a) (both occur at a frequency of 5% among Biaka pygmies [Cruciani et al. 2002]), which, together with the other haplogroups that belong to the group II of Underhill et al. (2001), is thought to be the remnant of early diversification and dispersal processes within Africa (Underhill et al. 2001; Cruciani et al. 2002). The second exception is provided by the haplogroup E3b*x(E3b1, E3b2, and E3b3), which is found only among !Kung from southern Africa (with a frequency of 11%) and in geographically distant populations such as Ethiopian Jews and Mossi from Burkina Faso (Cruciani et al. 2002). Therefore, the instances of haplogroup sharing mentioned above seem to be the result of the maintenance of ancestral characteristics diluted elsewhere by more recent demographic events rather than reverse gene flow (from HGPs to FPPs). On the other hand, the analysis of mtDNA haplogroup distribution show quite a different pattern. Western pygmy and !Kung have two different mtDNA modal types, L1c1a1 (60% among the Mbenzele pygmies and 30% among the Biaka pygmies [Destro-Bisol et al. 2004]) and L1d (frequency of 51% to 96% among !Kung: recalculated by Destro-Bisol et al. [2004] from Chen et al. [2000]). This substantial heterogeneity between pygmies and !Kung illustrates their long reciprocal isolation. These two mtDNA types have probably originated among pygmies and !Kung (Destro-Bisol et al. 2004; Salas et al. 2002) and are also present in some FPP neighbors of HGPs. The L1c1a1 is found among Ewondo (frequency of 13% [Destro-Bisol et al. 2004]), whereas the L1d is present among Mozambicans (frequency of 5% [Salas et al. 2002]). Some signatures of reverse gene flow (from FPPs to HGPs for maternal lineages) are also detectable in the mtDNA haplogroups of probable Bantu origin present both in the HGPs and in their FPP neighbors (L1a2, L1a1a, L3d3, and L3e2b [Pereira et al. 2001; Salas et al. 2002]). This finding is indicated by the cumulative frequency of the haplogroups mentioned above, which ranges from 0% (Botswana !Kung [Vigilant et al. 1991]) to 19% (South African !Kung [Chen et al. 2000]), with intermediate values of 4% among the Mbenzele (Destro-Bisol et al. 2004) and 18% among the Biaka (Vigilant et al. 1991). This indication of introgression of FPP maternal lineages into HGPs is not in contrast with the asymmetric gene flow predicted by our model. In fact, the cumulative frequency of the Bantu mtDNA haplogroups is substantially lower than the frequency of the E3a haplogroups in the same HGPs (from 39% in the !Kung to 65% in the Biaka [Cruciani et al. 2002]).
The evidence that the differential gene flow of paternal lineages has left a stronger signature than the differential gene flow of maternal lineages merits some further considerations. This difference may be seen on two different levels. First, haplogroups bearing the M2 mutation have been observed among all the HGPs analyzed so far, whereas the L1c1a1 and L1d haplogroups have only been found in some FPPs. Second, at present, no clear signs of reverse gene flow exists for Y chromosome (from HGPs to FPPs), whereas such signs do exist for mtDNA (from FPPs to HGPs). This discrepancy can be explained by the substantial difference in size between FPPs and HGPs. In the case of paternal lineages, the signs of the FPP-to-HGP gene flow are more evident and persistent because of the smaller size of recipient populations. Furthermore, the smaller size of HGPs could have facilitated the retention of FPP maternal lineages acquired during the initial period of symmetric gene flow. On the other hand, the larger size of the FPPs has probably diluted the signs of the HGP-to-FPP gene flow of Y chromosomes that probably occurred in the initial phase of contact between the two population groups.
Another important implication of our model is in the differential pressure of microevolutionary forces on maternal and paternal lineages of HGPs and FPPs. In fact, because of the combined effect of asymmetric gene flow and different levels of polyginy and patrilocality, the model predicts that genetic drift had been more effective on maternal than on paternal lineages of HGPs, whereas gene flow is expected to be the prevailing microevolutionary force on their paternal lineages. The opposite situation is expected for FPPs. Consequently, HGPs should show a higher intrapopulational diversity for paternal than for maternal lineages, whereas the opposite should be valid for FPPs. To test these expectations, we compared HVR-1 mtDNA and Y-chromosome microsatellite haplotype diversity in the same populations for both genetic systems. From this comparison, we found that HGPs show the lowest level of haplotype diversity for mtDNA but nearly the highest for the Y chromosome (fig. 3). Furthermore, the difference in the ratio of mtDNA HVR-1 to Y-chromosome microsatellite haplotype diversity between HGPs and FPPs is statistically significant by the Mann-Whitney U test (P = 0.011). Therefore, our results seem to reflect a substantial difference between FPPs and HGPs concerning the degree of patrilocality and polyginy, which is so far suggested by only a few, nonsystematic anthropological studies (Cavalli-Sforza 1986a; Bahuchet 1999; Biesele and Royal 1999).
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Conclusion |
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Supplementary Material |
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Acknowledgements |
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Footnotes |
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