Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Evolutionary Responses to a Constructed Niche: Ancient Mesoamericans as a Model of Gene-Culture Coevolution

  • Tábita Hünemeier,

    Affiliation Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil

  • Carlos Eduardo Guerra Amorim,

    Affiliation Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil

  • Soledad Azevedo,

    Affiliation Centro Nacional Patagónico, CONICET, U9120ACV, Puerto Madryn, Argentina

  • Veronica Contini,

    Affiliation Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil

  • Víctor Acuña-Alonzo,

    Affiliation Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia, Mexico City, Mexico

  • Francisco Rothhammer,

    Affiliations Programa de Genética Humana, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Santiago, Chile, Instituto de Alta Investigación, Universidad de Tarapacá, Arica, Chile

  • Jean-Michel Dugoujon,

    Affiliation Laboratoire d′Anthropologie Moléculaire et d′Imagerie de Synthèse, UMR 5288 CNRS, Université Paul Sabatier (Toulouse3), Toulouse, France

  • Stephane Mazières,

    Affiliation Anthropologie Bio-culturelle, Droit, Ethique et Santé (ADES), UMR 7268, Aix-Marseille-Université/CNRS/EFS, Marseille, France

  • Ramiro Barrantes,

    Affiliation Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica

  • María Teresa Villarreal-Molina,

    Affiliation Laboratorio de Genómica de Enfermedades Cardiovasculares, Instituto Nacional de Medicina Genómica, Mexico City, Mexico

  • Vanessa Rodrigues Paixão-Côrtes,

    Affiliation Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil

  • Francisco M. Salzano,

    Affiliation Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil

  • Samuel Canizales-Quinteros,

    Affiliations Unit of Molecular Biology and Genomic Medicine, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico, Departamento de Biología, Facultad de Química, Universidad Nacional Autónoma de México, Mexico City, Mexico

  • Andres Ruiz-Linares,

    Affiliation The Galton Laboratory, Department of Biology, University College London, London, United Kingdom

  • Maria Cátira Bortolini

    maria.bortolini@ufrgs.br

    Affiliation Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil

Evolutionary Responses to a Constructed Niche: Ancient Mesoamericans as a Model of Gene-Culture Coevolution

  • Tábita Hünemeier, 
  • Carlos Eduardo Guerra Amorim, 
  • Soledad Azevedo, 
  • Veronica Contini, 
  • Víctor Acuña-Alonzo, 
  • Francisco Rothhammer, 
  • Jean-Michel Dugoujon, 
  • Stephane Mazières, 
  • Ramiro Barrantes, 
  • María Teresa Villarreal-Molina
PLOS
x

Correction

10 Jul 2012: Hünemeier T, Amorim CEG, Azevedo S, Contini V, Acuña-Alonzo V, et al. (2012) Correction: Evolutionary Responses to a Constructed Niche: Ancient Mesoamericans as a Model of Gene-Culture Coevolution. PLOS ONE 7(7): 10.1371/annotation/c648ffaa-47da-45e4-9cde-ef2f4c95ce29. https://doi.org/10.1371/annotation/c648ffaa-47da-45e4-9cde-ef2f4c95ce29 View correction

Abstract

Culture and genetics rely on two distinct but not isolated transmission systems. Cultural processes may change the human selective environment and thereby affect which individuals survive and reproduce. Here, we evaluated whether the modes of subsistence in Native American populations and the frequencies of the ABCA1*Arg230Cys polymorphism were correlated. Further, we examined whether the evolutionary consequences of the agriculturally constructed niche in Mesoamerica could be considered as a gene-culture coevolution model. For this purpose, we genotyped 229 individuals affiliated with 19 Native American populations and added data for 41 other Native American groups (n = 1905) to the analysis. In combination with the SNP cluster of a neutral region, this dataset was then used to unravel the scenario involved in 230Cys evolutionary history. The estimated age of 230Cys is compatible with its origin occurring in the American continent. The correlation of its frequencies with the archeological data on Zea pollen in Mesoamerica/Central America, the neutral coalescent simulations, and the FST-based natural selection analysis suggest that maize domestication was the driving force in the increase in the frequencies of 230Cys in this region. These results may represent the first example of a gene-culture coevolution involving an autochthonous American allele.

Introduction

Human cultural practices have drastically modified environmental conditions and behaviors, promoting rapid and substantial genomic changes often associated with positive selection and adaptation (gene-culture dynamics [1], [2]). In the history of Homo sapiens sapiens, a particularly important event that triggered a new and striking gene-culture-coevolution cycle was the development of agriculture and animal domestication during the Neolithic period (∼10,000 years ago). Further, the human gene-culture coevolution mediated by the domestication of plants and animals has been argued to provide some of the clearest and most spectacular examples of niche construction. The Niche Construction Theory can be defined as a branch of evolutionary biology that emphasizes on the ability of organisms to modify the pressure of natural selection in their environment and thereby act as co-directors of their own evolution, as well as that of other directly associated species [3][6].

Although more than 100 regions/genes had been identified as the likely targets of recent positive selection resulting from cultural pressures in newly constructed niches [1], well-documented examples are scarce. One of the best-known cases of gene-culture coevolution is lactase persistence (LP; the ability of adult humans to digest the lactose found in fresh milk) and dairying. High frequencies of LP are generally observed in traditional pastoralist populations. For example, LP reaches ∼64% in Beni Amir pastoralists from Sudan, whereas its frequency in a neighboring non-pastoralist community is only ∼20%. In Europe, LP varies from 15–54% in eastern and southern regions, 62–86% in central and western regions, and 89–96% in northern regions [5], [7][13]. Multiple independent mutations have been associated with this characteristic, some of which are located in an intron of the MCM6 gene, a region fundamental to lactase expression [5], [14]. The alleles that led to lactose persistence in Europe, such as MCM6 13,910*T, first underwent selection among dairying farmers around 7,500 years ago, possibly in association with the dissemination of the Neolithic Linearbandkeramik culture over Central Europe [13]. The high copy number variation of the amylase gene and the spread of the corresponding alleles in agricultural societies are another well-studied example [7], [8], [11], [15], [16]. Additionally, the West African Kwa-speaking agriculturalists cut and clear the forest to grow yams, increasing the amount of standing water after rain, therefore providing better breeding grounds for malaria-carrying mosquitoes [1] favoring the HbS allele, which confers protection against malaria in heterozygous individuals [17].

America was the last continent colonized by modern humans in prehistoric times. In less than 15,000 years before present (YBP), these first migrants had to adapt to an immensely wide variety of environments. In some regions during this evolutionary trajectory, as in Mesoamerica and the Andes, hunter-gatherer/forager societies gave rise to agriculturalist and urban communities, while others remained with a hunter-gatherer/forager subsistence system until the time of contact with Europeans or even until the present day. Thus, studies with Native American populations can provide useful information for better understanding gene-culture coevolution and the niche construction processes.

Based on studies with blood groups and other classical genetic polymorphisms, J. V. Neel and F. M. Salzano were pioneers in identifying complex population processes highly dependent on cultural factors in Native Americans (e.g., fission-fusion dynamic; [18]). Other examples are related to the coevolution of genes and languages [19], [20], but only two more recently reported examples might be associated with positive selection: (1) Tovo-Rodrigues et al. [21] investigated the distribution of D4 dopamine receptor (DRD4) alleles in several South Amerindian populations and found a significant difference in the allelic distributions between hunter-gatherers and agriculturalists, with an increase of the 7R allele among the former; and (2) Acuña-Alonzo et al. [22] showed that the 230Cys allele (Arg230Cys, rs9282541) of the ATP-binding cassette transporter A1 (ABCA1) gene, which was previously associated with low HDL-cholesterol levels and obesity-related comorbidities, was exclusively present in Native American and mestizo individuals. These authors verified that cells expressing the ABCA1*230Cys allele showed a 27% cholesterol efflux reduction, confirming that this Native American autochthonous variant has a functional effect in vitro. Other investigations have shown that the presence of ABCA1*230Cys explains almost 4% of the variation in plasma HDL-C concentrations in Mexican admixed populations [23]. This variation in HDL-C concentration was the highest one associated with a single nucleotide polymorphism (SNP) among different continental populations in these genome-wide association studies, corroborating its functionality [23].

Acuña-Alonzo et al. [22] demonstrated that 230Cys resides in a haplotype that was the target of an ongoing directional selective sweep, suggesting that 230Cys conferred an advantage during periods of food deprivation in the past. On the other hand, under the current modern lifestyle, 230Cys may have become a major susceptibility allele for low HDL levels and has been correlated with metabolic diseases [22]. This study provides an example of the “thrifty” genotype hypothesis, which postulates that variants that increase the efficiency of energy use and storage during periods of famine would have been positively selected in prehistoric times but can be associated with diseases of affluence in contemporary societies, where food is usually abundant [24].

Here, we expand the investigations of the Arg230Cys polymorphism in Native Americans and integrate the thrifty genotype concept with the gene-culture coevolution process, considering the human ability to create new ecological niches that may lead to the selection of genetic variants.

Materials and Methods

(a) Populations

New data for the Arg230Cys polymorphism were generated for 19 Amerindian populations (n = 229) from Meso/Central America and South America (Table 1). Additional information about these tribes can be found in Bortolini et al. [25], [26], Wang et al. [27], and Mazières et al. [28], [29]. These new Arg230Cys data were then analyzed together with those of an earlier published report [22], providing a total of 1905 investigated individuals. One hundred and twenty-six individuals of our sample were also previously genotyped for ∼680,000 SNPs using Illumina Human 610-Quad BeadChips(Ruiz-Linares et al., unpublished data), and a part of this information was used in some of our analyses. The populations were clustered according to their geographical location and ancient mode of subsistence as follows: (1) Mesoamerican agriculturalists, (2) Andean agriculturalists, and (3) South American hunter-gatherers/foragers. Of course, caution is needed regarding this classification, since subsistence modes are not stable over time and may not be unique. However, the two categories adopted here (agriculturalists and hunter-gatherers/foragers) represent general pre-Colombian subsistence conditions, providing a starting point for research related to gene-culture dynamics in Native Americans.

thumbnail
Table 1. Genotypes, allele frequencies, and geographic locations of the Native American populations investigated.

https://doi.org/10.1371/journal.pone.0038862.t001

Ethical approval for the present study was provided by the Brazilian National Ethics Commission (CONEP Resolution no. 123/98) for the Brazilian samples, as well as by ethics committee of: (a) Universidad de Antioquia, Medellin, Colombia (Colombian samples); (b) Universidad Nacional Autónoma de México, Ciudad de México, México (Mexican samples); (c) Universidad de Costa Rica, San José, Costa Rica (Costa Rican and Panamanian samples); (d) Universidad of Chile, Santiago, Chile (Chilean samples); (e) Université Paul Sabatier Toulouse 3, Toulouse, France (Bolivian and French Guianian samples). Individual and tribal informed oral consent was obtained from all participants, since they were illiterate, and they were obtained according to the Helsinki Declaration. The ethics committees approved the oral consent procedure as well as the use of these samples in population and evolutionary studies.

(b) SNP Genotyping and Intra- and Inter-subdivision Structures

The Arg230Cys polymorphism was genotyped using TaqMan assays (ABI Prism 7900HT Sequence Detection System; Applied Biosystems). Allele frequencies were obtained by direct counting. The level of the population structure observed within and between Mesoamerican agriculturalist, Andean agriculturalist, and South American hunter-gatherer/forager groups was estimated using F statistics and the Arlequin 3.5.1 software [30]. Allele frequencies were compared between the 3 population subdivisions with the student’s t-test (alfa  = 0.05) using the R Stats package (R Development Core Team; http://www.R-project.org/).

(c) Allele Age and Neutrality/selection Tests

A large Asian and Native American sample, including the 126 individuals investigated here, were genotyped for a major panel of ∼680,000 SNPs (Ruiz-Linares et al., unpublished data). Based on this additional information (Tables S1, S2 and S3), the following analyses were performed:

(c.1) ABCA1*230Cys allele age.

Since estimates of allele age depend on assumptions about demographic history and natural selection, we have performed two approaches to estimate the age of the variant allele:

  1. Kimura and Ohta [31] were the first to consider the relations between allele age and its frequency. With this purpose they developed the equation E(t1)  =  [−2p/(1−p)]ln(p), where E(t1)  =  expected age, time is measured in units of 2N generations, and p  =  population frequency [31]. For ABCA1*230Cys, we considered the average of frequencies of all populations and only those from Mesoamerica/Central America (p = 9.6 and 15.4, respectively; Table 1). A generation time of 25 years and N = 720 (number of generation considering the upper limit for the peopling of America, 18,000 YBP [32]) were assumed.
  2. Slatkin and Rannala [33] began to exploit Linkage Disequilibrium (LD) to estimate allele ages, based on variation among different copies of the same allele, where the age of an allele is estimated by the intra-allelic variation following the LD exponential decay due to recombination and mutation rates. Rannala and Reeve [34], on the other hand, explored the use of LD to map genes, as well as to obtain the allele age using a Markov Chain Monte Carlo framework. We applied this method to obtain a second ABCA1*230Cys age estimative using the DMLE+ v2.2 software (http://www.dmle.org). This program allows a Bayesian inference of the mutation age using an intra-allelic coalescent model to assess LD across the nineteen SNPs that occur around ABCA1*230 (rs2065412, rs2515601, rs2472386, rs2274873, rs2487054, rs4149290, rs2487039, rs2472384, rs2253174, rs2230806, rs2230805, rs2249891, rs4149281, rs4743764, rs1929841, rs2000069, rs2275542, rs3904998, and rs4149268). Taken into account the historical information about our sampled populations, three parameters were introduced: (a) Generation time of 25 years; (b) Proportion of population growth of 0.005; and (c) Proportion of population sampled of 0.0002. The program was run in the haplotype mode using two million of iterations.

(c.2) Test to detect deviations from neutrality.

Based on the long-range haplotype test [35] and integrated haplotype scores [9], [36] Acuña-Alonzo et al. [22] suggested that the autochthonous Native American ABCA1*230Cys allele could have been positively selected. However, demographic events, population structure, and other stochastic processes can create complex patterns in the genome, obscuring signals of natural selection or mimicking adaptive processes [37]. Additionally, positive and balancing selections show different effects on the genetic diversity patterns within and between populations [38]. Therefore, we performed additional analyses to explore these issues and elucidate the factors responsible for the eventual effect of natural selection on the ABCA1*230 locus.

To detect loci under selection, we used a method that contrasted the observed population differentiation (FST) with that generated for a null simulated distribution under a hierarchical island model using a coalescent approach. In this model, demes exchange more migrants within groups than between groups to generate the joint distribution of genetic diversity within and between populations [38]. Thus, a p value can be estimated from the joint distribution for the population heterozygosity (He) and FST using a kernel density estimation procedure [30]. The analysis was performed using Arlequin 3.5.1 in consideration of 126 Native Americans whose results for the ABCA1*230 locus were known. Data from 20 other autosomal SNPs (rs6559725, rs11140096, rs4877767, rs4014024, rs11140109, rs7872891, rs7850633, rs17086298, rs10746709, rs5014093, rs10868019, rs11140116, rs3860938, rs3860941, rs4097644, rs9942844, rs12551103, rs7863524, rs4877785, and rs70439590) from these same individuals were compiled from a major SNP panel (Table S2). These 20 additional SNPs were selected based on their location (chromosome 9: from position 85252250 to 85317359) inside the putative neutral region, defined by Schroeder and colleagues [39], which comprises ∼76,000 bp around the D9S1120 locus. Using this database (Table S2 and Figure S1), we were able to evaluate whether the joint distribution of the observed He and FST for the ABCA1*230 polymorphism data departed from the expected outcome at neutrality. Fifty thousand coalescent simulations were performed with a 100-demes island model. Four comparative analyses were conducted: (1) Mesoamerican agriculturalists (n = 68) vs. Andean agriculturalists (n = 35), (2) Mesoamerican agriculturalists vs. South American hunter-gatherers/foragers (n = 23), (3) Mesoamerican agriculturalists vs. South Americans (agriculturalists + hunter-gatherers/foragers), and (4) Andean agriculturalists vs. South American hunter-gatherer/foragers.

In addition, we simulated 100,000 neutral genealogies for a region containing two distinct sets of 20 biallelic markers under demographic scenarios mimicking the settlement of the Americas [32], [40]. To accomplish these simulations, we used the msABC software [41], a modification of ms software [42] that uses the coalescent to generate samples under a neutral Wright-Fisher model. The demographic parameters included: (1) a current effective population size of 830 individuals [40], a number not very different from that used in the simulations of Schroeder et al. [39]; (2) three demes that corresponded to the sampled subdivisions (Mesoamerican agriculturalists, Andean agriculturalists, South American hunter-gatherers/foragers); (3) a single ancestral population that existed from 6,350 to 18,000 YBP [32], [40]; and (4) different exponential growth rates to include the possibility of an ancestral population of 70 to 830 individuals (i.e., constant population size [40]).

The genetic diversity obtained in the simulations–summarized by intra- (heterozygosity) and interpopulation (global and pairwise FST) statistics–was compared to the observed genetic diversity of two genetic datasets: (1) that of the ABCA1*230 locus plus the same 19 flanking SNPs listed in item c.1; (Table S3), and (2) the same 20 SNPs mentioned in section c.2 (Table S2; Figure S1). The summary statistics calculated for each simulation (S vectors) were then compared to the summary statistics of the observed data (S* vectors) using an Euclidean distance measure ∂  =  ||S-S*|| with the ABCestimator software, implemented with the ABCtoolbox [43]. The rationale of the analysis was to check which observed dataset could be reproduced with higher fidelity among the range of neutral simulations.

(d) Allele Frequencies vs. Maize Domestication

Genetic, archeological, botanical, and paleoecological data furnished evidence that maize (Zea mays ssp. mays) had a single domestication origin from the wild grass teosinte (Zea mays ssp. parviglumis) in the Río Balsas region, southwestern Mexico, approximately 6,300–10,000 calendar years before present [44][53]. Pollen samples taken from sediments in lakes, swamps, and archeological deposits have provided evidence for the presence or absence of Zea (maize and/or teosinte) in the Americas and have been used to estimate the age of maize domestication and dispersion [44]. Blake [44] summarized the Zea pollen dates from several American archeological sites, and we selected this data set to perform our analysis. To test the connection between maize culture and the ABCA1*230Cys variant, we used allele frequencies from Mesoamerica/Central America populations (Zapotec, Maya, Nahuatl,Kaqchikel-Quiche, Totonac, Cabecar, and Guaymí) as well as Zea pollen dates obtained in archeological sites located geographically near these populations (Table 2). Spearman rank order correlations between the two data sets (Zea pollen archeological records and ABCA1*230Cys allele frequencies) were obtained using the Statistica 7.0 software (StatSoft, Inc©).

thumbnail
Table 2. Zea pollen relics ages and 230Cys*ABCA1 populations frequencies used for the regression analysis.

https://doi.org/10.1371/journal.pone.0038862.t002

Results

SNP Genotyping and Intra- and Inter-group Structures

Table 1 presents the genotype and allele frequencies for the 1905 individuals analyzed, including the new samples genotyped in the present study. A molecular analysis of variance (AMOVA) test was performed to quantify the level of population structure observed within and between the 3 subdivisions adopted here (Mesoamerican agriculturalists, Andean agriculturalists, and South American hunter-gatherer/forager; Table 1). A significant difference was observed between the subdivisions (FCT  = 0.036; p = 0.000). On the other hand, the highest FST among populations within subdivisions was observed in the South American hunter-gatherers/foragers (0.053; p = 0.005), and a value 5 times lower was found among Mesoamerican agriculturalists (0.013; p = 0.008); no sign of structuration was found in the Andes area (p = 0.36).

No significant differences in allelic frequencies were found when subsistence modes (hunter-gatherer/foragers vs. agriculturalists) were compared using the student’s t-test (p = 0.1316; Table 1). However, significant differences were observed between Mesoamerican agriculturalists and Andean agriculturalists or South American hunter-gatherers/foragers (p = 0.0022 and p = 0.0174, respectively). A comparison of South American hunter-gatherers/foragers and Andean agriculturalists revealed no significant differences (p = 0.351).

(c.1) ABCA1*230Cys allele age.

The ABCA1*230Cys allele age estimates, using population frequency information, were 12,097 YBP and 19,409 YBP, considering data from all populations and only those from Mesoamerica/Central America, respectively. But the allele age obtained using the observed LD and a Bayesian approach, is relatively younger, 7,540 YBP, with a posterior probability of 99%. Although the numbers generated with these two distinct methods are compatible with an American origin of the ABCA1*230Cys allele [32], the last seems more realistic since methods based on LD, rather than frequencies, have the property of reflecting what happened to an allele more accurately [33]. Discrepancies between estimates obtained from these two approaches are usually taken as evidence that selection has increased the frequency of the allele to higher levels than expected by random genetic drift [33], [54].

(c.2) Detecting candidate loci for selection.

Patterns of genetic diversity between populations can be used to detect loci under selection [30]. The joint distributions of He and FST of the ABCA1*230 locus and 20 other SNPs (listed in item c.2 in the Materials and Methods section) were examined to test whether the ABCA1*230 locus and these SNPs departed from neutral expectation. The values obtained indicated that only the ABCA1*230 polymorphism departed significantly from neutral expectation (p = 0.02; Figure 1). However, when the comparisons excluded the Mesoamericans (e.g., Andean agriculturalists vs. South American hunter-gatherer/forager subdivisions), no significant departure from the expected under neutrality was found (data not shown). These results suggest that the ABCA1*230 allele frequencies in Mesoamerica are incompatible with a simple neutral model.

thumbnail
Figure 1. Plot of the joint FST and He distributions for the Mesoamerican agriculturalist versus South American (agriculturalists + hunter-gatherer/foraging) groups.

Each dot indicates a SNP (listed in item c.2 in the Materials and Methods section). The lines represent confidence intervals. Only the ABCA1 locus showed significance at the 5% level (filled blue circle). Five selected SNPs were not plotted in the figure because of monomorphic sites in all subdivisions, missing data, and/or dot superposition.

https://doi.org/10.1371/journal.pone.0038862.g001

Our neutral demographic simulation analysis showed results in the same direction. The region containing the ABCA1*230 polymorphism and 19 flanking SNPs presented a slightly lower average heterozygosity than the putative neutral region dataset (0.32 vs. 0.34 respectively); but global and pairwise FST were higher for the ABCA1 region (global FST 0.03 vs. 0.01; average pairwise FST 0.05 vs. 0.01). Considering that both genomic regions were studied using the same quantity of markers and the same sampling strategy, in populations that were subjected to the same demographic history, the observed differences may occur due to diverse factors, one of them being natural selection. To test this hypothesis each dataset, summarized by the above-mentioned statistics, was also compared to each of 100,000 neutral simulations by means of Euclidian distances. The empirical dataset containing the ABCA1*230 polymorphism presented a poorer fit to neutrality than the putative neutral region dataset, showing Euclidian distances that were twofold higher than those of the neutral simulations (70.64 vs. 35.12). Interestingly, when the Mesoamerican agriculturalist subdivision was excluded from the analysis, this difference dramatically decreased (45.80 vs. 35.12). Thus, the poor fit to neutrality observed at the ABCA1*230 site and its flanking regions may be associated with the genetic pattern found in Mesoamerica.

(d) Allele frequencies vs. maize domestication.

A significant correlation was observed between the ABCA1*230Cys allele frequencies and the distribution of the Zea pollen relics in Mesoamerica (Figure 2; r = 0.9, p = 0.002). It is important to note that the populations used in the correlation analysis performed here (Zapotec, Maya, Nahuatl, Kaqchikel-Quiche, Totonac, Guaymí, and Cabecar) were investigated for microsatellites and other genetic markers in previous studies conducted by our and other groups [27], [55], [56]. These studies indicated that these populations have a substantial Amerindian substrate, a generally small European contribution, and almost no African influence. For instance, Wang et al. [27] showed that the Maya and Guaymí showed the highest and the lowest numbers of individuals with some level of recent European and African admixture, respectively. This indicates an opposite trend from what would be expected if the level of admixture with non-Indians was influencing our findings, since the variant allele is absent in Europeans and Africans.

thumbnail
Figure 2. ABCA1*230Cys frequencies versus radiocarbon ages of maize domestication (Zea pollen relics; Blake [42]).

Spearman’s rho value  = 0.936975 and p = 0.0019.

https://doi.org/10.1371/journal.pone.0038862.g002

Discussion

We can now examine some hypotheses in an attempt to explain the results and to draw the evolutionary scenario associated with the pattern of diversity of the ABCA1* Arg230Cys polymorphism.

Maize is considered the most important native crop of the Americas [44][53]. Several lines of evidence indicate that the Mesoamerican village lifestyle began with maize domestication [44], [45], [49][51], [57], [58]. Originating in the Mexican southwestern lowlands, maize journeyed southwards, traveling hand-in-hand with pottery and bringing sedentary life to the Andes, although the date of its entry, as well as the dispersion pattern of this crop into and throughout South America, remain controversial [52].

Other crops were also present in the pre-Columbian Mesoamerican civilizations (squash and beans; [50], [59]), but maize was the dietary base for most of these civilizations. For example, Benedict and Steggerda [60] showed that 75% of the calories consumed by the Mayas were derived from maize. In addition, Mesoamerica was the only region in the world where an ancient civilization lacked a domesticated herbivore. Therefore, protein from domesticated animal sources would have been scarce in Pre-Hispanic Mesoamerica in comparison to other parts of the ancient urbanized world, including the Andes [61]. As a whole, these studies demonstrated that the diet of the first Mesoamerican sedentary communities was extremely dependent on maize. These early farmers, however, suffered periods of plantation loss, questioning the common assumption that farming and sedentary lifestyle brought increased dietary stability and health homeostasis [62]. Several studies have revealed that homeostasis should have declined with sedentary farming, and bioarcheologists and paleopathologists have also detected a deterioration in Mesoamerican health indices from ∼8,000 to ∼500 years before present-YBP ([63] and references therein). Domestic crops are more vulnerable than wild ones, crowding promotes crop diseases, and storage systems often fail (estimates suggest that as much as 30% of stored food is lost even in a modern sophisticated system [62]). In other study, based on the molecular analysis of dietary diversity for three archaic Native Americans, Poinar et al. [64] found evidence that, as compared to individuals dependent on agriculture, the diet of hunter-gatherers seems to have been more varied and nutritionally sound. Clearly, a diet based on one or only a few crops should have been deleterious to health in the pre-Columbian era [65]. These different lines of evidence illustrate that the incipient farming niches of Mesoamerica, when communities of hunters/gatherers/foragers started to cultivate and domesticate wild plants, could have been remarkably unstable like those of other pre-industrial societies [6].

Based on what was discussed above, as well as in our results (allele age and neutrality/selection tests), it is reasonable to suppose that ABCA1*230Cys has an American origin and it could have had a selective advantage during the periods of food scarcity experienced by Mesoamericans during the implementation of the sedentary life style based on maize. The strong correlation between maize culture propagation and 230Cys frequencies in this region reinforces this suggestion, even when considering that the advantage of the allele may have been lost after technological innovations had been implemented and agricultural production stabilized. Peng et al. [66] presented evidence for a similar case of gene-culture coevolution, suggesting that positive selection for the ADH1B*47His allele was caused by the emergence and expansion of rice domestication in East Asia.

Noteworthy is that other environmental factors may also have been involved in the distribution of the ABCA1 alleles, since cholesterol plays an important role in various infectious processes, such as the entry and replication of Dengue virus type 2 and flaviviral infection [67]. Additionally, the ABCA1 transporter participates in infectious and/or thrombotic disorders involving vesiculation, since homozygous ABCA1 gene deletions confer complete resistance against cerebral malaria in mice [68], [69]. These findings can be considered as additional causal factors to the ABCA1*230Cys selective sweep associated with agricultural development. A sedentary village lifestyle with a corresponding growth in the density of the local population can promote an increase in the mortality rate, particularly in children under 5 years of age [70]. For example, archeological and paleoecological evidence in Europe showed that during the Neolithic demographic transition, the causes of increased infant mortality would have included a lack of drinking water supplies, contamination by feces, emergence of highly virulent zoonoses, as well as an increase in the prevalences of other germs such as Rotavirus and Coronavirus (causing diarrhea, one of the main killers of children under 5 years of age), Streptococcus, Staphylococcus, Plasmodium (P. falciparum and P. vivax, which are believed to have emerged more recently), and Herpesvirus [70]. However, the real impact of the ABCA1*230Cys variant in these infectious processes will require additional functional studies.

In agreement with this historical scenario, the genetic variation in Arg230Cys presented a worse fit to neutrality than loci known to be neutral, indicating that selective mechanisms are necessary to explain the genetic diversity of Arg230Cys, especially when the Mesoamerican agriculturalist subdivision is considered in the analysis. This result also supports our hypothesis that maize domestication in Mesoamerica lead to changes in the gene pool of the natives from that region.

South America presents much more diversity in relation to habitats, people, and culture than Mesoamerica. For instance, maize arrived in South America, but apparently the level of consumption seen in Mesoamerica/Central America was rarely found there. Archaeological data indicate that only during the implantation and expansion of the Inca Empire (800–500 YBP) was the level of maize consumption important, but the level of consumption was not comparable to that of Mesoamerica/Central America [71][73]. Additionally, South Amerindian hunter-gatherers/foragers present lower intrapopulation genetic variation and higher levels of population structure when compared to those seen in Andean populations [27], [74]. This same tendency was also observed in the present study. These results indicate low levels of gene flow between villages/populations and low effective population sizes, favoring the role of genetic drift. Conversely, the Andean groups show opposing characteristics. These findings correlate well with distinguishing patterns of gene flow and historical effective sizes in these indigenous populations, with cultural differences, as well as with paleoclimatic and environment changes in their habitats [74]. Therefore, the significant role of random processes and/or more heterogeneous cultural and ecological scenarios makes it difficult to define a particular pattern associated with the Arg230Cys polymorphism in South American groups, a situation different from that in Mesoamerica.

In conclusion, our analyses demonstrate for the first time a robust correlation between a constructed niche and a selected Native American autochthonous allele. The 230Cys allele, with a probable origin in America continent, seems have been the target for an ongoing directional selective sweep as a result of the origin and spread of the maize culture in ancient Mesoamerica.

Supporting Information

Figure S1.

Twenty SNPs selected based on their location (chromosome 9: from position 85252250 to 85317359) inside the putative neutral region, defined by Schroeder and colleagues [39], which comprises ∼76,000 bp around the D9S1120 locus.

https://doi.org/10.1371/journal.pone.0038862.s001

(JPG)

Table S1.

Populations included in the selection analyses.

https://doi.org/10.1371/journal.pone.0038862.s002

(DOC)

Table S2.

Allele frequency by region of 20 SNPs located around the D9S1120 locus.

https://doi.org/10.1371/journal.pone.0038862.s003

(DOCX)

Table S3.

Allele frequency by region of 19 SNPs located around the ABCA1*230 locus.

https://doi.org/10.1371/journal.pone.0038862.s004

(DOCX)

Acknowledgments

We are very grateful to the volunteers who contributed in the sampling. We thank M. Villena and R. Vasquez for their assistance in the sample collection in Bolivia, Claiton H. D. Bau for laboratory support, and Rolando González-José, Lavínia Schüler-Faccini, Matthew Nunes, Sidia M. Callegari-Jacques, and Jorge Gomez-Valdez for their comments on the manuscript. We also thank R. Bisso-Machado for his help with editing the tables.

Author Contributions

Conceived and designed the experiments: TH MCB. Performed the experiments: TH VC. Analyzed the data: TH CEGA SA VRPC. Contributed reagents/materials/analysis tools: VAA FR JMD SM RB MTVM FMS SCQ ARL. Wrote the paper: TH FMS MCB.

References

  1. 1. Laland KN, Odling-Smee J, Myles S (2010) How culture shaped the human genome: bringing genetics and the human sciences together. Nat Rev Genet 11: 137–148.KN LalandJ. Odling-SmeeS. Myles2010How culture shaped the human genome: bringing genetics and the human sciences together.Nat Rev Genet11137148
  2. 2. Richerson PJ, Boyd R, Henrich J (2010) Gene-culture coevolution in the age of genomics. Proc Natl Acad Sci USA 107: 8985–8992.PJ RichersonR. BoydJ. Henrich2010Gene-culture coevolution in the age of genomics.Proc Natl Acad Sci USA10789858992
  3. 3. Odling-Smee FJ (1988) Niche construction phenotypes. In: The role of behavior in evolution (ed. H. C. Plotkin), 73–132. Cambridge: MIT Press. FJ Odling-Smee1988Niche construction phenotypes.In: The role of behavior in evolution (ed. H. C. Plotkin), 73–132. Cambridge: MIT Press.
  4. 4. Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Monographs in Population Biology 37. Princeton: Princeton Univ. Press. FJ Odling-SmeeKN LalandMW Feldman2003Niche construction: the neglected process in evolution. Monographs in Population Biology 37. Princeton: Princeton Univ.Press
  5. 5. Gerbault P, Liebert A, Itan Y, Powell A, Currat M, et al. (2011) Evolution of lactase persistence: an example of human niche construction. Philos Trans R Soc Lond B Biol Sci 366: 863–877.P. GerbaultA. LiebertY. ItanA. PowellM. Currat2011Evolution of lactase persistence: an example of human niche construction.Philos Trans R Soc Lond B Biol Sci366863877
  6. 6. Rowley-Conwy P, Layton R (2011) Foraging and farming as niche construction: stable and unstable adaptations. Philos Trans R Soc Lond B Biol Sci 366: 849–862.P. Rowley-ConwyR. Layton2011Foraging and farming as niche construction: stable and unstable adaptations.Philos Trans R Soc Lond B Biol Sci366849862
  7. 7. Holden C, Mace R (1997) Phylogenetic analysis of the evolution of lactose digestion in adults. Hum Biol 69: 605–628.C. HoldenR. Mace1997Phylogenetic analysis of the evolution of lactose digestion in adults.Hum Biol69605628
  8. 8. Bersaglieri T, Sabeti PC, Patterson N, Vanderploeg T, Schaffner S F, et al. (2004) Genetic signatures of strong recent positive selection at the lactase gene. Am J Hum Genet 74: 1111–1120.T. BersaglieriPC SabetiN. PattersonT. VanderploegF. Schaffner S2004Genetic signatures of strong recent positive selection at the lactase gene.Am J Hum Genet7411111120
  9. 9. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4: e72.BF VoightS. KudaravalliX. WenJK Pritchard2006A map of recent positive selection in the human genome.PLoS Biol4e72
  10. 10. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, et al. (2007) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39: 31–40.SA TishkoffFA ReedA. RanciaroBF VoightCC Babbitt2007Convergent adaptation of human lactase persistence in Africa and Europe.Nat Genet393140
  11. 11. Holden C, Mace R (1997) Phylogenetic analysis of the evolution of lactose digestion in adults. Hum Biol 81: 597–619.C. HoldenR. Mace1997Phylogenetic analysis of the evolution of lactose digestion in adults.Hum Biol81597619
  12. 12. Ingram CJ, Mulcare CA, Itan Y, Thomas MG, Swallow DM (2009) Lactose digestion and the evolutionary genetics of lactase persistence. Hum Genet 124: 579–591.CJ IngramCA MulcareY. ItanMG ThomasDM Swallow2009Lactose digestion and the evolutionary genetics of lactase persistence.Hum Genet124579591
  13. 13. Itan Y, Jones BL, Ingram CJ, Swallow DM, Thomas MG (2010) A worldwide correlation of lactase persistence phenotype and genotypes. BMC Evol Biol 10: 36.Y. ItanBL JonesCJ IngramDM SwallowMG Thomas2010A worldwide correlation of lactase persistence phenotype and genotypes.BMC Evol Biol1036
  14. 14. Lewinsky RH, Jensen T G, Møller J, Stensballe A, Olsen J, et al. (2005) T-13910 DNA variant associated with lactase persistence interacts with Oct-1 and stimulates lactase promoter activity in vitro. Hum Mol Genet 14: 3945–3953.RH LewinskyG. Jensen TJ. MøllerA. StensballeJ. Olsen2005T-13910 DNA variant associated with lactase persistence interacts with Oct-1 and stimulates lactase promoter activity in vitro.Hum Mol Genet1439453953
  15. 15. Beja-Pereira A, Luikart G, England PR, Bradley DG, Jann OC, et al. (2003) Gene-culture coevolution between cattle milk protein genes and human lactase genes. Nat Genet 35: 311–313. Erratum in: Nat Genet (2004) 36: 106.A. Beja-PereiraG. LuikartPR EnglandDG BradleyOC Jann2003Gene-culture coevolution between cattle milk protein genes and human lactase genes. Nat Genet 35: 311–313.Erratum in: Nat Genet (2004)36106
  16. 16. Burger J, Kirchner M, Bramanti B, Haak W, Thomas MG (2007) Absence of the lactase-persistence-associated allele in early Neolithic Europeans. Proc Natl Acad Sci U S A 104: 3736–3741.J. BurgerM. KirchnerB. BramantiW. HaakMG Thomas2007Absence of the lactase-persistence-associated allele in early Neolithic Europeans.Proc Natl Acad Sci U S A10437363741
  17. 17. Livingstone FB (1958) Anthropological implications of sickle-cell distribution in West Africa. Am Anthropol 60: 533–562.FB Livingstone1958Anthropological implications of sickle-cell distribution in West Africa.Am Anthropol60533562
  18. 18. Neel JV, Salzano FM (1967) Further studies on the Xavante Indians. X. Some hypotheses-generalizations resulting from these studies. Am J Hum Genet 19: 554–574.JV NeelFM Salzano1967Further studies on the Xavante Indians. X. Some hypotheses-generalizations resulting from these studies.Am J Hum Genet19554574
  19. 19. Hunley KL, Cabana GS, Merriwether DA, Long JC (2007) A formal test of linguistic and genetic coevolution in native Central and South America. Am J Phys Anthropol 132: 622–631.KL HunleyGS CabanaDA MerriwetherJC Long2007A formal test of linguistic and genetic coevolution in native Central and South America.Am J Phys Anthropol132622631
  20. 20. Kemp BM, González-Oliver A, Malhi RS, Monroe C, Schroeder KB, et al. (2010) Evaluating the Farming/Language Dispersal Hypothesis with genetic variation exhibited by populations in the Southwest and Mesoamerica. Proc Natl Acad Sci USA 107: 6759–6764.BM KempA. González-OliverRS MalhiC. MonroeKB Schroeder2010Evaluating the Farming/Language Dispersal Hypothesis with genetic variation exhibited by populations in the Southwest and Mesoamerica.Proc Natl Acad Sci USA10767596764
  21. 21. Tovo-Rodrigues L, Callegari-Jacques SM, Petzl-Erler ML, Tsuneto L, Salzano FM, et al. (2010) Dopamine receptor D4 allele distribution in Amerindians: a reflection of past behavior differences? Am J Phys Anthropol 143: 458–464.L. Tovo-RodriguesSM Callegari-JacquesML Petzl-ErlerL. TsunetoFM Salzano2010Dopamine receptor D4 allele distribution in Amerindians: a reflection of past behavior differences?Am J Phys Anthropol143458464
  22. 22. Acuña-Alonzo V, Flores-Dorantes T, Kruit JK, Villarreal-Molina T, Arellano-Campos O, et al. (2010) A functional ABCA1 gene variant is associated with low HDL-cholesterol levels and shows evidence of positive selection in Native Americans. Hum Mol Genet 19: 2877–2885.V. Acuña-AlonzoT. Flores-DorantesJK KruitT. Villarreal-MolinaO. Arellano-Campos2010A functional ABCA1 gene variant is associated with low HDL-cholesterol levels and shows evidence of positive selection in Native Americans.Hum Mol Genet1928772885
  23. 23. Romero-Hidalgo S, Villarreal-Molina T, González-Barrios JA, Canizales-Quinteros S, Rodríguez-Arellano ME, et al. (2012) Carbohydrate intake modulates the effect of the ABCA1-R230C variant on HDL cholesterol concentrations in premenopausal women. J Nutr 142: 278–283.S. Romero-HidalgoT. Villarreal-MolinaJA González-BarriosS. Canizales-QuinterosME Rodríguez-Arellano2012Carbohydrate intake modulates the effect of the ABCA1-R230C variant on HDL cholesterol concentrations in premenopausal women.J Nutr142278283
  24. 24. Neel JV (1962) Diabetes mellitus: a ‘thrifty’ genotype rendered detrimental by ‘progress’? Am J Hum Genet 14: 353–362.JV Neel1962Diabetes mellitus: a ‘thrifty’ genotype rendered detrimental by ‘progress’?Am J Hum Genet14353362
  25. 25. Bortolini MC, Salzano FM, Bau CH, Layrisse Z, Petzl-Erler ML, et al. (2002) Y-chromosome biallelic polymorphisms and Native American population structure. Ann Hum Genet 66: 255–259.MC BortoliniFM SalzanoCH BauZ. LayrisseML Petzl-Erler2002Y-chromosome biallelic polymorphisms and Native American population structure.Ann Hum Genet66255259
  26. 26. Bortolini MC, Salzano FM, Thomas MG, Stuart S, Nasanen SP, et al. (2003) Y-chromosome evidence for differing ancient demographic histories in the Americas. Am J Hum Genet 73: 524–539.MC BortoliniFM SalzanoMG ThomasS. StuartSP Nasanen2003Y-chromosome evidence for differing ancient demographic histories in the Americas.Am J Hum Genet73524539
  27. 27. Wang S, Lewis CM, Jakobsson M, Ramachandran S, Ray N, et al. (2007) Genetic variation and population structure in Native Americans. PLoS Genet 3: e185.S. WangCM LewisM. JakobssonS. RamachandranN. Ray2007Genetic variation and population structure in Native Americans.PLoS Genet3e185
  28. 28. Mazières S, Guitard E, Crubézy E, Dugoujon JM, Bortolini MC, et al. (2008) Uniparental (mtDNA, Y-chromosome) polymorphisms in French Guiana and two related populations–implications for the region’s colonization. Ann Hum Genet 72: 145–156.S. MazièresE. GuitardE. CrubézyJM DugoujonMC Bortolini2008Uniparental (mtDNA, Y-chromosome) polymorphisms in French Guiana and two related populations–implications for the region’s colonization.Ann Hum Genet72145156
  29. 29. Mazières S, Sevin A, Callegari-Jacques SM, Crubézy E, Larrouy G, et al. (2009) Population genetic dynamics in the French Guiana region. Am J Hum Biol 21: 113–117.S. MazièresA. SevinSM Callegari-JacquesE. CrubézyG. Larrouy2009Population genetic dynamics in the French Guiana region.Am J Hum Biol21113117
  30. 30. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564–567.L. ExcoffierHE Lischer2010Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Mol Ecol Resour10564567
  31. 31. Kimura M, Ohta T (1973) The age of a neutral mutation persisting in a finite population. Genetics 75: 199–212.M. KimuraT. Ohta1973The age of a neutral mutation persisting in a finite population.Genetics75199212
  32. 32. González-José R, Bortolini MC, Santos FR, Bonatto SL (2008) The peopling of America: craniofacial shape variation on a continental scale and its interpretation from an interdisciplinary view. Am J Phys Anthropol 137: 175–187.R. González-JoséMC BortoliniFR SantosSL Bonatto2008The peopling of America: craniofacial shape variation on a continental scale and its interpretation from an interdisciplinary view.Am J Phys Anthropol137175187
  33. 33. Slatkin M, Rannala B (2000) Estimating allele age. Annu Rev Genom Hum Genet 1: 225–249.M. SlatkinB. Rannala2000Estimating allele age.Annu Rev Genom Hum Genet1225249
  34. 34. Rannala B, Reeve JP (2008) Joint Bayesian estimation of mutation location and age using linkage disequilibrium. Pacific Symp Biocomp 8: 526–534.B. RannalaJP Reeve2008Joint Bayesian estimation of mutation location and age using linkage disequilibrium.Pacific Symp Biocomp8526534
  35. 35. Sabeti PC, Reich DE, Higgins JM, Levine HZ, Richter DJ, et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832–837.PC SabetiDE ReichJM HigginsHZ LevineDJ Richter2002Detecting recent positive selection in the human genome from haplotype structure.Nature419832837
  36. 36. Pickrell JK, Coop G, Novembre J, Kudaravalli S, Li JZ, et al. (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Re 19: 826–837.JK PickrellG. CoopJ. NovembreS. KudaravalliJZ Li2009Signals of recent positive selection in a worldwide sample of human populations.Genome Re19826837
  37. 37. Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23: 347–351.L. ExcoffierN. Ray2008Surfing during population expansions promotes genetic revolutions and structuration.Trends Ecol Evol23347351
  38. 38. Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103: 285–298.L. ExcoffierT. HoferM. Foll2009Detecting loci under selection in a hierarchically structured population.Heredity103285298
  39. 39. Schroeder KB, Jakobsson M, Crawford MH, Schurr TG, Boca SM, et al. (2009) Haplotypic background of a private allele at high frequency in the Americas. Mol Biol Evol 26: 995–1016.KB SchroederM. JakobssonMH CrawfordTG SchurrSM Boca2009Haplotypic background of a private allele at high frequency in the Americas.Mol Biol Evol269951016
  40. 40. Hey J (2005) On the number of New World founders: a population genetic portrait of the peopling of the Americas. PLoS Biol 3: e193.J. Hey2005On the number of New World founders: a population genetic portrait of the peopling of the Americas.PLoS Biol3e193
  41. 41. Pavlidis P, Laurent S, Stephan W (2010) msABC: a modification of Hudson’s ms to facilitate ABC analysis. Mol Ecol Res 10: 723–727.P. PavlidisS. LaurentW. Stephan2010msABC: a modification of Hudson’s ms to facilitate ABC analysis.Mol Ecol Res10723727
  42. 42. Hudson RR (2002) Generating samples under a Wright-Fisher neutral model. Bioinformatics 18: 337–338.RR Hudson2002Generating samples under a Wright-Fisher neutral model.Bioinformatics18337338
  43. 43. Wegmann D, Leuenberger C, Neuenschwander S, Excoffier L (2010) ABCtoolbox: a versatile toolkit for approximate Bayesian computations. BMC Bioinformatics 11: 116.D. WegmannC. LeuenbergerS. NeuenschwanderL. Excoffier2010ABCtoolbox: a versatile toolkit for approximate Bayesian computations.BMC Bioinformatics11116
  44. 44. Blake M (2006) Dating the initial spread of Zea mays. In Histories of maize (eds. J. E Staller, R H Tykot, BF Benz), 55–68. San Diego: Academic Press. M. Blake2006Dating the initial spread of Zea mays. In Histories of maize (eds. J. E Staller, R H Tykot, BF Benz), 55–68.San Diego: Academic Press
  45. 45. Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez JG, Buckler E, et al. (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99: 6080–6084.Y. MatsuokaY. VigourouxMM GoodmanJG SanchezE. Buckler2002A single domestication for maize shown by multilocus microsatellite genotyping.Proc Natl Acad Sci USA9960806084
  46. 46. Dull R (2006) The maize revolution: a view from El Salvador. In: Histories of maize (eds. J. E Staller, R H Tykot, B F Benz), 357–363. San Diego: Academic Press. R. Dull2006The maize revolution: a view from El Salvador.In: Histories of maize (eds. J. E Staller, R H Tykot, B F Benz), 357–363. San Diego: Academic Press.
  47. 47. Jaenicke-Després VR, Smith BD (2006) Ancient DNA and the integration of archaeological and genetic approaches to the study of maize domestication. In: Histories of maize (eds. J E Staller, RH Tykot, BF Benz), 83–92. San Diego: Academic Press. VR Jaenicke-DesprésBD Smith2006Ancient DNA and the integration of archaeological and genetic approaches to the study of maize domestication.In: Histories of maize (eds. J E Staller, RH Tykot, BF Benz), 83–92. San Diego: Academic Press.
  48. 48. Lesure RG (2008) The Neolithic demographic transition in Mesoamerica? Larger implications of the strategy of relative chronology. In The Neolithic demographic transition and its consequence (eds. JP Bocquet-Appel, O Bar-Yosef), 107–138. New York: Springer. RG Lesure2008The Neolithic demographic transition in Mesoamerica? Larger implications of the strategy of relative chronology. In The Neolithic demographic transition and its consequence (eds. JP Bocquet-Appel, O Bar-Yosef), 107–138.New York: Springer
  49. 49. Ranere AJ, Piperno DR, Holst I, Dickau R, Iriarte J (2009) The cultural and chronological context of early Holocene maize and squash domestication in the Central Balsas River Valley, Mexico. Proc Natl Acad Sci USA 106: 5014–5018.AJ RanereDR PipernoI. HolstR. DickauJ. Iriarte2009The cultural and chronological context of early Holocene maize and squash domestication in the Central Balsas River Valley, Mexico.Proc Natl Acad Sci USA10650145018
  50. 50. Piperno DR (2007) Late Pleistocene and Holocene environmental history of the Iguala Valley, Central Balsas Watershed of Mexico. Proc Natl Acad Sci USA 104: 11874–11881.DR Piperno2007Late Pleistocene and Holocene environmental history of the Iguala Valley, Central Balsas Watershed of Mexico.Proc Natl Acad Sci USA1041187411881
  51. 51. van Heerwaarden J, Doebley J, Briggs WH, Glaubitz JC, Goodman MM, et al. (2011) Genetic signals of origin, spread, and introgression in a large sample of maize landraces. Proc Natl Acad Sci USA 108: 1088–1092.J. van HeerwaardenJ. DoebleyWH BriggsJC GlaubitzMM Goodman2011Genetic signals of origin, spread, and introgression in a large sample of maize landraces.Proc Natl Acad Sci USA10810881092
  52. 52. Lia VV, Confalonieri VA, Ratto N, Hernández J A, Alzogaray AM, et al. (2007) Microsatellite typing of ancient maize: insights into the history of agriculture in southern South America. Proc Biol Sci 274: 545–554.VV LiaVA ConfalonieriN. RattoA. Hernández JAM Alzogaray2007Microsatellite typing of ancient maize: insights into the history of agriculture in southern South America.Proc Biol Sci274545554
  53. 53. Tian F, Stevens NM, Buckler ES 4th (2009) Tracking footprints of maize domestication and evidence for a massive selective sweep on chromosome 10. Proc Natl Acad Sci USA 106: 9979–9986.Tian F, Stevens NM, Buckler ES 4th2009Tracking footprints of maize domestication and evidence for a massive selective sweep on chromosome 10.Proc Natl Acad Sci USA10699799986
  54. 54. Ding YC, Chi HC, Grady DL, Morishima A, Kidd JR, et al. (2002) Evidence of positive selection acting at the human dopamine receptor D4 gene locus. Proc Natl Acad USA 99: 309–314.YC DingHC ChiDL GradyA. MorishimaJR Kidd2002Evidence of positive selection acting at the human dopamine receptor D4 gene locus.Proc Natl Acad USA99309314
  55. 55. Vargas-Alarcon G, Moscoso J, Martinez-Laso J, Rodriguez-Perez JM, Flores-Dominguez C, et al. (2007) Origin of Mexican Nahuas (Aztecs) according to HLA genes and their relationships with worldwide populations. Mol Immunol 44: 747–755.G. Vargas-AlarconJ. MoscosoJ. Martinez-LasoJM Rodriguez-PerezC. Flores-Dominguez2007Origin of Mexican Nahuas (Aztecs) according to HLA genes and their relationships with worldwide populations.Mol Immunol44747755
  56. 56. González-Martín A, Gorostiza A, Rangel-Villalobos H, Acunha V, Barrot C, et al. (2008) Analyzing the genetic structure of the Tepehua in relation to other neighbouring Mesoamerican populations. A study based on allele frequencies of STR markers. Am J Hum Biol 20: 605–613.A. González-MartínA. GorostizaH. Rangel-VillalobosV. AcunhaC. Barrot2008Analyzing the genetic structure of the Tepehua in relation to other neighbouring Mesoamerican populations. A study based on allele frequencies of STR markers.Am J Hum Biol20605613
  57. 57. Raymond JS, Deboer WR (2006) Maize on the move. In Histories of maize (eds. JE Staller, RH Tykot, BF Benz), 337–341. San Diego: Academic Press. JS RaymondWR Deboer2006Maize on the move. In Histories of maize (eds. JE Staller, RH Tykot, BF Benz), 337–341.San Diego: Academic Press
  58. 58. Chisholm B, Blake M (2006) Diet in prehistoric Soconusco. In Histories of maize (eds. JE Staller, RH Tykot, BF Benz), 161–167. San Diego: Academic Press. B. ChisholmM. Blake2006Diet in prehistoric Soconusco. In Histories of maize (eds. JE Staller, RH Tykot, BF Benz), 161–167.San Diego: Academic Press
  59. 59. Brown CH (2010) The pastoral niche in pre-Hispanic Mesoamerica. In Pre-Columbian foodways: interdisciplinary approaches to food, culture, and markets in ancient Mesoamerica (eds. J Staller, M Carrasco), 273–291. New York: Springer. CH Brown2010The pastoral niche in pre-Hispanic Mesoamerica. In Pre-Columbian foodways: interdisciplinary approaches to food, culture, and markets in ancient Mesoamerica (eds. J Staller, M Carrasco), 273–291.New York: Springer
  60. 60. Benedict FG, Steggerda M (1936) The food of present-day Maya Indians of Yucatan. Washington: Carnegie Institute of Washington. FG BenedictM. Steggerda1936The food of present-day Maya Indians of Yucatan.Washington: Carnegie Institute of Washington
  61. 61. Parsons JR (2010) The pastoral niche in pre-Hispanic Mesoamerica. In Pre-Columbian foodways: interdisciplinary approaches to food, culture, and markets in ancient Mesoamerica (eds. J Staller, M Carrasco), 109–136. New York: Springer. JR Parsons2010The pastoral niche in pre-Hispanic Mesoamerica. In Pre-Columbian foodways: interdisciplinary approaches to food, culture, and markets in ancient Mesoamerica (eds. J Staller, M Carrasco), 109–136.New York: Springer
  62. 62. Cohen NM (2008) Implications of the NDT for worldwide health and mortality in prehistory. In The Neolithic demographic transition and its consequence (eds. JP Bocquet-Appel, O Bar-Yosef), 481–500. New York: Springer. NM Cohen2008Implications of the NDT for worldwide health and mortality in prehistory. In The Neolithic demographic transition and its consequence (eds. JP Bocquet-Appel, O Bar-Yosef), 481–500.New York: Springer
  63. 63. Kennett DJ, Voorhies B, Martorana D (2006) An ecological model for the origins of maize-based food production on the Pacific Coast of Southern Mexico. In Behavioral ecology and the transition to agriculture (eds. DJ Kennett, B Winterhalder), 103–136. Berkeley: University of California Press. DJ KennettB. VoorhiesD. Martorana2006An ecological model for the origins of maize-based food production on the Pacific Coast of Southern Mexico. In Behavioral ecology and the transition to agriculture (eds. DJ Kennett, B Winterhalder), 103–136.Berkeley: University of California Press
  64. 64. Poinar HN, Kuch M, Sobolik KD, Barnes I, Stankiewicz AB, et al. (2001) A molecular analysis of dietary for three archaic Native Americans. Proc Natl Acad USA 98: 4317–4322.HN PoinarM. KuchKD SobolikI. BarnesAB Stankiewicz2001A molecular analysis of dietary for three archaic Native Americans.Proc Natl Acad USA9843174322
  65. 65. Steckel RH, Rose JC, Larsen CS, Walker PL (2002) Skeletal health in the western hemisphere from 4000 B.C. to the present. Evol Anthropol 11: 142–155.RH SteckelJC RoseCS LarsenPL Walker2002Skeletal health in the western hemisphere from 4000 B.C. to the present.Evol Anthropol11142155
  66. 66. Peng Y, Shi H, Qi XB, Xiao CJ, Zhong H, et al. (2010) The ADH1B Arg47His polymorphism in east Asian populations and expansion of rice domestication in history. BMC Evol Biol 20: 10–15.Y. PengH. ShiXB QiCJ XiaoH. Zhong2010The ADH1B Arg47His polymorphism in east Asian populations and expansion of rice domestication in history.BMC Evol Biol201015
  67. 67. Lee CJ, Lin HR, Liao CL, Lin YL (2008) Cholesterol effectively blocks entry of flavivirus. J Virol 82: 6470–6480.CJ LeeHR LinCL LiaoYL Lin2008Cholesterol effectively blocks entry of flavivirus.J Virol8264706480
  68. 68. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31–39.K. SimonsD. Toomre2000Lipid rafts and signal transduction.Nat Rev Mol Cell Biol13139
  69. 69. Combes V, Coltel N, Alibert M, van Eck M, Raymond C, et al. (2005) ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am J Pathol 166: 295–302.V. CombesN. ColtelM. AlibertM. van EckC. Raymond2005ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology.Am J Pathol166295302
  70. 70. Bocquet-Appel JP (2008) Explaining the Neolithic demographic transition. In The Neolithic demographic transition and its consequence (eds. JP Bocquet-Appel, O Bar-Yosef), 35–56. New York: Springer. JP Bocquet-Appel2008Explaining the Neolithic demographic transition. In The Neolithic demographic transition and its consequence (eds. JP Bocquet-Appel, O Bar-Yosef), 35–56.New York: Springer
  71. 71. Zarrillo S, Pearsall DM, Raymond JS, Tisdale MA, Quon DJ (2009) Directly dated starch residues document early formative maize (Zea mays L.) in tropical Ecuador. Proc Natl Acad Sci USA 106: 9979–9986.S. ZarrilloDM PearsallJS RaymondMA TisdaleDJ Quon2009Directly dated starch residues document early formative maize (Zea mays L.) in tropical Ecuador.Proc Natl Acad Sci USA10699799986
  72. 72. Schwarcz HP (2006) Stable carbon isotope analysis and human diet: a synthesis. In Histories of maize (eds. JE Staller, RH Tykot, BF Benz), 315–324. San Diego: Academic Press. HP Schwarcz2006Stable carbon isotope analysis and human diet: a synthesis. In Histories of maize (eds. JE Staller, RH Tykot, BF Benz), 315–324.San Diego: Academic Press
  73. 73. Tykot RH, Burger RL, Van der Merwe N (2006) The importance of maize in initial period and early horizon Peru. In Histories of maize (eds. JE Staller, RH Tykot, BF Benz), 187–233. San Diego: Academic Press. RH TykotRL BurgerN. Van der Merwe2006The importance of maize in initial period and early horizon Peru. In Histories of maize (eds. JE Staller, RH Tykot, BF Benz), 187–233.San Diego: Academic Press
  74. 74. Tarazona-Santos E, Carvalho-Silva DR, Pettener D, Luiselli D, De Stefano GF, et al. (2001) Genetic differentiation in South Amerindians is related to environmental and cultural diversity: evidence from the Y chromosome. Am J Hum Genet 68: 1485–1496.E. Tarazona-SantosDR Carvalho-SilvaD. PettenerD. LuiselliGF De Stefano2001Genetic differentiation in South Amerindians is related to environmental and cultural diversity: evidence from the Y chromosome.Am J Hum Genet6814851496