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

Hünemeier, Tábita; Amorim, Carlos Eduardo Guerra; Azevedo, Soledad; Contini, Veronica; Acuña-Alonzo, Víctor; Rothhammer, Francisco; Dugoujon, Jean-Michel; Mazières, Stephane; Barrantes, Ramiro; Villarreal-Molina, María Teresa; Paixão-Côrtes, Vanessa Rodrigues; Salzano, Francisco M.; Canizales-Quinteros, Samuel; Ruiz-Linares, Andres; Bortolini, Maria Cátira

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.