The interplay of demography and selection during maize domestication and expansion

Abstract

The history of maize has been characterized by major demographic events including changes in population size associated with domestication and range expansion as well as gene flow with wild relatives. The interplay between demographic history and selection has shaped diversity across maize populations and genomes. Here, we investigate these processes based on high-depth resequencing data from 31 maize landraces spanning the pre-Columbian distribution of maize as well as four wild progenitor individuals (Zea mays ssp. parviglumis) from the Balsas River Valley in Mexico. Genome-wide demographic analyses reveal that maize domestication and spread resulted in pronounced declines in effective population size due to both a protracted bottleneck and serial founder effects, while, concurrently, parviglumis experienced population growth. The cost of maize domestication and spread was an increase in deleterious alleles in the domesticate relative to its wild progenitor. This cost is particularly pronounced in Andean maize, which appears to have experienced a more dramatic founder event when compared to other maize populations. Introgression from the wild teosinte Zea mays ssp. mexicana into maize in the highlands of Mexico and Guatemala is found found to decrease the prevalence of deleterious alleles, likely due to the higher long-term effective population size of wild maize. These findings underscore the strong interaction between historical demography and the efficiency of selection species-and genome-wide and suggest domesticated species with well-characterized histories may be particularly useful for understanding this interplay.

Adaptive introgression: an untapped evolutionary mechanism for crop adaptation

“…Since wild species are expected to have a lower genetic load than cultivated species, spontaneous introgression from wild species could be favored, because it alleviates the domestication cost, even in the absence of strong directional selection on the introgressed alleles. Recent findings in maize support this expectation, as negative correlations were observed between wild introgression and genetic load (Wang et al 2017).…”

“…Regarding the introduction or re-introduction of adaptive variation, it might be wondered to what extent introgression from wild relatives can affect the whole crop genome. Recent studies have suggested that introgression can be favored at genome-wide level when it reduces the genetic load of the recipient species (Sankararaman et al, 2014; Wang et al, 2017). Genetic load refers to the genome-wide accumulation of weakly deleterious alleles that reduces its fitness (Crow, 1958).…”

“…In crops, a reduction in fitness is expected compared to the wild progenitor, the so-called ‘cost of domestication’ (Lu et al, 2006). A greater genetic load than in the wild counterpart was observed in several domesticated species such as rice (Lu et al, 2006), maize (Wang et al, 2017), sunflower (Renaut and Rieseberg, 2015), dogs (Marsden et al, 2016) and horses (Schubert et al, 2014). Since wild species are expected to have a lower genetic load than cultivated species, spontaneous introgression from wild species could be favored, because it alleviates the domestication cost, even in the absence of strong directional selection on the introgressed alleles.…”

The extent of adaptive wild introgression in crops

“…Wang et al . () employed the ABBA‐BABA and statistics to evaluate if maize with mexicana introgression was transferred to other highland regions or whether highland adaptation was obtained de novo outside of Mexico. Overall, analyses revealed that mexicana introgression was pervasive in maize from Mesoamerican high‐elevation regions (the highlands of Mexico, Guatemala, and the southwestern United States), but that more distant high‐elevation regions (e.g.…”

“…Plant domestication is often conceptualized as a geographically constrained process, with crops originating from a wild progenitor within defined centers followed by expansion to the modern‐day range of cultivation (Harlan, ). However, archaeological and genetic evidence is beginning to reveal that, in many cases, domestication has been temporally protracted and geographically diffuse (Fuller et al ., ; Meyer et al ., ; Wang et al ., ). An additional aspect of the emerging complexity of domestication is the occurrence of beneficial gene flow from locally adapted wild relatives to crops during their expansion following domestication.…”