Plant domestication, a unique opportunity to identify the genetic basis of adaptation

Abstract

Despite the fundamental role of plant domestication in human history and the critical importance of a relatively small number of crop plants to modern societies, we still know little about adaptation under domestication. Here we focus on efforts to identify the genes responsible for adaptation to domestication. We start from a historical perspective, arguing that Darwin's conceptualization of domestication and unconscious selection provides valuable insight into the evolutionary history of crops and also provides a framework to evaluate modern methods used to decipher the genetic mechanisms underlying phenotypic change. We then review these methods, framing the discussion in terms of the phenotype-genotype hierarchy. Top-down approaches, such as quantitative trait locus and linkage disequilibrium mapping, start with a phenotype of interest and use genetic analysis to identify candidate genes. Bottom-up approaches, alternatively, use population genetic analyses to identify potentially adaptive genes and then rely on standard bioinformatics and reverse genetic tools to connect selected genes to a phenotype. We discuss the successes, advantages, and challenges of each, but we conclude that bottom-up approaches to understanding domestication as an adaptive process hold greater promise both for the study of adaptation and as a means to identify genes that contribute to agronomically important traits.

Fig. 1.

Schematic of the phenotype–genotype hierarchy as represented by top-down and bottom-up approaches.

Fig. 2.

Schematic representation of a population bottleneck and its effect on a neutral gene and a selected gene. In Upper, shaded circles represent genetic diversity. The bottleneck reduces diversity in neutral genes, but selection decreases diversity beyond that caused by the bottleneck alone. Lower illustrates sequence haplotypes of these two hypothetical genes. The neutral gene lost several haplotypes through the domestication bottleneck, but the selected gene is left with only one haplotype containing the selected site.

Fig. 3.

Resampling tests to examine empirical ranking methods for finding candidate genes. Left represents sequence data from maize alone; Right demonstrates the difference in statistics between maize and teosinte. The statistics are the number of SNPs (S) (Top), Tajima's D (Middle), and a combination of both (Bottom) (see text). For each graph, the heavy line represents the median number of genes, of ≈800, that are inferred to be under selection. Boxes represent the central 50% of the data, and lines extend out to 3/2 of the interquantile range.